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Home , Acalypha, Acalypha indica, Cnesmone, Cyathium, Dalechampia, Euphorbiaceae

Amer. J. Bot. 59(6): 573-586. 1972.

THE MORPHOLOGY AND RELATIONSHIPS OF SCANDENS ()1

GRADY L. WEBSTER AND BARBARA D. WEBSTER Departmentof Botanyand Departmentof Agronomyand Range Science, Universityof California,Davis

A B S T R A C T The circumtropicalbut preponderantlyAmerican Dalechampia, comprisingnearly 100 speciesof twiningvines (or rarelysubshrubs), is strikinglyisolated within the Euphorbiaceae because of its distinctivebibracteate . There has been considerabletaxonomic controversywith regardto the relationshipsof the genus, and it has been suggestedthat Dalechampia is allied to the tribeEuphorbieae because of a supposed analogy betweenits inflorescenceand the cyathiumin the . Field and laboratoryinvestigations of the commonAmerican D. scandens,together with a comparativesurvey of related species,have thrownsome lighton these problems. The Dalechampia inflorescenceseems best interpretedas consistingof a terminalstaminate pleiochasium (with part of the lateral branchestransformed for nectarproduction), juxtaposed to a 3-floweredpistillate cyme. The lips of the conspicuousbilabiate involucre are formedby the hypertrophiedbracts which sub- tend the staminateand pistillatecymes. The bisexual inflorescencesappear to be distinctly proterogynous,rather than proterandrous, as has been previouslysuggested. The configuration of the -abilaterally symmetrical pseudanthium-suggests adaptation for cross- pollination,but the closing movementof the bractsmakes self-pollinationprobable in the absenceof visitsby pollinators.The similarityof theDalechampia inflorescence to thecyathium of the Euphorbieaeappears to be entirelysuperficial, and both reproductiveand vegetative data suggestthat Dalechampia is relatedto taxa of tribePlukenetieae.

DALECHAMPIA IS A GENUS of Euphorbiaceae so withother taxa of Euphorbiaceaehave been con- isolated and sharplydelimited that it has usually troversial.Mueller (1866) placed the tribeDale- been placed in a distinctmonogeneric since champieae adjacent to the Euphorbieae. He thus the originaldisposition of Mueller (1864). Ac- adoptedan interpretationsimilar to thatof Jussieu cordingto Pax and Hoffmann(1931), the genus (1824), who referredDalechampia to his Sectio comprisesabout 100 tropical species, of which VI along withAnthostema, , and Pedi- over three-fourthsare American;probably half of lanthus. Baillon (1858), on the otherhand, re- the species in the genus occur withinthe bound- jectedthis disposition (though partly for the wrong aries of Brazil. Most of the common species of reasons, since he regardedthe cyathiumof Eu- Dalechampia are herbaceous twiningvines, but phorbiaas a hermaphroditicflower) and indicated some of the Brazilian ones are suffrutescent,and an affinityof Dalechampia to .Bentham one of these-D. spathulata-is commonlyculti- (1878, 1880) went so far as to include Dale- vated in greenhousesbecause of its attractivered- champiain the subtribePlukenetiinae, adjacent to dish inflorescences. and . Pax (1890) at firstmade The systematicproblems facing the studentof the same dispositionas Bentham,but later (Pax Dalechampia are somewhatdifferent from those and Hoffmann, 1919, 1931) removed Dale- usually encounteredin the Euphorbiaceae,where champia to a separate tribe without,however, the major difficultylies in definingand discrimi- negatingthe relationshipto the Plukenetieae(here nating among taxa. Dalechampia is so sharply treated as a tribe in accord with Hutchinson, differentiatedfrom other Euphorbiaceous taxa and 1969). at the same time so relativelyhomogeneous at More recentlyCroizat (1940, 1942) has re- the infragenericlevel thatits genericintegrity has turnedto the originalhypothesis of Jussieu(1824) never been seriouslydoubted. Preciselybecause and has attemptedto derive the cyathiumof of its isolated position,however, its relationships Euphorbiafrom the Dalechampia inflorescence via 1 Receivedfor publication2 September1971. the zygomorphiccyathium of Pedilanthus. How- The authorsare pleased to acknowledgethe assistance ever, in his monographof Pedilanthus,Dressler of Dr. Kim I. Miller,Mr. Bryce Christman,and Miss (1957) has remarkedthat there is no evidenceto Mary Craig in the preparationof this paper. Part of the researchwas supportedby grantsfrom the National supportthis theory. Hurusawa (1954), on the Science Foundation. otherhand, has followedCroizat in placingDale- 573

