Torrey Botanical Society

Stem and Leaf Anatomy of Saruma henryi Oliv., Including Observations on Raylessness in the Aristolochiaceae Author(s): William C. Dickison Source: Bulletin of the Torrey Botanical Club, Vol. 123, No. 4 (Oct. - Dec., 1996), pp. 261-267 Published by: Torrey Botanical Society Stable URL: http://www.jstor.org/stable/2996773 . Accessed: 20/08/2011 14:12
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Bulletinof the TorreyBotanical Club 123(4), 1996, pp. 261-267

Oliv., Stem and leaf anatomyof Saruma henryi in on raylessness includingobservations the Aristolochiaceae
William C. Dickison
of NorthCarolina, Chapel Hill, NC 27599-3280 of Biology, University Department of North Carolina, Chapel Hill, NC 27599-3280). The of Biology, University W. C. (Department DICKISON, stem and leaf anatomyof Saruma henryiOliv., includingobservationson raylessnessin the Aristolochiaceae. of the Aristolochiaceae, Oliv., a Chinese monotype Bull TorreyBot. Club 123: 261-267. Year.-Saruma henryi as a thinleaf mesophyllwithspherical features It shows such typicalaristolochiaceous is describedanatomically. nodes with two lengthand size; anomocyticstomata; trilacunar oil cells; simple uniseriatehairs of different an arc of threeor more widely separated the median gap; and a petiole containing vascular bundles confronting Lactoridaceae,and Piperaceae includevessel elements betweenAristolochiaceae, bundles. Shared xylemfeatures to alternate. scalariform and vessel pitting plates, vessels in radial chains and multiples, withsimple perforation fromotherAristolochiaceaein the absence of xylemrays and axial parenchyma. distinct Saruma is anatomically shifttowardthe replacementof both wood a previouslyunreported represent features These distinctstructural of trueaxial and ray elementsthatstorestarch.The elimination by living,fiber-like rays and axial parenchyma by short,nucleated,living ground cells can be related to an increased parenchymaand its total substitution storagecapacity and mechanical strength. Saruma wood, systematics, Key words: Magnoliaceae, Aristolochiaceae,anatomy,

The genus Saruma consists of a single spe- daceae, Piperaceae, and Saururaceae (Carlquist cies, S. henryiOliv., thatis confinedto only a 1990, 1992, 1993; Carlquist et al. 1995). Sarufew provincesin China (Ma 1990). The plantis ma, however,was not included in these studies known.In i perennial, rhizomatousherb thatformsa lim- and its anatomyremainsincompletely of the gesignificance ited amount of secondary xylem in the aerial view of the phylogenetic stem.As pointedout in a previouspaper (Dick- nus and the questions regardingits most satisof an investigation treatment, systematic considerable factory ison 1992), the genus has attracted in orderto promemberof the Aristo- vegetativepartswas undertaken as a primitive attention inforby fea- vide a more complete body of structural lochiaceae. This opinion is strengthened morphologysuch as acti- mation on the family and make comparisons tures of reproductive withwell-developedpetals,a withanatomicaldata obtainedelsewhereon othflowers nomorphic gynoecium composed of multiple carpels that er members of the family and theirpresumed show extensivefreedomand thatmatureinto a closest allies. and the occurrenceof monosulfollicularfruit, imcate pollen grains.Saruma assumes further Materials and Methods. This study was portance as a component of the "paleoherb" based upon examination of plants of Saruma complex, a group that has been suggested to henryicultivatedat the United States National bearingon theearlyevolution Arboretum,Washington,D.C. (Dickison s.n., have an important of angiosperms(Taylor and Hickey 1992). April 19, 1991). Leaves and young stems were and prepared by standardmethods of paraffin emAlthoughstudyof the floralmorphology anatomy of Saruma supportedits inclusion in bedding and sectioning(Johansen1940). Stainisolated position ing was accomplished with safranin-fast the Aristolochiaceae,its rather green. within the family was emphasized (Dickison Mature stems were softenedin ethylenediamine 1992). The patternof early floraldevelopment for one or two hours as recommendedby Caof Saruma has been used to show an affinity rlquist (1982), and then embedded in paraffin with the magnoliaceous family Annonaceae and sectioned. Nodes were serially sectioned, (Leins and Erbar 1995). During the past few and petiole anatomywas examinedalong theenyears, detailed examinationsof wood and bark tire length.Stomatal patterns were observed in evidence of close preparedparadermalsections. Stomatal dimenanatomyhave providedstrong relationshipbetween Aristolochiaceae,Lactori- sions were based on twenty Leaf measurements. venationwas examined using leaves cleared in withsafReceived forpublicationFebruary28, 1996, and in 5% NaOH at 60?C followedby staining ranin.Measurementsof xylem cell lengthwere revised formJune20, 1996.

