Floral Morphology and Phylogeny in the Hydrocharitaceae Robert B

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Faculty Publications in the Biological Sciences Papers in the Biological Sciences

3-1968 Floral Morphology and Phylogeny in the Hydrocharitaceae Robert B. Kaul University of Nebraska - Lincoln, [email protected]

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Kaul, Robert B., "Floral Morphology and Phylogeny in the Hydrocharitaceae" (1968). Faculty Publications in the Biological Sciences. 462. http://digitalcommons.unl.edu/bioscifacpub/462

This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in the Biological Sciences by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Kaul in Phytomorphology (March 1968) 18(1): 13-35. Copyright 1968, International Society of Plant Morphologists. Used by permission.

FLORAL l\tl0RPHOLOGY AND PHYLOGENY IN THE HYDI~OCHARITACEAEI

ROBERT B. KAUL Department of Botany, University of Nebraska, Lincoln, Nebraska, U.S.A.

Abstract

The vascular anatomy of 13 of the 15 genera of the Hydrocharitaceae has been studied, and certain aspects of floral morphology are con­ sidered. The flowers of the family show a broad range of specialized structures combined with primitive characteristics. The origin of paired and single stamens is interpreted as probable modifications of fascicled stamens. Extreme reduction in the androccium is shown for several genera. Tendencies toward reduction and fusion within the gynoecium are pronounced. Most genera are at least slightly syncarpous, but a few are apocarpous. The inferior ovary is appendicular in nature, with some genera exhibiting more complete fusion than others. The car­ pels arc open and show no signs of closure. The multicarpellate genera have the most primitive gynoecia within the family while the tricar­ pe11ate genera exhibit the most advanced types in the family. Inter­ mediate forms are Blyxa and Vallisneria.

Introduction number in each taxon being approxi­ mately constant. The carpels are free The Hydrocharitaceae is a small family or fused with each other. Most authors presently recognized as comprising 15 have interpreted the gynoecium of the genera and fewer than 100 species. Most entire family as apocarpous. There are of the genera are tropical or subtropical, as many styles as there are carpels and and all are aquatics. Three genera arc these styles arc often split into two long strictly marine. Many genera are mono­ stigmatic arms. There arc several to typic or have but a few species. numerous anatropous or orthotropous All genera except Oitelia have at least ovules; both types are found in some some species with unisexual flowers which flowers. The embryology is known for are usually borne on separate plants. most genera. The female flowers possess three sepals The male flowers have one to many and three petals except in Halophil a stamens, and the number is approxi­ and Thalassia where there are three mately constant in each genus. Some perianth segments. Many female flowers have staminodia; paired stamens and have staminodia. The ovary is inferior paired staminodia are frequent. Many and consists of 3 to 20 carpels, with the have three pcrianth segments, a few have

------1. Received for pnbJication: January 20, 1966. I am indebted to Dr E. C. Abbe and Dr Thomas Morley of the University of Minne­ sota for their encouragement and comments. A portion of this work formed part of a doc­ toral dissertation presented to the Faculty of the University of Minnesota. I am also indebt­ ed to the National Science Fou nd ation, \Vashington, the Society of the Sigma Xi, the Min­ nesota Academy of Scicncc, and the University of Minnesota for financial support, and to the botanists of India, Ceylon, Malaysiu, and the Philippines for assistance while I visited those countries. 14 PH YTo.MoRPHOLOGY [ ~!arch four, and others have six. The male flower per cent lactic acid and brought to lOOe of M aidenia is reported to lack a perianth for about ten minutes. They were then and the entire flower to be reduced to ready for study without staining. Those a single stamen (Rendlc, 1916). In those specimens with considerable tannin were species in which the male flower is very bleached quickly in boiling water to tiny the entire flower breaks loose from which a few drops of sodium hypochlorite th~ submerged inflorescence and floats were added. They were then transferred upon the surface. The very interesting to lactic acid. No softening occurred pollination mechanisms of the various with this method. genera have been studied in some detail Flowers of all genera studied, except (Hartog, 1957). Lagarosiphon and Stratiotes, were embed­ The vegetative anatomy of the family ded in paraffin and sectioned. Larger has been studied in detail by Caspary flowers were sectioned at 20, 30 and 50 (1858), Rohrbach (1871), Balfour (1879), microns and smaller flowers at 12 and Cunnington (1912), Solcrcdcr (1913), and 15 microns. The sections were stained others. The writer has not attempted with safranin and fast green; crystal to correlate the data obtained in these violet and ervthrosin were very unsatis­ studies with anatomical characteristics factory for staining the weakly differen­ of the flowers. The Hydrocharitaceae tiated tissues. Clarite was used for is one of the six monocotyledonous fami­ mounting. lies reported by Cheadle' (1953) to lack Slightly oblique sections were more vessels. useful than perfectly transverse ones. For some genera complete develop­ Materials and Methods mental series were obtained. Because the ontogeny of the flowers is beyond the Fourteen of the 15 genera of the Hydro­ scope of the present paper, data arc pre­ charitaccae have been studied. I collect­ sen ted onlv from sections and cleared ed Otielia alismoides in India and the material o (flowers at or ncar anthesis. Philippines; Enhalus acoroides, IIalopMla spp. and Thalassia hemprichii in Singapore Observations and the Philippines; and Blyxa spp. and Hydrilla »erticillata in Singapore. OTHLIA AUSMOIDES (L.) PERS.- In O. I also collected Hvdrocharis morsus-ranae alismoides the sessile bisexual flowers and Straiiotes aloides in Germany; \Techa­ are borne singly within the inflorescence. mandra alternifolia in India; Vollisneria The three green sepals are alternate with spp. in the Philippines, Minnesota, and the three large white petals. There are Nebraska; and Elodea canadensis in usually six stamens but nine are not Minnesota and Nebraska. These collec­ uncommon, Other species regularly tions were made in 1961) 1962 and 1964. possess three and nine stamens (Dandy, Elodea densa and Limnobium spongia 1934). All specimens from the Phili­ were grown in the greenhouse from com­ ppines examined by me had at least mercial stock. Boottia cordata was col­ nine stamens and many had ten or eleven. lected in Burma by A. L. Bogle and In those with ten stamens an antisepalous shipped to the au thor. Lagarosiphon stamen was replaced by two stamens has been studied from herbarium material. fused by their filaments (Fig. 1). Each ]VIaidenia rubra, a little-known monotype member of these pairs has an indepen­ from Australia, has not been investigated dent vascular supply. There is a pro­ here. minent nectary opposite each petal. All specimens were prescrvud in These structures are not mentioned by formalin-acetic-alcohol. Clearings, micro­ Asclierson S: Gurke (1889), Hartog (195i) tome sections, and hand sections were or Dandy (1934). Suhramanyam (1962) employed. The materials cleared readily mentioned rudimentary stamens and in weak sodium hydroxide solution at Richard (1811) illustrated fleshy tubercles 60 C. When clear they were rinsed opposite the petals. The antisepalous briefly in distilled water, 'placed ill 85-90 pairs of stamens arise first. When 1968J h:AtTL - HYDROCHARITACEAE 15