This content downloaded from 169.237.8.35 on Mon, 16 Sep 2013 16:48:05 PM All use subject to JSTOR Terms and Conditions 574 AMERICAN JOURNAL OF BOTANY [Vol. 59 champia adjacent to the Euphorbieaeand Antho- relativelyancient one, and not the resultof recent stemeae. long-distancedispersal. At any rate, it should be The interpretationof the Dalechampia inflores- kept in mind that the discussionsin this paper cence is of considerable systematicimportance, apply only to the NorthAmerican populations of since it may affectnot only the placementof this D. scandens and do not take into account varia- genusbut the tribal arrangements within the tions which mightoccur in the South American as a whole. There are furthermoresome purely or Africanplants. morphologicalproblems with regard to the in- florescencewhich need to be settledbefore mak- MATERIALS AND METHODS-Living of ing a systematicjudgment. Urban (1888) took Dalechampia were studiedin the greenhousesat issue with the interpretationof Baillon (1858) the Universityof California,Davis, and at Purdue that the secretoryscales of the male part of the University,Lafayette, Indiana. Wild populations inflorescencerepresent modified of sterile were observedin Mexico, Nicaragua, and in the cyme-branches.Because therewere no bractsas- West Indies. sociatedwith the male flowersin the inflorescence Anatomicalpreparations were made fromma- of D. spathulata2which he investigated,Urban terialfixed in FAA (fornLalin,acetic acid, alcohol), proposed that the scales representedmodified dehydratedthrough the standard TBA (tertiary . Michaelis (1924), on the basis of a butylalcohol) series,embedded in paraffin,and surveyof a largenumber of species,disagreed and stained followingthe usual safranin-fastgreen returnedto an interpretationcloser to that of technique(Jensen, 1962). Baillon. Macrophotographswere taken with polaroid Aside fromthe intrinsicallyinteresting features film,using an Aristophotapparatus. Photomicro- of this curious genus,we wish to contributeto a graphsof sectionedmaterial were also takenwith better understandingof its relationshipsby re- polaroidfilm, using a Zeiss photomicroscope.The investigatingits morphologywith particularem- photographsof pollen and trichomeswere made phasis on inflorescenceand floral structure. with a CambridgeStereoscan Microscope; speci- Relativelyfew species of Dalechampia are found mens were treatedwith gold shadowing. in cultivation,and theonly detailed morphological Voucherspecimens of Dalechampia plantshave analysis of the genus (Michaelis, 1924) omits been deposited in the Department of Botany considerationof most structuresother than the Herbarium,University of California,Davis. inflorescence.It thus appears sound strategyto The terminologyused here is that of Webster thoroughlydefine the structureand morphological (1968), where a detailed taxonomicdescription variationswithin a singlespecies. may be found. The species consideredhere, D. scandens,pre- sentsa unique problemsince it is the only species RESULTS-Growthand phyllotaxy-Dalecham- in the genus listedas nativeto both America and pia scandens,like the otherspecies of sect. Scan- (Pax and Hoffmann,1919). It is notclear dentes (Pax and Hoffmann,1919), is an herba- whethertheir dispositionwill stand the test of ceous, twiningvine which in natureeither climbs contemporaryinvestigations, but the apparent or sprawlsalong the ground. The aerial portion presenceof distinctendemic races in both South of the is composed of twininglong-shoots America and Africa suggests a natural trans- which come off the suffruticosebase and which Atlantic occurrence of D. scandens. Leandri may die back duringunfavorable seasons. The (1943), for example,has recognizedD. scandens characteristically3-lobed are borne on the as nativeto Madagascar,and has pointedout close monopodiallong-shoots in a spiral arrangement; affinitiesbetween it and some of the endemic each on the long-shootmay subtenda short- Malagasian species. Leonard (1962) appears to shoot,which terminates in an inflorescence(Fig. accept some African forms of Dalechampia as 1). Each short-shootmay produce a single in- belongingto D. scandens. It is possible, there- florescencesubtended by a "rameal" leaf smaller fore, that the distributionof D. scandens is a than thatfound on the long-shoot.On the other hand, the rameal leaf may subtenda second in- 2 Urban used the name D. roezliana Muell. Arg. for volucre with its own subtendingrameal leaf. thisplant, and the same name has been appliedin more Technically,the inflorescencesshould perhapsbe recentpapers by Michaelisand VenkataRao, despitethe fact that Pax and Hoffmann(1919) have relegatedD. termedpseudoterminal, since there is nearly al- roezliana to synonymyunder D. spathulata (Scheidw.) ways a bud in the axil of the firstrameal leaf, and Baill. thisprobably represents the terminalbud. Unlike

Fig. 1-4. Habit of Dalechampiascandens.-Fig. 1. Portionof long-shoot,with axillaryshort-shoot bearing an inflorescenceand small rameal leaf. X 0.8.-Fig. 2. Short-shootwith two expandedinflorescences and anotherin bud. X 1.-Fig. 3. Tip of short-shootwith one inflorescencein anthesis,the otherin bud. X 1.3.-Fig. 4. Frontal view of expandedinflorescence, with male flowersbeginning to open. X 2.