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of separating not obtainabledue to the difficulty fibersfromxylem groundtissue. A extraxylary few vessel elementlengthswere measuredfrom both macerationand sections but these data are Drawings were made from only approximations. preparedand stainedsectionswitha Wild Heerbrug camera lucida. Results.
NODAL ANATOMY AND VASCULATURE

The nodal anatomyof Saruma is regions in which threeinterfascicular trilacunar are presentin the eustele of the stem.Each leaf is vascularizedby a pair of discretemediantraca single median gap, and a pair es thatconfront of lateraltraces(Fig. 1). The two medianstrands are independentat the nodal level and remain separateinto proximalregionsof petiole. At approximatelymidlevel the two median bundles fuse to forma single midvein,thatis accompanied on eitherside by a lateral strand(Fig. 2). At distal-mostlevels of the petiole the lateral in an arc of fivewidely strandsdivide, resulting spaced petiolar bundles (Fig. 3). Each bundle entersthe lamina as a major vein. Sclerenchyma is absent from around the petiole vascularization. As noted by Hickey and Wolfe (1975), the leaf venation of Saruma is basal acrodromous, veins of equal with threeand thenfive primary in convergent archestoward thickness extending the leaf apex (Fig. 4). High orderveins are narcells in width.Free row,generally2-3 tracheary in a single linear vein endingsusually terminate tracheid. Sheathing around the major veins is and composed of thin-walledpamultilayered cells. Veinlets are borderedby a renchymatous uniseriate, inconspicuous, parenchymatous sheath.
OF THE LEAF. LEAF LAMINA. The cordate leaves are alternate,simple,petiolate,withentiremargins.Uniunbranchedtrichomesare seriate,multicellular, presenton both lamina surfaces.Foliar hairs on the petiole and lamina exhibitconsiderablevariof component cells, ation in size, length, number of cell walls (Figs. 5-8). Hairs are and thickness most numerous along the major veins. Some hairs are presumably glandularas evidenced by head cell (Fig. 7). The presa swollen, terminal cell of some ence of crystalsand in the terminal hairs was noted by Metcalfe and Chalk (1950) here (Fig. 6). Minute birefrinand is confirmed gent crystal prisms and flecks impregnatethe cells of some trichomes walls of terminal (Figs. 5, 8).