5 " ----./

9 vv

Figs. 1-10 -i-Ottelia and Boottia (d+, dorsal bundle which also serves perianth andandroecium; n, nectary; p, petal; st, sepal; st , stamen; sl a, starninodiu m : 1'1', ventral bundle serving adjacent carpels). Figs. 1-4. Ott.el i a alisnioidcs, transverse sections of flower and peduncle. 8. Fig. 1. Through styles and pcrianth . Fig. 2. Lower stvlar rq;ion shmving vascular plexus. Fig. 3. Ovary. Fig. 4. Peduncle of inflorescence. Figs. 5-10. Boottia cordata. Fig. 5. Portion of style of female flower with nectaries and st.amiriodiurn. X 14. Fig. 6. Transverse section through perianth of female flower. X 20. Fig. 7. Stylar region with vascular plexus. X 10. Fig. 8. Ovary. X 10. Fig. 9. Portion of androocium of male flower with outer stamens fertile, penultimate expanded staminodium, and central Iuscd sta.rn inodia.. y 8. Fig. 10. Cross section of male flower, paired bundles shown in expanded st.aruinodia, central stamiuodia black. xiS. 16 PHYT02VIORPHOLOGY [ 'March present, the single antiscpalous stamens to arise directly from the receptacular arise next; they arc sometimes double. vascular tissue. The placental bundles The antipctalous nectarics arise last. arc connected at numerous points with Eichler (1875) and Ascherson & Gurke both the dorsal and ventral bundles. A (1889) observed six carpels in Ottclia but similar situation obtains in the female Hartog (1957) listed six to nine carpels. flOWN of lJ oottia cordata and the reader The writer has not observed as few as is referred to the illustration of that six in Indian and Philippine specimens; species in Fig. 31. most of those examined had ten or more Above the level of the stylar plexus carpels. The ventral margins are free several bundles depart for the adaxial from each other (Fig. 3) but adjacent surface of each sepal. The abaxial sur­ carpels arc partly fused by their abaxial face of each sepal is served by numerous walls. tiny bundles derived directly from the In the center of the peduncle, below peripheral peduncle bundles. These the attachrncn t of the fused bracts, there peripheral bundles are not involved in arc six collateral bundles arranged in the stylar plexus. a ring (Fig. 4). Outside of this ring there About five bundles from the stvlar are several alternating rings of smaller plexus serve each petal. Each stamen bundles. At the level of attachment of receives one bundle anel each nectarv the bracts the six inner bundles arc suc­ two or three bundles from the stvlar cessively fused, branched, and expanded. plexus. That the nectary is composed At the base of the gynoecium, just above of reduced stamens is attested to bv the the level of attachment of the bracts, fact that the vascular supply is like- that approximately twice as many bundles to the stamens. as there are carpels depart from the The placental bundles do not become vascular ring and pass up the ovary wall involved in the stylar plexus but pass to the stylar plexus where their identities directly into the style and stigmatic are lost (Fig. 2). Usually there is one branches where they end. A few bundles bundle opposite the loculc of each carpel, from the stylar plexus also enter each the dorsal bundle, and one bundle oppo­ style and examination of younger material site the point of fusion of adjacent carpel shows them to be derived from the dorsal walls. These latter bundles arc some­ bundle only. A similar situation is found times displaced laterally. They arc in Bootiia and the reader is referred to interpreted here as fused ventral bundles the illustrations of that plant in Figs. of adjacent carpels because they provide 5 and 28. some of the placental bundles to both BOOTTIA CORDATA \VALL.- The female ad jacent carpels (Fig. 3). flower of this species is similar to the At the point of departure of the bundles flower of Ottelia alismoides. It is borne of the ovary wall from the receptacular singly within the inflorescence. The plexus a small meshwork of tiny bundles androecium is represented by at least also departs from this plexus into each nine starninodia, and numbers up to 15 carpel wall. Many of these tiny bundles, arc common. There is a pair of stami­ which are the placental bundles, appear nadia opposite each sepal and often the

Figs. 11-27 - F./lhIlIIlS, Lt nt nobi u.ni and 'Th.alassia (d, dorsal bundle; p, petal median bundle: SC, sepal bundle; sf, stamen bundle; sto, starninodium bundle; u, ventral bundle). Figs. 11-15. Enhalus acoroidcs. Fig. 11. Section through stylar region. X 9. Fig. 12. Section through ovary. X 9. Fig. 13. Section through receptacle at level of departure of carpel bundles. X 9. Fig. 14. Male flower. X 11. Fig. 15. Female flower, ovary and styles invested with hairs. X 3. Figs. 16-21. Limnobiu.m spongia. Fig. 16. Section across pcrianth. X 15. Fig. 17. Stylar region. X 15. Fig. 18. Ovary. X 15. Fig. 19. Receptacle. X 15. Fig. 20. Pedicel. X 15. Fig. 21. Male flower; each bundle serves a stamen; filaments monadclphous. X 15. Figs. 22-27. 'Th alassia hcm prichi], female. 12, Fig. 22. Section across perianth. Fig. 23. Stylar region. Fig. 24 Fertile portion of ovary. Fig. 25. Sterile portion of ovary. Fig. 26. Receptacle. Fig. 27. Pedicel. 1968 -: 1\::\PL - HYDROCHARITACEAE 17 single antiscpalous staminodium is re­ of a member of the outer, antisepalous presented by two incompletely fused pair. Further, apparently single stami­ staminodia. Similar fused paus may nodia are found in any position and be found in any position including that contain two, three, four, or even five