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the long-shoot,the short-shootis determinatewould appear to conformto the inflorescence underordinary conditions, and thegrowth of the patternof themajority of species. shootsystem as a wholeis carriedon by long- In D. scandensa secondaryfertile shoot some- shootbuds whichoccur in thesame axils as the timesgrows from a bud in theaxil of the single short-shoots.Rarely, the short-shoot may produce ramealleaf; the involucre produced by thisshoot threepseudanthia (Fig. 2), or (especiallyfollow- is mostoften smaller than the "primary" one (Fig. ing woundingor removalof the long-shoottip) 2). The same relationshipappears to hold in may grow out into a long-shoot.Most other manyother species, so thatmeasurements of in- speciesof Dalechampiaappear to be similarin volucresmust be madewith this difference inmind. possessingaxillary determinate short-shoots, and The leaves of D. scandensare somewhatless manyof these (e.g., D. triphylla,D. dioscoreifolia)polymorphic, both in the same and in different have onlya singleprimary inflorescence on the individuals,than those of many other species. The short-shootsubtended by a singleleaf. The wide- leaves are long-petiolateand mostlydeeply 3- spreadD. tiliifoliaonly diverges insofar as it usu- lobed, witha characteristicallyprominent retic- allyproduces two leaves on theshort-shoot below ulumbeneath. In plantsobserved in the green- the involucre(Webster, 1968, Fig. 18). Some- house,there is a definitetendency for ontogenetic timesthe single leaf on thefertile shoot is reduced foliarmodification: the lowermostleaves are 3- to a scale and the subtendingnode is shortened,lobed, but the two laterallobes of thoseleaves so thatthe involucre then may appear to be simply producedtowards the tip of thevine become pro- axillary.This is true,for example, in the culti- gressivelyindented until the distal leaf blades are vatedD. spathulata.On theother hand, in some essentially5-lobed (Fig. 5). of the smallsuffrutescent Brazilian species, such In other species leaf dimorphismor poly- as D. caperonioides,the involucre may terminate morphism is muchmore marked,but it is not an uprightbranch with 3-5 leavesor more. It is alwayseasy to observethe patternfrom frag- difficultto suggestwhat the original condition may mentaryherbarium specimens. In thecommon D. havebeen in the genus, but at anyrate D. scandens tiliifoliathe first (lower) ramealleaf of the fertile

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short-shootis commonlyentire and unlobed,while togenyof stinginghairs in the two generastrongly theupper leaf is distinctly3-lobed (Webster, 1968, suggestsphylogenetic affinity between the tribe Fig. 18). Both lobed and unlobed leaves occur Plukenetieaeand the tribeDalechampieae. on thelong-shoots of D. tiliifoliaas well,and their distributionappears at least in part to be onto- Inflorescence-In Dalechampia the inflores- geneticallydetermined (lowermost blades being cence is a bilaterallysymmetrical pseudanthium of entire). a configurationunique withinthe Euphorbiaceae. This ontogeneticcomponent of leaf variation The inflorescencein most formsof D. scandens has some ratherdisturbing taxonomic implications, is conspicuousbecause of the two large, creamy- because Pax and Hoffmann(1919) have separated white,3-lobed bractswhich subtend the staminate species in both sect. Triphyllaeand sect. Scan- and pistillatecymes (Fig. 4). The two bractsare dentes on the basis of whetherthe leaves are attachedat slightlydifferent levels (althoughthey dimorphicor not. This is a poor "key" character, appear oppositeon cursoryinspection), the lower because individualspecimens of a putativelydi- one subtendingthe pistillate,and the upper one, morphicspecies may not necessarilyshow both the staminateinflorescence. Since thepeduncle of kindsof leaves. Furthermore,supposedly "mono- the inflorescenceis orientedmore or less upward, morphic"species withlobed or partedleaves may themale flowerslie above but closelyappressed to occasionallyhave entireones. It would appear, the femaleflowers (Fig. 3, 4, 10, 20). therefore,that the position of leaf types on the In certainrespects the Dalechampia pseudan- plant, and (wheneverpossible) a statisticalesti- thiummay be referableto the class of "flag blos- mate of their frequencyshould be included in soms" recognized by Faegri and van der Pijl futuresystematic descriptions. (1966), since the reproductiveorgans are posi- tioned so that an approachinginsect would have Indumentum-The leaves and stems of D. to receivepollen on the ventralsurface if cross- scandens have a pubescence of unicellularhairs pollinationwere to occur. Unfortunately,no de- whichin scanningelectron micrographs (at mag- tailedobservations have yetbeen reportedof insect nificationsof 500 x or more) clearly appear visitsin the field,so thatreasoning about function spirallytwisted (Fig. 7). Interspersedwith these mustremain inferential. relativelylong hairs are much shorterones of a verypeculiar structure:a centralcell armed with Involucre-The involucresof the inflorescences a sharp-pointedcrystal, surrounded by several become evidentnear the stem tip as apparently epidermal jacket-cells (Fig. 8). Knoll (1905) axillarybuds at a stage when the stipulesof the showed that the centralcell of these remarkable subtendingleaf are stilllonger than its blade. In trichomesrepresents a highly modified subepi- the youngeststages the stipulesof bothleaves and dermalcrystalliferous cell in whichthe outerperi- involucralbracts are erect and longer than the clinal wall protrudesbeyond the epidermallayer, blades, but theysoon become recurved(Fig. 6). and one arm of the druse crystalhypertrophies In greenhousematerial of D. scandens, the in- into a long, sharp "hypodermicneedle." These volucral bractsturn whitish by the time theyare crystal-armedhairs appear to functionin a similar 5 mm long, so theyare easily discerned. mannerto those of Tragia (Knoll, 1905; Miller Typically,involucres require 2 weeks to attain and Webster,1967), and the hairs of the latter fullsize (2.5-3 cm long). At firstthe bractsare genusare strikinglysimilar to thoseof D. scandens tightlyappressed, but the involucrebegins to open (Fig. 9). Althoughthe of Dalechampia when the bractsare about 1.5-2 cm long; within do not cause the immediateburning sensation 2 or 3 days afterthat stage, the bractsdiverge to characteristicof Tragia hairs, theycan definitely an angle of 90-120? (Fig. 10, 11). Pax and Hoff- be quite irritatingto the skin. The generally mann (1919) reportedthat Dalechampia inflores- smaller size of the hairs of Dalechampia may cences are stronglyproterandrous, but this does perhapsaccount for their lesser degree of noxious- not seemto be trueof our materialof D. scandens. ness as comparedwith Tragia. The male flowerstypically remain closed for at As remarkedby both Rittershausen(1892) and least one day afterthe bractsare fullyopen and Knoll (1905), the similarityof these"Brennhaare" divergent;during this time the inflorescenceap- of Tragia and Dalechampia appears to be taxo- pears to be functionallyproterogynous (Fig. 10, nomicallysignificant. The similarform and on- 12). By the time the firstthree or four male