A very thin cuticle covers both adaxial and abaxial surfaces. Adaxial epidermal cells vary as considerablyin size, shape, and orientation section, and have straight viewed in transverse or curved outer walls. The adaxial and abaxial epidermallayers in species of Aristolochia,Asarum, and Thotteahave been describedas often papillose (Metcalfe and Chalk 1950), a condition thatcould be very loosely applied to Saruma. Anticlinalwalls are curved or undulatedin outlinein surfaceview. Abaxial epidermalcells in outline,smallerthanthose of the are irregular anticlinal undulating withhighly adaxial surface, walls. Stomata are confinedto the abaxial surface and conformto the anomocytictype (Fig. 15). Guard cells are thin-walledand approximately34.0 pimin length.Lamina construction is bifacial. The mesophyllis thin,composed of one layer of shortpalisade cells and a loosely arranged spongy region (Fig. 14). Numerous thin-walledand enlarged oil cells are scattered in the spongymesophyll(Fig. 16). They are surroundedby a collection of radiatingmesophyll cells. Althoughtypicallyspherical in form,oil cells may occasionally become lobed or irreguor oil ductsare also lar in shape. Large secretory presentin the secondary phloem of major leaf bundles. veins proThe major and intermediate-sized trudeabove and below the surfaceof the blade. by a uniseriateor multiVeins are surrounded Infreparenchyma. seriatesheathof thin-walled stonecells occur sinlignified quentthin-walled, gly in the cortex around the primaryveins. Small crystalflecksalso occur in the cortexsurroundingthe major veins. are abundanton young stems. Hairs are of different sizes and lengths,some have an enlarged glandularhead. Epidermal cells are rectangular to circularin outline and covered by a thincuinto an outer, ticle. The cortex is differentiated zone and an inner 3-4 layeredcollenchymatous region of large parenchyma.In the youngest stemsthe vascular tissue is organizedinto8 discollateral widely separated,wedge-shaped, tinct, vascular bundles thatlack associated perivascuxyprimary lar sclerenchyma (Fig. 9). Abundant elementsare embedded in parenlem tracheary chyma. In progressivelyolder portionsof the stem the individual primarybundles become capped by fibers,which persist in the mature stem as separate fibrousstrands(Fig. 10). The vascular cambium forms a complete cylinder
AERIAL STEM. Multicellular unbranched hairs

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Figs. 1-10. Camera lucida drawingsof stem and leaf anatomyof Sarumahenryi. 1. Transversesection of node showing trilacunar condition.Note pair of median traces (mts) and two lateral traces (lt). 2. Transverse section at midlevel of petiole showingthreevascular bundles and sclereids (sc). 3. Transversesection of petiole at base of lamina. 4. Cleared leaf showingmaturevenationpattern. 5. Multicellular, unbranchedtrichome from leaf. Note crystalsand in wall of terminalcell. 6. Glandular trichomefromleaf. Note crystalsand in terminal cell. 7. Glandular trichome fromleaf. 8. Multicellular, unbranched trichome fromleaf. Note crystalsin walls of terminalcells. 9. Transversesection of young stem showing widely separatedvascular bundles. Note complete vascular cambium(vc). 10. Transverse sectionof base of matureaerial stem.Note completecylinder of secondary xylem and perivascularfibrousstrands.Collenchyma, cross-hatched;xylem, striped;phloem, dotted; sclerenchyma,solid black.

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to produce early in developmentand functions a complete and uniformcylinderof secondary xylem and phloem. The pith cells are thinwith some cells conwalled in mature-stems, crystals and taining small, irregularly-shaped starch. Periderm does not develop in aerial stems. XYLEM. A limitedamountof secSECONDARY ondary xylem is produced. At the base of the aerial stem a cylinderof one-year's growthis about 0.75 mm thick. Vessel elementsare narin lumina to 27 pLm row, rangingfrom 13 pLm tangential diameter,with a mean of 19 iLm. Pores are angular or almost circularin outline withthinwalls, ca. 2.0 iim thick.Vessels occur as well as frequent in the solitarydistribution radial multiplesof 2-9, also less common small clustersof 3-4 (Fig. 11). Vessel elementsrange with to 342 pLm, in lengthfromabout 181 pLm Intervessel pitmean of 243 iLm. an approximate arAlternately ting is alternateto scalariform. rangedpits are rounded,oval, or elongatein outline, with a mean diameterof ca. 5.0 iLm.Scalariform pits extend the entirewidthof the lateral wall. Perforation plates are simple in end walls. inclinedto transverse The groundtissueis composed of erect,living elements that substitutefor imperforatetracheary elements and are the pervasive backgroundtissue (Fig. 11). All groundcells are nucleated and possess moderatelythick,lignified in transverse walls thatare square and fiber-like numberof these outline (Fig. 13). A significant elementsare septate.Groundelementshave slitlike pits with very reduced bordersand can apin size and morpear somewhat intermediate fibersand parenchyphology between libriform ma. Starch is stored in all axial elements. towardstoGroundcells show a slighttendency Rays are absentin thematurexylem(Fig. 12). In the immediatevicinityof the vascular camrays bium it is possible to recognizemultiseriate composed of erect cells. At a shortdistance removed fromthe cambiumtheray cells elongate, walls, and bedevelop taperedends and lignified come gradually indistinguishable from the groundtissue. Thus, a rayless conneighboring ditionis evidentin the maturesecondaryxylem. fromthe the elementsdifferentiated At maturity cambial ray initials are nucleated and store starch(Fig. 12). Discussion. A summationof vegetativeanatomical charactersindicates that Saruma interrying.