Figs. 11-27 18 PHYTO:'IOH 1'1ioi.ocv [ March independent bundles. There is a large nectarv at the base of, but not fused with, each petal. The order of development of the staminodia and the nectaries is now being investigated. The number of carpels ranges from 9 to 15. In all specimens examined by the writer there were as man V stvles as carpels. The ventral margins ~lf the carpels are not fused nor are the project­ ing carpel walls (Fig. 8). The various interpretations of the gynoecillrn are considered in the' Discussion'. Nine to 12 large vascular bundles can be seen within the aerenchymatous pe­ duncle of the female inflorescence. There is a larger number of smaller bundles toward the periphery. All of the larger bundles and some of the smaller ones make up a confused plexus at the level of attachment of the bracts. The other smaller ones proceed into the abaxial surfaces of the bracts and sepals. Within the receptacle, slightly above the attachment of the bracts, approxi­ mately twice as many bundles as there arc carpels depart from the plexus. One bundle is seen opposite the locule of each carpel (Fig. 8); this is the dorsal bundle. One bundle is found opposite the point of fusion of adjacent carpel walls; it represents the fused ventral bundles of adjacent carpels. Some placental bun­ dles to both carpels are derived from it.

There are numerous vascular connections -; ...•\ "" ...~. between it and the dorsal bundle (Fig. ....,.:..... 31). The dorsal and ventral bundles enter into a stylar plexus (Figs. 7, 28). At the level of departure of the bundles of the ovary wall from the receptacular Fig. 28 Boottia cordata. Drawing made plexus a meshwork of tiny bundles departs from cleared specimens arid serial sections of directly from the plexus into the carpel female flower. Dorsal, fused ventral, and walls. These are also placental bundles placental bundles shown leaving the reccptac­ (Fig. 31). ular plexus. Supply to perianth, staminodia, and nectaries shown leaving stylar plexus. From the stylar plexus several bundles Peripheral bundles serving sepals not shown. pass to the adaxial surface of each sepal Bracts removed and their vascular supply not and several pass into each petal. The shown. >< 4. petal median bundle is united in the stvlar plexus with a dorsal bundle and ~ the petal lateral bundles are united with the of the dorsal bundle which has main­ fused ventral bundles. Each stamino­ tained its identity in the stylar plexus. dium receives one bundle and each nec­ The placental bundles are independent tary receives three or four (Fig. 5). One of the stylar plexus and pass directly bundle passes into the dorsal portion of in to the ventral portions of the styles each style and is possibly a continuation and of the stigmatic branches (Fig. 5). 1968 J 1\..\ UL - HYDH.OCH\ RITACEAE 19

Figs. 29-31 - Linutobium, Enhalus and Boottia, single carpel wall; drawings made from cleared material. Fig. 29. Limnobium spongin, ovules and ventral bundle of adjacent carpel shown by dashed lines. X 11. Fig. 30. Enhalus acoroides, with one stigmatic arm shown. X 8. Fig. 31. Boottia cordata, bundles serving non-carpcllarv tiSS1H' not shown. X 7.

Nine to 15 male flowers are borne in innermost androecial whorl is made up the inflorescence of the male plant. The of three long and bifurcate starninodia; nature of the male inflorescence has not they are alternate with the innermost been reported in the literature. It fertile whorl. The order of maturation appears to be a reduced cyme. is acropetal. The writer observed 12 fertile stamens At the base of the receptacle of the in each flower, whereas Ascherson & male flower all the pedicellar bundles, Gurke (1889) mentioned 6-12 stamens. except the peripheral ones, unite and The outer six stamens are about one-half form a ring of vascular tissue within as long as the inner six (Fig. 9). The which the identity of the bundles is lost. 20 l'HYTOMOH.I'HOLOGY [ ;\Iarch

From this confused plexus three bundles bundles (Fig. 29). The reticulum of depart for each sepal and three for each placental bundles is connected to both petal. Each stamen receives one bundle the ventral and the dorsal bundles. and each staminodium receives a single The walls of adjacent carpels are com­ bundle which branches into the arms pletcly fused except for the extreme (Fig. 10). ventral margins and the placental bundles Above the departure of the bundle of adjacent carpels arc also fused. There­ to each staminodium a single bundle fore, the same reticulum supplies the enters the fleshy central body where it ovules of adjacent walls of adjacent branches weakly and rapidly becomes carpels (Fig. 29). diffuse. This central structure (Figs. 9, Each dorsal bundle continues through 10) is considered in the (Discussion'. the style and into the stigmatic arms LIJfXOIJIUM Sl'OS(~IA (Bose) STEUD.­ where it branches. The ventral bundle, In this species the female flower is sessile which is a double bundle formed by within the inflorescence, which usually the fusion of adjacent ventral bundles, contains but one flower. Ascherson l\ also continues through the style and then Gurke (1889) reported only three stami­ branches into the walls of adjacent carpels nadia, as did Richard (1S11). Eichler which, from the level of the upper styles, (1875) reported three split antiscpalous arc not fused (Fig. 29). staminodia. Modern taxonomic manuals There is no plexus of vascular tissue give the number as three to six. The formed in the stylar region. The bundles writer has not observed fewer than six to the perianth, except for the abaxial and he found 7 or 8 not uncommon. sepal bundles and the staminodial There is a pair of staminodia opposite bundles, arc derived directly from the each sepal and often one or two single receptacular plexus. Bundles of stamino­ antipetalous starninodia. No fusion was dia and perianth segments which are op­ seen among the staminoclia. The order posite each other arc often fused from the of development is centripetal, with the rcccptacular plexus to the upper portion of paired members arising first. the style, where they separate (Fig. 17, The number of carpels varies from six sc-l-sto). Each staminodium receives a to nine. The ventral margins arc not single bundle which does not branch, fused although adj acent carpel walls and each petal receives three bundles. are fused almost to their margins (Fig. Each male flower is simply constructed 18). The ovules arc borne on the pro­ of 3 sepals, 3 petals, and 12 stamens in jecting carpel walls but not toward the 4 alternating whorls of 3 members each. ventral margins. There arc no ovules There is no evidence of paired stamens, along the dorsal region. or of staminodia, or of a rudimentary Three large vascular bundles occupy gynoecium. Tile stamens are monadel­ the central portion of the pedicel of the phous (Fig. 21). The order of matura­ female flower. Three smaller bundles tion, and presumably of origin, is are alternate with them and arc slightly acropetal. Hartog (1957) reported six farther from the center. Toward the partly connate stamens in L. stoloniferum. periphery there arc numerous smaller The three large bundles in the center bundles regularly disposed around the of the pedicel of the male flower of L. inner six. The outermost bundles arc sjJongia are surrounded by a ring of six the smallest (Fig. 20). Withiu the recep­ smaller bundles, three of which are oppo­ tacle the six inner bundles arc expanded site, and three alternate, with them. and form a ring of vascular tissue (Fig. These nine bundles form a receptacular 19). The first bundles to depart from plexus. The three large bundles become this ring serve the staminodia and the completely fused with the three smaller perianth. Above the departure of those ones opposite them while the three small bundles the dorsal and ventral carpel alternate bundles are only weakly united bundles depart. At this level a few La the plexus. These latter supply the small bundles leave the receptacle for petals. All of the sepal bundles arc the carpel walls. These are the placental derived from the plexus. 1968 J E AIJL - HYDROCIL\lUT,\CEAE 21