Fig. 10-13. Inflorescencesof D. scandens.-Fig. 10. Inflorescenceshowing proterogynous condition; B, ; S, stipuleof bract;G, staminate"gland"; M, male flowers;F, femaleflowers. X 3.3.-Fig. 11. Older inflorescence withmale flowersdehiscing and femalecalyx lobes becomingbristly. X 2.-Fig. 12. Inflorescencewith lower in- volucralbract removed, exposing abaxial bractletof pistillatecymule. X 2.7.-Fig. 13. Inflorescencewith lower involucralbract removed and pistillatecymule turned back to exposepeduncle of staminateinvolucel. X 2.5.

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This content downloaded from 169.237.8.35 on Mon, 16 Sep 2013 16:48:05 PM All use subject to JSTOR Terms and Conditions 580 AMERICAN JOURNAL OF BOTANY [Vol.59 flowersopen, thebracts are alreadyturning green- species, such as the common D. tiliifolia,the ish and startingto reclose. bracts are similarlycolored (white or creamy- The two involucralbracts of D. scandens have white) but less deeplylobed. Otherspecies, such a verycharacteristic shape, the threelobes being as D. spathulata, have brilliantred or yellow cut about halfwayto the base (Fig. 4). As in bracts (the color apparentlyvaries in different mostother species, the bracts are palmatelyveined, races). One ratherconspicuous neotropical spe- with five (or sometimesseven) veins departing cies, D. dioscoreifolia,has strikingpink bracts fromthe cordate base. In most plants observed with dark, reddishveins and a lacerate margin. in cultivationand in the field, the bracts attain Other species have bracts that are greenish. It a brilliantsnow-white or creamy-whitecolor at would be temptingto assume bird pollinationin peak anthesisof theinflorescence; but they quickly someof thespecies with red-bracted inflorescences, begin to turn greenishafter divergenceexceeds but in fact, almost nothingis known about pol- 90, and withinabout one week afteropening, linatingagents. theyhave reclosedand becomeleaf-green in color. Involucresproduced late in the growingseason, Pistillateinflorescence-The pistillateinflores- or on depauperateplants, may have smallerbracts cence is insertedaxillary to the lower of the two which become at most yellowish-greenat full involucralbracts and terminatesan extremelyab- anthesis. breviatedaxillary shoot (Fig. 12, 13). The pistil- Due to the remarkableadhesiveness of the mu- late cymeordinarily consists of two lateralsessile cilage produced withinthe staminateinvolucel, or short-pedicellateflowers flanking a single the staminateinflorescence adheres to the sub- central which eventuallybecomes long- tendingbracts when it breaks off beforethe in- pedicellate (Fig. 18). The apetalous flowersare volucre closes. This appears to be an effective subtendedby a broad abaxial bractand two rather way of promotingself-pollination, particularly smalleradaxial bracts which are, however,often since several male flowersdo not dehisce until fused into one. These three structuresperhaps shortlybefore closure of the involucre. Experi- representthe basal bractof the cymeplus the two mental crosses suggest that the plants could be bracteolessubtending the two lateralflowers (Fig. self-compatible,since involucresbagged before 16). dehiscenceof the male flowersproduce normal- At anthesisthe three female flowersare still appearing capsules. Unfortunately,in the few nearlysessile and have conspicuousglandular tips crosses made, no viable seeds were obtained,so on thelobes of thecalyx (Fig. 17). In laterstages that the possibilityof self-incompatibilitycannot the calyx lobes elongateand become prominently be excludeduntil further testing is done. bristlywith hypodermichairs, while the pedicel The sequence of changes in color and position may become distinctlyelongated (especially that of the bracts during inflorescencedevelopment of the centralflower) (Fig. 18). The position reflectssuccessive adaptation to (1) protection of the expanded stigmasof the flowersis such of flowers (before anthesis); (2) attractionof thatpollination can be effectedsoon afteropening pollinators(at anthesis); and (3) protectionof of the involucreand before anthesisof the first capsules (afteranthesis). However, in greenhouse- male flower. The average lengthof the stylesat grownplants the timing appears far from optimum, anthesisis between 5 and 6 mm, but in other at least in relationto pollination. The bractsor- species (such as D. pentaphylla)the styleselon- dinarilyremain white for only 1 or 2 days,mainly gate to 15 or 20 mm. duringthe timewhen only the femaleflowers are receptive;they are almost always beginningto Female flower-The female flower of Dale- turn green by the time that most of the male champiais relativelysterotyped. There are always flowershave opened. The timingof the male threecarpels which are almost completelyunited flowers,with only a minorityattaining anthesis to the tip of the compoundstyle. The stigmais duringthe most colorful phase ofthe inflorescence, enlargedinto a peltate structurein D. scandens suggeststhat the Dalechampia pseudanthium,like and many other species; the stigmaticstructure many other blossoms,is adapted for both cross- suggeststhat in some of thespecies of Pera (which, pollinationinitially and self-pollinationlater. however,show littlegynoecial similarity in most The involucralbracts in other taxa of Dale- other aspects). The calyx consistsof a variable champia show a numberof divergences.In many numberof segments,usually 8-12, which in D.