grades closely with othermembersof the Arisanatomical similarities tolochiaceae. Significant in vegetativeanatomyinclude the formof the of the node, petiole, and vascularizationpattern leaf mesophyllwith lamina; a thin,membranous palisade cells; anomocytic a singlelayerof short stomata; and simple uniseriatehairs that show variationin lengthand size. Metcalfe and Chalk (1950) commentedthat typical glandular hairs are absent fromthe Aristolochiaceae,although trichomeswith an enlarged secretoryhead cell on the leaves of Saruma. Precipiare frequent tated secretionsare evidentin the trichometerminal cell. Metcalfe and Chalk (1950) also reportedthat some hairs of Apama, Aristolochia, and Thottea have a dome-shaped pedestal, a cell with shortneck cell, and a hooked terminal cells a silicifiedtip. Hairs withhooked terminal are unknownin Saruma. Stem and leaf cells of contain all membersof the familyinfrequently clusters of small crystals. Spherical oil cells, which are so common in Asarum and Aristolothe chia, are abundantlyscatteredthroughout leaf of Saruma. Sclereids are reportedhere in the leaves of Saruma, where they are confined to corticaltissueof thepetiole and in close proximityto the major veins of the lamina. Similar idioblasts are known forotheraristolochiaceous genera (Metcalfe and Chalk 1950). The nodal anatomyof the Aristolochiaceaeis in which all of the vascutrilacunar, uniformly lature of the leaf is related to threeinterfascicular areas in the eustele of the stem.As a family, the Aristolochiaceae are characterizedby having the relativelyuncommonconditionof a variable numberof vascular strandsassociated with the median gap at the level of the node (Nair and Narayanan 1962, Bowman 1973). In Aristolochia,one, two, or threebundles are related to the median gap. Two discrete strands the median gap in Asarum and Braganconfront tia. The nodal anatomyof Saruma resemblesthe latterpatternand is thus in keeping with the overall aristolochiaceous condition. Nair and of Narayanan(1962) consideredan even number the median gap to the chartraces confronting conditionforthefamand fundamental acteristic ily. Higher up in the petiole the leaf traces undergo union and subdivisionto produce an arc of threeor more widely separatedbundles. The families Annonaceae, Myristicaceae, Canellaceae, Saururaceae and Piperaceae also have a nodal anatomy. trilacunar The xylemanatomyof Saruma exhibitsmany of the featuresthatCarlquist (1990, 1993) con-

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0.1

mm

pirAi

0.1mm

14

Mrimm

Figs. 11-16. Vegetative anatomyof Saruma henryi. 11. Transversesection of secondary xylem showing solitarypores and radial multiples.12. Tangentialsectionof xylemillustrating raylesscondition.13. Tangential section of xylem. Note prominent nuclei in ground elements. 14. Transversesection of leaf. 15. Paradermal sectionof leaf showinganomocyticstomata.16. Cleared leaf showingoil cells.