Each of the four whorls of stamens is vascular supply to the ovules in adjacent supplied from successively higher levels carpels. The ventral bundle is therefore of the plexus. Each stamen receives a interpreted here as representing the fused single bundle which departs from the ventral bundles of adjacent walls of plexus individually; there is no fusion adjacent carpels. or branching of the stamen bundle. There The vascular anatomy of the female is no vascular suggestion of a rudimentary flower of H. morsus-ranae is well illus­ gynoecium (Fig. 21). . trated with transverse views by Saunders HYDROCH.1RIS JtORSUS-RASAE L.- The (1929). The reader is referred to the genus Hvdrocharis is similar to Linino­ illustrations of Limnobium spongia (Figs. bium. There is a single female flower 16-20, 29) in which the vasculature is in each female inflorescence. There are similar. six subulate, free staminodia arranged The interpretations of the androecium in antisepalous pairs, and there is a large in the male flower of H. morsus-ranae bilobed nectary at the base of each petal. arc various. Rohrbach (1871) considered Six carpels arc present, In all specimens it to represent four centripetally arising examined by the writer adjacent carpel whorls of three members each. Richard walls within the ovary were fused almost (1811) saw only six stamens, each split to their margins. This interpretation into two members on the same radius. is contradictory to that of Aschcrson He interpreted the outer stamen as bear­ & Gtirke (1889) and others. Saunders ing two anthers and the inner stamen as (1929) and Eber (1934), however, saw bearing a single anther on its outer such fusion. branch; he interpreted the inner branch According to Rohrbach (1871) the as an appendage. Rohrbach (1871), Eichler paired staminodia arise as a single pri­ (1875) and Ascherson & Gtirke (1889) mordium which soon bifurcates. The called the sterile branches staminodia. carpels arise in two whorls of three each, Rohrbach (1871) presented convincing the outer whorl opposite the petals and ontogenetic evidence that there is no the inner whorl opposite the sepals. branching of the stamens. He showed After the appearance of the carpels a that each member of a so-called branched nectary arises between each petal and stamen arises independently and that the carpel opposite it. ontogenetic fusion of members on the There is a system of small peripheral same radius produced the apparently bundles in the pedicel of the female flower. forked stamens. He demonstrated that These serve the abaxial surfaces of the the anrlroecium arises in four alternating sepals. Above the departure of the whorls of three members each, with the bundles to the bracts the confused recep­ inner whorl being staminodial. Daumann tacular plexus rapidly sorts itself out. (1931a) believed the fleshy central body About a dozen small bundles leave the of the male flower to represent the inner­ plexus and proceed up the ovary wall. most androecial whorl fused with three These branch variously and serve the antipetalous rudimentary carpels. He sepals, staminodia, and ncctaries directly. observed some specimens in which The dorsal, ventral, and placental bundles stigmatic branches could be seen in the depart just above the departure of the middle of the male flower. These branches perianth bundles. The single dorsal were surrounded by fused staminodia, bundle of each carpel continues un­ STRATJOTI,S ALO]])ES L.- The six carpels branched into the stvle where it branches of the female flower have been shown to and serves both stigmatic arms. The arise in two whorls of three each, the ventral bundle continues into the lower lower whorl being antisepalous (Rohrbach, stylar region and then branches into the 1871). The projecting walls of adjacent styles of two adjacent carpels. The carpels are not fused, and the ovules are placental bundles are attached to both borne on the projecting walls except at the dorsal and the ventral bundles. Fur­ the margins. There are no ovules along ther, each reticulum of placental bundles, or near the dorsal bundle. About 15 to and each ventral bundle, provides the 30 starninodia occur between the perianth 22 PHYTOMO!(PHOLOGY [ :\larch and the carpels. They are united laterally three bundles, the central one of which into groups of three or more. According passes almost to the tip of the structure. to Rohrbach (1871) they arise in two The author has been unable to positively whorls, the upper whorl antisepalous identify trunk bundles serving groups of and the lower antipetalous, with the stamens or nectary-staminodia. lower arising first. Salisbury (1926) con­ THALASSIA HFMPRICHII (EHRENB.) As­ cluded, after examining transverse sec­ CHERSON- The female flower of this tions, that it is the upper whorl that is marine plant possesses three perianth an tipetalous, segments. The position of each opposite Each carpel has a single dorsal bundle. a pair of staminodia suggests that they The ventral bundles are on the same are sepals. There are six small suhulate circumference as the dorsal bundle and staminodia in the female flower. Stami­ they arc not fused with those of adjacent nodia appear not to have been recorded carpels. A diagrammatic illustration of previously in this genus. The flower the gynoecium is given in Fig. 70. The has six carpels and six styles, each of numerous placental bundles form a com­ which branches into two very long stig­ plex network attached to both the dorsal matic arms. Adjacent walls of adjacent and the ventral bundles in numerous carpels are not fused within the ovary places. The placental bundles of ad­ (Fig. 25). jacent carpels are not at all fused. The Thalassia tesiudinum is the only other ventral bundles and some of the placental species in the genus. It is reported by bundles pass directly through the style Hartog (1957) to have 9 to 12 undivided and serve the stigmatic arms with nume­ styles. The author has not seen speci­ rous bundles. The supply to the perianth mens of this plant. and the staminodia is derived from the The three large bundles of the pedicel bundles located in the outer portion of of the female flower of T. hembrichii are the ovary wall. These bundles depart expanded into a continuous ring of vascu­ independently of the dorsals and ventrals lar tissue within the receptacle (Figs. from the receptacular plexus. Each of 26, 27). Three bundles depart at the the staminodia receives two or three tiny same level from the lower part of this bundles from the single trunk bundle ring. Each of these bundles continues which