Fig. 14-19. Flowers and fruitsof D. scandens.-Fig. 14. Abaxial view of staminateinflorescence with central male floweropen. X 7.5.-Fig. 15. Male flower,arrow indicating articulation in the pedicel. x 9.-Fig. 16. Pistil- late cymulewith adaxial bractletsturned back to exposecalyces of thefemale flowers. X 6.-Fig. 17. Female flower at anthesis.X 10.-Fig. 18. Pistillatecymule after abscission of involucralbracts, showing development of fromtwo of the threefemale flowers. X 3.2.-Fig. 19. Fruitwith persistent female calyx. X 5.

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Fig. 20-23. Sectionsof inflorescencesand flowersof D. scandens. Fig. 20. Cross sectionof infloresencein bud, showingfollowing structures from top to bottom:upper involucralbract; abaxial lip of staminateinvolucel; sterilebractlets of staminate"gland"; male flowers;adaxial lip of staminateinvolucel; female flowers; abaxial pistil- late bractlet;lower involucralbract. X 8.-Fig. 21. Cross sectionof staminateinflorescence: S1, abaxial lip of staminateinvolucel; S2, adaxial lip of staminateinvolucel. X 10. Fig. 22. Longitudinalsection of male flower.x 25. -Fig. 23. Longitudinalsection of ,ovule (with thickenedinner integument) in sagittalsection: N, nucellar beak; 0, obturator.x 65.

scandensare prominentlylobed. Duringdevelop- hairs of Dalechampia. The fruitand seeds of mentof the ,the calyxlobes elongateand Dalechampiaare also suggestivelysimilar to those becomequite bristly with stinging hairs (Fig. 19). of certainspecies of Tragia,e.g., to theAfrican Theovule of D. scandensis anatropousand sub- T. involucrata. globose,with a narrowconical nucellusand a ratherhighly thickened inner integument, which Staminate inflorescence-The staminateinflo- is shorterthan the outerintegument (Fig. 23). rescenceterminates the axis of the fertileshoot The thincap-like obturator is closelyappressed in D. scandensand is separatedfrom the pistillate to themicropyle in lid-likefashion. As shownby dichasiumby a distinctinternode (Fig. 13). This Singhand Pal (1968), theovules in D. spathulata "peduncle"may in someother species become ex- are verysimilar. The entireconfiguration of the tremelyelongated, as in D. chlorocephalaof ovule is so extraordinarilylike that of Tragia Madagascar(Leandri, 1943). In D. scandensthe urticifolia(Miller, 1964; Miller and Webster, staminateinvolucel is 2-lippedand transversely 1967) thatit is difficultto attributethe similarity elongated, so thatthere appear to be two fused to anythingother than a phylogeneticrelationship. bracts (Fig. 13, 14, 21). In D. spathulata,how- The onlyimportant gynoecial differences between ever, thereare clearlytwo pairs of decussate thetwo genera appear to be themore completely bracts. The observationsof Michaelis(1924) fusedstyles and much smallerovarial stingingindicate that four or fiveis thebasic numberof