sidereddistinctive forthe Aristolochiaceae, Lactoridaceae, and Piperaceae. These shared features include vessels with simple perforation plates, vessels in radial chains and pore multiples, and vessel to vessel pittingscalariform to alternate. The observationof simple perforation platesin Saruma confirms thischaracter statefor theentirefamilyAristolochiaceae.In contrast, a few representativesof the minimally woody families Saururaceae and Chloranthaceae containscalariform vessel elementperforations. The

limitedxylem of Saruma, however,also shows conspicuous evidences of phylogeneticmodification thatdeviate fromotherAristolochiaceae and pointto extreme specialization.Of particular note is the absence of both wood rays and axial parenchymafollowingtheirreplacementby fiber-like elements.Crystalsand oil cells were not observed in the xylemof Saruma althoughthey are known fromothermembersof the family. in Aristolochiaceaeranges Axial parenchyma fromdiffuse, diffuse-in-aggregates, scantyvasi-

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and variousaggregateand pervasivedis- ing wide, tall rays. As noted by Carlquist et al. centric, thejuvenile raysof the ArAsarum is described as having per- (1995), furthermore, tributions. withvessels embedded in a istolochiaceae, Chloranthaceae, Lactoridaceae, vasive parenchyma, axial ground tissue, with im- Piperaceae, and Saururaceae suggestthatat least parenchymatous trachearyelements absent. Following some woodiness in these familiesmay be a secperforate thisconditionwas ondarilyderived condition. As emphasized by observations, my preliminary also reportedfor Saruma (see Carlquist 1993). Carlquist,the concept of the "paleoherb" need axial not connotatethe complete absence of cambial It is now evident,however,thattraditional thatmost Arisinterest in a activity.It is of further cells scattered i.e., thin-walled parenchyma, fibrous groundtissue,is absentin Saruma. Rath- tolochiaceae possess a closed ring of perivaser, the ground tissue is composed totallyof a cular fibersin the young stem. As the stem inliving, fibrous, intermediatecell type that is creases in girththe fibrousring subdivides into elongated but comparativelyshort,has tapered separate strands.The absence of a continuous ends, along with lignifiedwalls and very re- ring of sclerenchymain the youngeststems of and indicmay be significant duced pit borders.Many of these elementsare Saruma, therefore, septate. Nuclei and starchgrains are conspicu- ative of a secondarilyherbaceous condition. The eliminationof true axial and ray parenous withinthese elements.A suggestionof stonucleby short, ryingcan be seen in these cells, a featurealso chyma and its total substitution in reported for a few other Aristolochiaceae. ated, livinggroundcells thatare intermediate between parenchymaand true fibers Carlquist(1993) emphasizedthe absence of true structure elementsin the tribeAsa- can be relatedto an increased storagecapacity. tracheary imperforate walls of these elementsand sparse presencein dif- The lignified reae (Asarum,Saruma) and their to mechanicalstrength would also impart ferent formsin tribesBragantieaeand Aristolo- pitting the uprightaerial stems of Saruma. Carlquist chieae. All Aristolochiaceae examined by Carlquist (1969) postulatedthatwoods in which the rays or exclusively of (1993) possessed exclusively tall, multiseriate are composed predominantly upright erect or square cells, as in most Aristolochixylem rays composed of predominantly cells. Juvenilistic raysof thistypeare also found aceae, are essentiallythe equivalents of being between fibersand in Chloranthaceae, Lactoridaceae, Piperaceae, rayless. The intergradation cells, as occurs in the Aristoand Saururaceae. As in otherfamilies,this fea- erectparenchyma for lochiaceae, is evidence of the apparentlack of turepointsto a probableherbaceousancestry between these cell types. some woody membersof thesegroups.The spe- distinction cialized xylem anatomyof Saruma, in contrast, Literature Cited illustratesa distinctand previouslyunreported shifttowardraylessnessin the Aristolochiaceae. BowMAN, inT. C. 1973. Comparativemorphological However,the presence of wide, tall xylem rays Unpubi.Ph.D. on theAristolochiaceae. vestigations Tempe. Arizona State University, Dissertation, in the extremeouter portionof the secondary xylem very near the cambium of Saruma indi- CARLQUIST, S. 1969. Wood anatomyof Lobelioideae (Campanulaceae). Biotropica 1: 47-72. cates thatthe cambium is not devoid of ray in. 1970. Wood anatomy of insular species of itials, as has occurredin a numberof otherdiBull. TorPlantago and theproblemof raylessness. cotyledonousfamilies. rey Bot. Club 97: 353-361. in soft. 1982. The use of ethylenediamine The secondaryxylemof Saruma is of interest sectioning. forparaffin ening hard plant structures to structural because it can provideclues relating Stain Techn. 57: 311-317. Althoughthe undifspecializationand ancestry. . 1990. Wood anatomy and relationshipsof ferentiated secondaryxylemshows theexistence Lactoridaceae. Amer.J. Bot. 77: 1489-1505. . 1992. Wood anatomyand stem of Chloranof tall, multiseriate rays, in fullydifferentiated thus; summaryof wood anatomy of Chloranthaxylem, the rays are lost as the erect rays cells vessellessceae, with commentson relationships, into more elongate, lignibecome transformed ness, and the origin of monocotyledons.IAWA of the elements fied cells resembling other Bull. n.s. 13: 3-16. groundtissue.Rayless wood is foundmostoften . 1993. Wood and bark anatomyof Aristolochiaceae; systematic and habital correlations. in groups thatare secondarilywoody (Carlquist IAWA J. 14: 341-357. 1970). The xylem of Saruma indicates thatthe , K. DAUER AND S. Y. NISHIMURA. 1995. Wood from a plant genus may well have been derived to and stemanatomyof Saururaceae withreference having some cambial activityand possessing a and origin of the monocotyecology, phylogeny, ledons. IAWA J. 16: 133-150. wood anatomycontaintypicalaristolochiaceous