supplies a group of three or more of un branched through the ovary wall and them. enters a sepal (Figs. 22-25). Above the The male flower of Straiiotes possesses departure of the sepal bundles the bundles 12 stamens and about 24 nectary-stami­ serving the carpels and the staminodia nodia. Rohrbach (1871) studied the leave the receptacle. Some of these ontogeny of the male flower and found bundles serve both as carpel dorsal bundles that, after the initiation of the petal and as staminodium supplies but others primordia, the paired an tisepalous sta­ serve a staminoclium directly (Figs. 22­ mens arise as a single primordium. A 24, sto). A weakly developed system of single antipetalous stamen arises later ventral and placental bundles is derived and above the paired stamens, and finally from the receptacle (Fig. 24). Some of a single antisepalous stamen arises above the ovules are also supplied by tiny each antipetalous stamen. Thus, there branches from the ventral bundles. In is a regular centripetal development of the five specimens studied by the writer alternating whorls of fertile stamens, no two adjacent carpels bore ovules. The the outer one of which consists of six stylar region is served not only by the paired stamens. After the last whorl dorsal bundles and the perianth-stami­ of stamen primordia has arisen, about nodia supplies, but also by the weak 24 primordia form between the pcrianth ventral bundles. There IS no stvlar and the outer whorl of stamens. They plexus. • arise in two whorls, just as in the female ENH.4LCS ACOROID]';S (L.) RICH. EX. flower (Rohrbach, 1871). STEUD -- Each female flower of this Each stamen receives a single bundle marine plant has three green sepals and each ncctary-staminodiurn receives and three very long and crinkled white 1968 J h.,\lJL - HYDROCtL\TUTACEAE 23 petals (Fig. 15). There are six carpels and Hundreds of tiny male flowers are borne six styles which bear two long stigmatic in each submerged male inflorescence. branches. Toward the base of the ovary Each is simply constructed of three sepals, adjacent carpel walls arc fused bv three petals, and three stamens (Fig. 14). their abaxial surfaces and their ventral There are no staminodia or rudimentary margins arc united at the center of the carpels. ovary. A 6-chambered ovary is thus The vasculature of the male flower is produced at this level by the~e fusions. equally simple. A single pedicellar bundle A similar condition was seen in Limno­ branches in the receptacle and provides bium spongia, Cunnington (1912) reported each stamen with a single bundle. There a small vascular column in the center of is no vascular tissue in the perianth. the base of the ovary. The writer has VnusNERIA AlvIFRICANA MrcHx.-The been unable to discover such a column genus V'allisneria is variously interpreted in any of his material from Singapore. as including 6 to 10 species. A single Two large bundles occupy the center sessile female flower is borne in the inflo­ of the aerenchyrnatous peduncle of the rescence of the female plant. The flower female inflorescence, which possesses but has three tiny scarious petals alternate one flower. Around these two bundles with the larger sepals. Three tiny stami­ there are numerous smaller peripheral nadia are alternate with the petals (Fig. bundles which serve the abaxial surfaces 32). The writer has observed occasional of the bracts. Each of the two large antisepalous pairs of staminodia (Fig. 34). bundles of the peduncle provides each Subramanyam (1962) reported bifid sta­ bract with three main bundles. Above minodia in V. spiralis. the departure of the main bract bundles The ovary of V. americana consists of the two large peduncular bundles form three carpels whose margins projeet a a weakly developed receptacular plexus short way into the locule (Fig. 36). These (Fig. 13). From this plexus about 12 margins are rapidly crushed and obscured bundles run almost horizontally to the by the developing ovules. The numerous periphery of the receptacle where they ovules are borne in the area of bending turn upward and, passing unbranched of the carpel walls (Figs. 33, 36). The along the ovary wall, serve the pcrianth. identity of the carpel is maintained in There are no staminodia, the style. The stigmatic arms are short Immediately above the departure of and blunt; at anthesis they are greatly the perianth bundles the six carpellary reflexed. bundles leave the plexus. At the base of A single bundle occupies the center of each carpel each hundle divides into one the peduncle of the female inflorescence. dorsal and two ventral bundles (Fig. 30). A single large bundle is at the periphery The ventral bundles continue into the and two smaller bundles are also at the stigmatic arms hut the dorsal bundle periphery alternate with the central and branches and becomes diffuse in the style the larger peripheral bundles (Fig. 39). (Figs. 11, 13). The dorsal and ventral At the level of attachment of the bracts bundles are connected by several small these four bundles form a plexus in which but well-defined bundles (Fig. 30). The their identities are lost (Fig. 38). From placental bundles arc connected at several this plexus four large bundles serve the places with the ventral bundles and some bracts. Above the departure of the bract of them originate below the point of bundles the plexus becomes organized divergence of the dorsal and ventral into three large bundles of similar size. bundles. Ordinarily only two ovules are These three bundles occupy the same formed in each carpel. Each is attached radii as the sepal median bundles (Figs. on or near a ventral bundle and at a 34-37) and they are located at the point different level from that of the other ovule. of fusion of adjacent carpels. One or all The ventral bundles of adjacent carpels of these bundles may be inverted. From are not fused with each other (Fig. 12). each of these bundles a branch departs These bundles were termed "marginal and fuses with a similar branch of an bundles" by Cunnington (1912). adjacent bundle (Fig. 37,d). The product 24 PHYTCnmRPHOLOGY I March of this union occupies a median position 32). The vascular supply to the ovules in the carpel wall and is, therefore, the is derived mainly from the three large dorsal bundle. The dorsal bundle forks bundles opposite the point of fusion of again towards the upper part of thc ovary adjacent carpels (Fig. 33). These bundles and each branch then reunites with its are the fused ventral bundles of adjacent parent bundle in the stylar region (Fig. carpels. Each of these bundle: supplies