This content downloaded from 169.237.8.35 on Mon, 16 Sep 2013 16:48:05 PM All use subject to JSTOR Terms and Conditions July,1972] WEBSTER AND WEBSTER-MORPHOLOGY OF DALECHAMPIA 583 involucel bracts in the genus and that the male interpretationhas recentlybeen advancedby Ven- bractletshave undergonea great deal of fusion kata Rao (1971). As shown in cross sections in D. scandens. (Fig. 20, 21) the scales appear definitelyfoliar, The dispositionof organs withinthe staminate and we thereforeagree with the view of Baillon involucel is unusual and has given rise to con- and Michaelis thatthe scales of the staminatein- siderable controversy.In D. scandens there are florescenceof D. scandens representbractlets of nine or ten male flowersarranged almost in a the male flowers. single plane on the side toward the female di- The functionof the glandularmass in the stam- chasium; on the ab-femaleside there is a large inate inflorescenceof D. scandens is not entirely "gland" composed of flange-likestructures (evi- clear. Muller (1879) reportedthat in a Brazilian dentlymodified bractlets) with secretoryepithe- species the "waxy" secretionof the male "gland" lium (Fig. 10, 14, 20). Close inspectionindicates was collectedby carpenterbees and used fornest thatsome of thesebractlets face the male flowers, building.On theother hand, as notedby Michaelis but a greaternumber face away, towardthe upper (1924), the filiformprocesses in the "gland" of bract (Fig. 21). The bractletsbegin to secrete D. spathulatado not produce an especiallysticky stickymaterial before the firstmale flowersopen, secretion.Since D. spathulatahas red bractsand and the secretionis conspicuousat full anthesis. is possibly bird-pollinated,the differencein Eventuallyafter its "peduncle" disarticulates,the glandularsecretion is not unexpected. staminateinflorescence adheres to theupper bract. Since at this time the bracts are reclosing,the Male flower-The male flowersin the Dale- effectis to bring the male flowersclose to the champia inflorescenceare relativelyconspicuous stigmasand to make self-pollinationhighly prob- because of the ball-likeheads of antherslined up able. underneaththe nectariferousmass (Fig. 4, 13). Althoughthe male flowersappear to be aligned The flower pedicel is nearly always articulated approximatelyin one plane (Fig. 13, 14) it is (Fig. 15), althoughthe stoutpedicels of D. scan- clear fromserial microscopicsections that there dens do not show the articulationas clearly as is a singleterminal male flowerand thatthe male congenerssuch as D. tiliifoliaand D. cissifolia.The clusteris reallya pleiochasiumwith the threead- calyx splits open into four valvate lobes in D. axial arms developed (Fig. 20, 21). The studies scandens (oftenfive or six in otherspecies); these of Michaelis (1924) suggestthat the male pleio- segmentsbecome reflexedand thus expose the chasiumin Dalechampia originallyhad five radi- anthersto best advantage. The stamenshave the ating branches; in D. scandens the two missing filamentsconnate along most of theirlengths into branches are representedby the two rows of a stoutishcolumn, with about 25-35 bilocular glandularbractlets facing toward the abaxial side longitudinallydehiscent anthers in most popula- of the staminateinvolucel (S1 in Fig. 21). The tions of D. scandens (Fig. 22). central dichasium (with a pair of male flowers next to S2 in Fig. 21) develops later than the Pollen-The pollengrains of Dalechampia (Fig. othertwo, but eventuallyall of the male flowers 25), which have been described and illustrated in the inflorescenceare in anthesisconcurrently. by Punt (1962), are very distinctiveand unlike Thereis considerablevariation within D. scandens those of any other genus of Euphorbiaceae. In in developmentof the lateral axes of the pleio- the five species investigatedby Punt, the tricol- chasium.Some axes maydevelop only two flowers, porate pollen grains are characterizedby their so that the total numberof male flowersmay be relativelylarge size (57-105, long), ellipsoidal onlyeight or nine insteadof ten. In otherspecies shape, shortcolpi (extending1/2-2/3 the length there may be additional pleiochasial arms: D. of thegrain), and especiallyby thevery prominent micranthamay produce four lateral axes with a reliefof the exine: the walls (muri) of the reticu- total of 13 flowers,whereas D. leandriimay pro- lum are more prominentthan in any other Eu- duce a dichasium with a total of only seven phorbiaceousgenus. A featurescarcely evident flowers. in scanning electron micrographsbut strikingly Urban (1888) regardedthe fringedbractlets of visible in microscopic observationswith phase D. spathulata as abnormallydeveloped flowers, contrastis the equatorial belt apparentlyformed partlyon the groundsthat since there were no by confluenceof the transverselyelongated germ bractletsassociated with the male flowers,the pores; the cytoplasmof the pollen grainis equa- rest of the organs withinthe involucelshould be toriallyconstricted along thisbelt in a configura- regardedas flowersalso. Hutchinson(1969) has tion somewhatsuggestive of a desmidcell. recently upheld this interpretation.Michaelis In our materialof D. scandens (mounted in (1924), on the other hand, has criticizedthis Hoyer's medium), the pollen grainsmeasure ap- viewpointand has espoused the originalview of proximately75-85/A in length,definitely smaller Baillon (1858) thatthe scales representbractlets than the 1051, reportedby Punt. Pollen grains of sterile proliferatedmale dichasia. A similar examinedunder the scanning microscope appeared

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Fig. 24-25. Scanningelectron micrographs of pollen grains.X 1650.-Fig. 24. .-Fig. 25. Dalechampiascandens. stillsmaller (less than70 /Along). Possiblythere valvesof the cocci and the seeds tendto be re- mayprove to be considerablevariation in pollen tainedwithin the bristly calyx lobes and themore sizewhen larger samples are studied. or less closedinvolucre. The roundishseeds are In viewof theconsiderable similarity between not especiallydistinctive and are similarin most Dalechampiaand Tragiain certainvegetative and relatedspecies exceptfor size. Developmental reproductivefeatures, it is remarkablethat the stagesof seed maturationin D. scandensclosely pollengrains of thetwo genera are so dissimilar.follow those demonstratedin D. spathulataby The grainsof Tragia(Fig. 24) areusually smaller Singhand Pal (1968). No informationis avail- (17-30u across) and are oblatein shape. Each able concerningseed dispersal,but thelack of a colpushas a prominentoperculum, and theexine distinctcaruncle suggests that the myrmecophilous is nearlysmooth (covered with 'nanospinules' a dispersalfound in manyother Euphorbiaceae may fractionof a micronhigh). However,it seems be absentin Dalechampia. probablethat this great pollen difference is cor- relatedin someway with the specialization of the DISCUSSION-Dalechampia is not only a very inflorescencein Dalechampiaand the attendantisolated genus of Euphorbiaceae, but it also shows functionalshifts with regard to pollinators.Con- a highdegree of bothvegetative and reproductive sequently,it does not appearthat dissimilarity in specialization.The monopodialtwining habit of pollenstructure provides a compellingargument D. scandens,with inflorescences terminating de- againsta ratherclose phylogeneticrelationship terminate short-shoots, could be derivedfrom betweenthe two genera. modificationof a sympodialgrowth form evident in generaof therelated tribe Plukenetieae such as Fruits and seeds-One of the most striking Cnesmone(Wagner, 1930) and Tragia (Miller changeswhich follows pollination of the Dale- and Webster,1967). It is not clearwhether the champiainflorescence is the enlargement and in- twiningor theshrubby habit is primitivein Dale- creasedspininess of the femalecalyx segments champia;although experience with otherplant (Fig. 18, 19). The 8-12 narrowcalyx segments groupswould indicate that the woody habit should ofD. scandenselongate about 100 % intoa "pali- be original,the shrubbygroups of Dalechampia, sade fence"of rigid"stakes" beset withsharp- suchas sect.Cremophyllum, are not particularly pointedhairs about 1-1.5 mmlong. It is difficultunspecialized in reproductivecharacters. to avoid ascribinga protectivefunction to these The originof the distinctiveDalechampia in- armedcalyx segments, since this formidable arma- florescenceremains unresolved. The white-bracted turedevelops concurrently with the maturation of speciesappear to be insect-pollinated,as the single thefertilized ovary into a fruit. definitereport of Miller (1879) suggests.The The capsularfruit of D. scandensattains about red bractsof species such as D. magnoliifolia 1 cm in diam,with three distinctly carinate cocci stronglysuggest bird-pollination; these taxa have (Fig. 19). The fruitreadily shatters, but the presumablybeen derivedfrom insect-pollinated