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in den Bluten von Saruma henryi erungsmuster to and stemanatomyof Saururaceaewithreference Oliv. (Aristolochiaceae). Bot. Jahrb. Syst. 117: and origin of the monocotyecology, phylogeny, 365-376. ledons. IAWA J. 16: 133-150. and the W C. 1992. Morphologyand anatomyof MA, J.-S. 1990. The geographicaldistribution DICKISON, systemof Aristolochiaceae.Acta Phytotaxonomica the flowerand pollen of Saruma henryiOliv., a Sinica 28: 345-355. phylogeneticrelict of the Aristolochiaceae.Bull. 1950. Anatomyof METCALFE, C. R. AND L. CHALK. TorreyBot. Club 119: 392-400. 2 Vols. ClarendonPress, Oxford. dicotyledons. of bases The 1975. A. WOLFE. AND J. L. J. HICKEY, NAIR, N. C. AND K. R. NARAYANAN. 1962. Studies on angiosperm phylogeny; vegetative morphology, the AristolochiaceaeI. Nodal and floralanatomy. Ann. Missouri Bot. Gard. 62: 538-589. Proc. Nat. Inst. Sci. India 28B: 211-227. Mc- TAYLOR, D. W. AND L. J. HicKEY. 1992. Phylogenetic D. A. 1940. Plant microtechnique. JOHANSEN, Graw-Hill,New York and London. evidence forthe herbaceousoriginof angiosperms. P1. Syst. Evol. 180: 137-156. DifferenziLEINS,P. ANDC. ERBAR. 1995. Das friuhe

ANNOuNCEMENT Awarding of the 1996 Lawrence Memorial Award. Amy J. Litt at the New York Botanical Garden, is the recipientof the 1996 Lawrence Memorial Award. A studentof Dr. Scott Mori, a study of the phyloMs. Litt has undertaken gencyof the Vochysiaceae. She will use theproceeds of the $1000 Award for travelin Cameroon for fieldresearch.The Award, commemoDiDr. George H. M. Lawrence,founding rating rector of the Hunt Institute for Botanical Documentationat Carnegie Mellon University, doctoralcandidatefor is made to an outstanding researchin systravelin supportof dissertation or the historyof tematicbotanyor horticulture, and exthe plant sciences, includingliterature ploration.