Figs. 32-52 1968 J KAUL - HYDROCHARITACEAE 25 the ovules of adjacent walls of adjacent that this is an artificial division because carpels. There are occasional vascular the male flower of dioecious species pos­ connections between the ovules and the sesses three stylodia and the female flower dorsal bundle (Fig. 33). At the upper sometimes possesses one or more stamens. part of the ovary the bundles of the ovary The writer has examined only mono­ wall are approximate. The sepal bundles, ecious species which show a single flower one to each sepal, depart quickly from in the inflorescence. Each flower posses­ the converged bundles (Fig. 32). The ses three sepals, three petals, and three, identities of the bundles serving the petals, six, or nine stamens (Figs. 41, 47). In staminodia, and styles arc obscured the species examined here, H. auberii briefly in the congress of bundles but Rick and B. aliernifolia (Miq.) Hartog, they depart quickly (Fig. 32). There there arc three stamens. is no dorsal bundle in the upper portion The ovary consists of three carpels of the style. whose walls project a short distance into Numerous tiny male flowers arc pro­ the locule (Figs. 44, 49, 52). The ovules duced in the submerged inflorescence. are borne in the region of bending of the In V. americana the male flowers have carpel walls. There arc three styles three sepals, a single petal, two stamens, which do not branch but bear filiform and one staminodium (Fig. 40). Hartog stigmas. (1957) reported three petals in the male 13. .tLTlJ:SIFOLI.1 (Miq.) HARTOG - flower of V. gigantca. H.ichard (1811) There arc two large bundles in the pedun­ illustrated a single organ alternate with cle of B. alternifolia. Each of these the petals in V. spiralis ; presumably it supplies a bract with one bundle. Above is a petal. He also showed three organs the departure of the bract bundles the opposite the sepals; their nature is un­ two peduncular bundles become ex­ known to the writer. Subramanvam panded and lose their identities (Fig. 46). (1962) observed that the structure ot the From the plexus formed by them three male flower of V. spiralis is the same as bundles depart on the sepal radii (Fig. that of V. americana. 44). Each of these bundles soon branches The writer was unable to discover any to form two bundles of unequal size vascular tissue in the male flowers of II. located on the same radius (Figs. 44, 45). americana. The outer and larger of these courses up HLi'XA THOL\I~S - The genus Blyxa through the ovary wall without branching comprises about ten species. Aschcrson until it disappears in the stylar plexus. & Gurke (1889) divided the genus into The inner, smaller bundle runs parallel two sub-genera: Saiuala (dioccious, 6-9 with the outer bundle and is the source of stamens),· and Diplosipholl (monoccious, the vascular supply to the ovules (Figs. 3 stamens). Hartog (1957) pointed out 44, 53). This bundle is located opposite