This content downloaded from 169.237.8.35 on Mon, 16 Sep 2013 16:48:05 PM All use subject to JSTOR Terms and Conditions July,1972] WEBSTER AND WEBSTER-MORPHOLOGY OF DALECHAMPIA 585 ancestors. The speciesof sect. ,with ratherrepresents an endpointof theevolutionary rudimentaryinvolucres, are especially baffling. line of twiningplants in the tribePlukenetieae, Vegetatively,such taxa as D. micrantha,with fromwhich it differsprimarily in itsadaptive shift foliage suggestiveof Plukenetia,could be inter- to a newmode of pollination.This evolutionary preted as remainingat an "ancestral" condition. "quantum"displacement has resultedin a very However, if Michaelis (1924) is correctin his distinctivefloral morphology for Dalechampia, suggestionthat the primitiveinflorescence struc- whileat thesame time it has obscuredits relation- tureis thatfound in D. tamifoliafrom Madagascar, shipswith other Euphorbiaceous taxa. then the reduced inflorescencesin D. micrantha The dilatorinessof botanists in elucidatingthese do not representthe ancestralcondition for the problemsof affinity is piquantly highlighted by an genus. At present,therefore, there seems some- old and neglectedobservation of Fritz Muller what more justificationfor considerationof D. (1884), who pointedout thatthe caterpillars of micranthaas a "pseudo-primitive"plant withre- therelated butterfly genera Ageronia and Didonis ductionof the involucrethan thereis for ranking ()had been observedto feed on it as an ancestraltype. Dalechampia and Tragia, respectively.Referring Venkata Rao (1971) has discussed the inflo- to thethen recent (1880) taxonomicjuxtaposition rescencestructure in Dalechampia on the basis of of thetwo plant genera by Benthamand Hooker, his observationson D. spathulata. His conclusion Mullerslyly concluded that the affinity of Dale- that the cyathiumof Euphorbieae cannot be de- champiaand Tragia,"which has been dulyap- rived fromthe pseudanthiumof Dalechampia is preciatedby butterflies,has finallybeen recog- in accordwith the views expressed here. However, nizedby botanists also." We hopethat neotropical we cannotagree that the inflorescence of botanistswill now proceedto followthis lepi- indica is ancestral to that of Dalechampia, as dopteraninspiration by investigating the compara- suggestedby Venkata Rao. The racemoid inflo- tive biochemistryas well as the morphologyof rescence of , with its terminal Dalechampia and its allies. malformedfemale flower and spirallyseparated clustersof male flowers,contrasts strongly with LITERATURE CITED the Dalechampia inflorescence,in whichthere is a BAILLON,H. 1858. E2tudegenerale du groupe des terminal male flower in a terminal staminate Euphorbiacees. VictorMasson, Paris. pleiochasium. It appears to us thatVenkata Rao BENTHAM,G. 1878. Notes on Euphorbiaceae. J. has placed too much emphasis on the terminal Linnean Soc. Bot. 17: 185-267. femaleflower of Acalyphaindica, which is actually . 1880. Euphorbiaceae. In G. Bentham and characteristicof the genus Acalypha and not of J. D. Hooker,Genera Plantarum 3: 239-340. the tribeAcalypheae as a whole. In fact,the in- CROIZAT,L. 1940. On the phylogenyof the Euphor- florescencesin Plukenetieaesuch as Tragia have biaceae and some of theirpresumed allies. Revista a terminalflower which, although malformed, is Univ. Chile 25: 205-220. staminaterather than pistillate(Miller and Web- . 1942. Peculiaritiesof the inflorescencein the Euphorbiaceae. Bot. Gaz. 103: ster, 1967). It would appear, therefore,that the 771-779. DRESSLER,R. L. 1957. The genusPedilanthus. Contrib. ancestral patternfor the Dalechampia inflores- Gray . 182: 1-188. cence is to be soughtwithin the taxa of Plukene- FAEGRI,K., ANDL. VANDER PIJL. 1966. The principles tieae ratherthan in Acalypha. of pollinationecology. PergamonPress, Oxford. The analysis of both vegetativeand reproduc- HURUSAWA,I. 1954. Eine nochmaligeDurchsicht des tivestructures leaves no doubtthat Baillon (1858), herkommlichenSystems der Euphorbiaceen im Bentham(1880), and Pax and Hoffmann(1919, weiterenSinne. J. Fac. Sci. Univ. Tokyo Bot. 6: 1931) were correctin closely juxtaposingDale- 209-342. champia and the Plukenetieae,and thatthe treat- HUTCHINSON,J. 1969. Tribalism in the family Eu- mentsof Jussieu(1824), Croizat (1940, 1942), phorbiaceae. Amer.J. Bot. 57: 738-758. and Hurusawa (1954) cannotbe followedin JENSEN,W. A. 1962. Botanicalhistochemistry. W. H. asso- Freemanand ciating Dalechampia with the tribe Euphorbieae Co., San Francisco. JUSSIEU, A. 1824. De Euphorbiacearumgeneribus (Webster and Webster, 1966; Webster, 1967). medicisque earumdem viribus tentamen. Didot, The recenttreatment of Hutchinson (1969), in Paris. which Dalechampia is placed betweenHura and KNOLL, F. 1905. Die Brennhaareder Euphorbiaceen- Pera, does not reflectphylogenetic relationships, GattungenDalechampia und Tragia. Sitzungsber. and in fact, is a retrogradestep. The involucre Kais. Akad. Wiss. Wien Math.-naturwiss.KI. 114: of Pera and the male "involucre"recognized by 29-48. Hutchinsonin Huiraare not homologouswith that LEANDRI,J. 1943. Contributiona 1'etudedes Euphor- of Dalechampia, and these threegenera are dis- biacees de MadagascarVII. Dalechampiees. Not. similarin such importantcharacters as trichomes, Syst.Paris 11: 35-46. LE'ONARD, J. 1962. Euphorbiaceae, Dalechampieae. pollen, and fruits. Flore du Congo et du Rwanda-Burundi8(1): 194- From the phylogeneticviewpoint, Dalechampia 202. certainlyhas little affinitywith Euphorbia but MICHAELIS, P. 1924. BlutenmorphologischeUnter-