+--

Figs. 32-52··- Vollisncria and Blyx a (d, dorsal bundle; p, petal bundle; SC, sepal bundle; st, stamen bundle; sto, staminodium : ou, fused ventral bundles of adjacent carpels). Figs. 32-40. Vnllisncria amcrican.a . Fig. 32. Drawing from cleared specimen and serial sections of upper por­ tion of female !lower; stigmatic branches still apprcsscd before anthesis. X 50. Fig. 33. Mid­ portion of o varv at an Lhevis showing dorsal and fused ventral bund lcs (slightly exaggerated for emphasis) and slig11th' projecting carpel wall«. X 75. Figs. 34-39. Serial sections through female inflorescence. x 20. Fig. 34. Pcriarith. Fig. 35. Stvlar region showing vascular plexus. Fig. 36. Ovary. Fig. 37. Receptacle, fused bracts shown. Fig. 38. Upper peduncle. Fig. 39. Peduncle. Fig. 40. Male Hower. 20. Figs. 41-46. Blyxa alternifolia., serial sections through flower. x 35. Fig. 41. Pcria.n t h. Fig. 42. Stvla.r region wi t h vascular plexus. Fig. 43. Stylar region below plexus. Fig. 44. Ovary. Fig. 45. Base of ovarv at level of separation of ventral bundles from bundles to pcrianth and androecium. Fig. 46. Pedicel. Figs.47-51. Blvs a auberti, serial sections of flower. X 50. Fig. 47. Perianth. Fig. 48. Upper st.y lar region. Fig-. 49. Ovary. Fig. 50. Base of ovarv at level of separation of ventral bundles and supply to sepals and androeciurn : petal and dorsal bundles h ave alreadv departed. Fig. 51. Pedicel. Fig. 52. Blysa sp., ovary slit opcn to show arrangcment of ovules along the slightly projecting carpel walls. X 2.5. 26 l'H1TO:\lORPHOLOCY t, March the point of fusion of adjacent carpels H.1WPHIL:1 Ol"ALI'l (R. BR.) HOOK. F.­ and, because it supplies the ovules of 11alaplzila is a marine genus of nine spe­ both adjacent carpels, represents the cies, according to the most recent study fused ventral bundles of those adj acent (Hartog, 1<)59). Vegetative differences carpels. There is no dorsal bundle in among the species are pronounced but, the ovary. as far as is known, the ftoralmorphologies The three double ventral bundles and are quite similar. I examined only H. the three larger outer bundles unite in oualis in detail. a weak plexus at the top of the ovary The female flower of H. ooalis is sessile (Figs. 42, 43). The bundles do not com­ and has a perianth of three segments. pletely lose their identities. From this The ovary consis ts of three carpels whose plexus three bundles proceed to each fused adjacent walls project very slightly sepal and three bundles enter each petal. into the ovarian cavity (Fig. 58). Bal­ One bundle enters each stamen and each four (1879) correctly interpreted the style, where it occupies the median posi­ structure of the ovary although he con­ tion (Fig. 53). It is likely that this sidered the plant to belong to the Naiada­ median stigmatic bundle represents the ccac. He described three parietal carpel dorsal bundle even though there placentae, each bearing two rows of ovules. is no dorsal bundle in the ovary. These placcnt.ac arc easily detected in B. A UIiJ-:NTI RrcH.- Two larg~ bundles young specimens (Fig. 58) but they arc occupy the center of the peduncle of D. quickly distorted by the growth of the aubcrti. Each of these bundles sends ovules (Fig. 55). There is a very long one branch into one of the bracts. Above stylar region composed of the fused styles the departure of the bract bundles the of the three carpels. The styles separate peduncular bundles form a receptacular at the level of the perianth and each plexus of vascular tissue (Fig. 51). The bears a long filiform stigma (Fig. 56). plexus immediately gives rise to six The stigmas are receptive on their inner bundles which run up the ovary wall. grooved surfaces for their entire lengths. Just above the departure of these six Above the departure of the bundles to bundles three more bundles depart oppo­ the bracts the peduncle of II. oualis con­ site three of the lower bundles (Fig. 50). tains a single large central bundle. Thus, there are nine bundles in the ovary Within the receptacle this bundle pro­ wall, six of them in pairs on the same duces six branches. Each of the three radius. The inner bundle of each pair lower branches, which depart at the same provides the: vascular supply to the ovules level, provides the vascular supply to of adjacent carpels and represents the; one of the three perianth segments and fusion of ventral bundles of adjacent to the dorsal region of the style (Fig. walls of neighbouring carpels (Fig. 49, 57, pc d). The three upper branches vv). When these fused ventral bundles of the peduncular bundle provide the reach the level of separation of styles vascular supply to the ovules. Each they separate and each branch proceeds of these branches serves ovules in adja­ into the style of one carpel. The outer cent carpels and represents the fusion of bundle of each pair, as seen in the ovary ventral bundles of adjacent walls of branches in the stylar region and sends adjacent carpels (Fig. 58, vv). The ven­ three bundles to a sepal and one bundle tral bundles end in the stylar region. to a stamen (Figs. 47-49, 53, sc-j-st). The male flowers of II. ooalis are pcdi­ Each of the single bundles in the ovary celled an d consist simply of three perianth wall, upon reaching the upper stylar segments and three stamens alternate region, branches and provides a petal with them (Fig. 54). The single pedi­ with a single bundle and also provides cellar bundle sends one bundle to each the style with a dorsal bundle (Fig. 53). of the three pcriarith parts. Above the Therefore, the single bundle, as seen in departure of the perianth bundles a single the ovary, represents the fusion of the bundle passes into each of the three carpel dorsal bundle and the petal bundle. stamens. There are no bundles which There is no stylar plexus. might suggest a vestigial gynoecium. 1968 J KAUL - H\'DROCHARITACEAE 27

Figs. 53-68- Blvx«, Hvdrilla, Elodea and Halophila (d, dorsal bundle: p, petal bundle: »« periauth bundle ; SI', sepal bundle; sf, stamen bundle; sio , staminodium : vv, fused ventral bundles). Fig. 53. Diagrammatic rcprescuta.tion of vascular supply in the flowers of Blyxa auberii and B. alt eruifolia ; drawn as i [ the fl owcrs were split open and l1attenecl above t he receptacle. In B. aubcrti the dottl~clli;le represents se+st only; in B. alternifolia it represents se+st+p+d, and there is no p +d; not drawn to scale. Figs. 54-58. Halophila oualis, Fig. 54. Male flower. X 6. Fig.55. Large mature fruit showing attachment of seeds (stippled line) and bundle serving dorsal portion of carpel and periauth. :< 10. Fig. 56. View of female ilower at arrthesis. X 4. Fig. 57. Stylar region showing tricarpcllate nature of g"lIoeciulll. 14. Fig. 58. Fertile region of ovary. X 14. Figs. 59-62. Hvdrilla rcrtic.illa!«. Fig. 59. Ovarv opened to show attachment of ovules along fusecl ventral buud lcs. >~ 20. Fig. 60. Section through pcrianth; a pair of starninodia is seen in one position. X 20. Fig. 61. Stvlar region with vascular plexus. X 20. Fig. 62. Section across fertile region of ovary. X 20. Figs. 63-68. Elodea. Fig. 63. E. canadensis, ovary opened to show attach­ ment of ovules along ridges formed In' fusion of adjacent carpel walls. X 20. Fig. 64. Section across stylar neck region showing slight fusion uf bundles. x 65. Fig. 65. Section across pcriarith region showing staminodia. 65. Fig. 66. Section throngh ovary showing attachment of ovules at sides of ridges; nute the slime gland cells Oll ridges. 65. Fig. 67. E. den.sa, male, showing disposition of stamens. X 15. Fig. 68. Section slightly lower than Fig. 67 showing slight monadelphy. X 15. 28 Pl-lYTO~10RPIIOTJ)GY [ March