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suchungenan den Euphorbiaceen. Bot. Abh. Jena PUNT, W. 1962. Pollen morphologyof the Euphor- 3: 1-150. biaceae withspecial referenceto .Wentia MILLER, K. I. 1964. A taxonomicstudy of the species 7: 1-116. of Tragiain theUnited States. Ph.D. thesis,Purdue RITTERSHAUSEN, P. 1892. Anatomisch-systematische Univ. Untersuchungvon Blatt und Axe der Acalypheen. , AND G. L. WEBSTER. 1967. A preliminary Inaug.-dissert.,Munich. revisionof Tragia (Euphorbiaceae) in the United SINGH, R. P., AND A. PAL. 1968. Structureand de- States. Rhodora 69: 241-305. velopmentof seeds in Euphorbiaceae:Dalechampia MULLER, F. 1884. Butterfliesas botanists. Nature roezeliana Muell.-Arg. Tech. Comm. Nat. Bot. 30: 240. Gard. Lucknow 1968: 65-74. MULLER, H. 1879. Die Wechselbeziehungenzwischen URBAN, I. 1888. Ueber den Bliithenstandvon Dale- den Blumen und den ihre Kreuzungvermittelden champia. Jahrb.Kg. Bot. Gart. Berlin4: 252-259. Insekten,p. 1-112. In A. Schenck,Handbuch der VENKATARAO, C. 1971. Anatomyof theinflorescence Botanik. I. Eduard Trewendt,Breslau. of some Euphorbiaceae.With a discussionon the MUELLER, J. 1864. Systemender Euphorbiaceen.Bot. phylogenyand evolutionof the inflorescence,in- Zeit. 22: 324. cludingthe . Bot. Notis. 124: 39-64. 1866. Euphorbiaceae. DC. Prodr. 15(2): WAGNER,R. 1930. Ueber die Verzweigungder Cnes- 189-1261. monejavanica Bl. Ann. Naturhist.Mus. Wien 44: PAX,F. 1890. Euphorbiaceae,p. 1-119. In A. Engler 39-43. and K. Prantl[ed.], Die NatuirlichenPflanzenfami- WEBSTER, G. L. 1967. The genera of Euphorbiaceae lien 111.Teil. 5. Abt. Engelmann,Leipzig. in the SoutheasternUnited States. J. Arnold , AND K. HOFFMANN. 1919. Euphorbiaceae- Arboretum48: 303-430. Dalechampieae. In A. Engler [ed.], Das Pflanzen- 1968. Dalechampia. In Flora of Panama, reichIV. 147. XII (Heft 68): 1-59. Part VI. Ann. Mo. Bot. Gard. 54: 308-316. , AND . 1931. Euphorbiaceae,p. 11-233. , AND B. D. WEBSTER. 1966. The morphology In A. Engler and K. Prantl[ed.], Die Naturlichen and relationshipsof Dalechampia. Amer. J. Bot. Pflanzenfamilien.2nd ed. 19c. Engelmann,Leipzig. 53: 635.

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