EWJ)[~.l JTICHX.--- Elodea is a ~ew World The vascular anatomy of the male genus variously interpreted as contain­ flower of E. densa is as simple as its gross ing 5 to 10 species. The female flowers morphology. A single bundle passes possess three sepals and three petals and from each of the three pedicellar bundles often three, and sometimes six, stami­ into a sepal. Above the sepal bundles, nodia (Fig. 65). T11(:s(' staminodia are and alternate with them, a single bundle occasionally fertile (Wylie, 1904). The passes into each petal where it branches ovary is composed of three carpels, a into three. At successively higher levels feature correctly recognized by Van within the receptacle the three whorls Tieghem (1891) but generally overlooked of these stamens each is provided with before and since. The lateral portions of bundles. Tiny bundles pass into each each carpel are fused with adjacent lateral lobe of the central body; each of these portions of ad jacent carpels and the bundles is opposite a petal. The ex­ products of these fusions are three slight tremely reduced nature of the central ridges on the inner surface of the ovary body obscures its true character. How­ (Figs. 63, 66). The ovules arise at the ever, I interpreted similar but more fully sides of these ridge" and as they grow they developed structures in Boottia as fused assume a pseudo-terminal position on starninodia. them. The terminal portion of each ridge HYl!JULLA j'/';RTfCIUATA (L.) ROYLE­ is occupied by mucilage cells (Fig. 66). Hvdrilla is a monotypic monoecious or Above the level at which the single dioecious genus with unisexual flowers. central peduncular bundle of E. canadensis The female flower is borne singly within provides each of the two fused bracts the inflorescence and possesses three with a single bundle, three bundles pass sepals, three petals, and three slightly into the: ovarv wall. Each of these thrc« bifid styles. Neither Caspary (1858), bundles is loc:tted within the ridge formed Hartog (1957), nor Subrainanyam (1962) by the fusion of carpel walls, and each mentioned the presence of staminodia is the source of the vascular supply to the but Ascherson & Gtirke (1889) said there ovules on adjacent walls of neighbouring are sometimes three but more often none. carpels (Fig. 66). There are no dorsal All specimens examined by me had at bundles. In the stylar region these least three staminodia, and often one of three bundles form a ring of vascular these was replaced by a pair (Fig. 60). tissue (Fig. 64). From this ring one The ovary consists of three carpels whose bundle passes into each of the three sepals margins are not at all protruded into the and, just above, into each of the three locule (Figs. 59,62). The ovules are borne petals. Then a single bundle passes into at the point of fusion of adjacent carpels. each staminodium and a single bundle The single central pcdicellar bundle into the dorsal position of each style. produces the three bundles seen in the The stvlar bundle then forks and a branch ovary \'\'a11 in Fig. 62. Tiny branch proceeds to each stigmatic arm. bundles serve the ovules from these large The male flowers of Elodea possess bundles. The three bundles form a ring three sepals, usually three petals, and of vascular tissue in the stylar region three or nine stamens. Tn E. canadensis (Fig. 61) and six bundles pass upward the nine stamens are slightly monadel­ from this ring. Three of these six serve phous (Fig. 68), but in E. dcnsa they are the sepals. Each of the other three, free. In some species, e.g. E. canadensis, alternate with the sepal bundles, pro­ the male flower is tiny and breaks from vides a petal with a single bundle and the inflorescence bdoI-e anthesis. Wylie provides the style opposite that petal (1904) reported well-developed stigmas with a tiny dorsal bundle. The three in some staminate flowers of E. canadensis; bundles seen in the ovary represent the Eichler (1875) called them staminodia. fused adjacent ventral bundles as well as The large fleshy structure at the center the entire supply to the perianth. The of the male flower of E. densa (Fig. 67) dorsal bundle is reconstituted above the was interpreted by Casparv (1858) as a stvlar plexus. The st aminodia lack vas­ rudimentary gynoecium. cular tissue. 1968 l l\Al:L - HYDEOCH.\H.ITc\CE.\E 29

The tiny male flower is also horne walls. He showed the ovules ans111g all singly in each inflorescence. It is simply over the inner surface of the ovary. constructed of three sepals, three petals, According to Rendle (1916) the male and three stamens, all in alternating flowers are each reduced to a single sta­ whorls. The vasculature of the male men, with no trace of a perianth, If flower is extremely simple. From a the male flowers are truly as he depicted single pedicellar bundle single bundles them, they then represent the most pass, in alternating whorls of three and reduced flower in the entire Iamilv. at successively higher levels, to the sepals, Rcndlo, however, examined onlv dri~d petals, and stamens respectively. material and my experience with dried Nic'CHA MAXlJNA A Ul-HSlIUU.l (1\OXB.) material of tinv male flowers of other THw.-- The female flower of N cchamandra genera shows that the perianth readily possesses three perianth parts and three falls away. bilobcd stigmas. The ovary consists of Rendlc v believed the genus to show three carpels whose fused walls projcct great affinity with V'ailisneria, and Dandy a slight distance into the locule. The (1959) placed it in that genus. ovules arc borne at the region of turning of the carpel margins. A single bundle Discussion passes through the small ridge formed by fusion of adj accnt carpel walls. The The pcrianth of the Hydrocharitaceae ovules are borne directly on these bun­ shows several specializations. The most dles, which represent the fused ventral conspicuous of these is a tendency toward bundles of adjacent carpels. There is reduction in size and number of segments. no dorsal bundle within the ovarv, The basic pattern in the family is the The author has not seen male~ flowers possession of three sepals and three petals of N echamandra. According to Subra­ but this is sometimes reduced by loss of mallyam (1962) they are very similar to entire whorls, as in H alophila oualis and the male flowers of Vollisneria. Thalassia hem brichii, or parts of whorls, LAGAROSIl'HOX HARVEY -- I did not as in the male flowers of N cchamandra study the vasculature of the flowers of and Vallisneria. At least five, and often Lagarosibhon but the illustrations pro­ more, bundles serve the sepals of Oitelia vided by Harvey (1842) in his original alismoidcs, female Boottia cordata, Enhalus description of the genus suggest that and Lininobium spongia, but in the tri­ the basic pattern is the same as that of carpcllate genera, except for Blyxa, the N cchamandra, at least as far as the female sepals receive but one bundle. The flower is concerned. According to his perianth of H alophila oualis lacks vascular illustrations, the ovary is interpreted tissue altogether. A similar variability here as composed of three carpels whose is found in the petals where one, three, fused adjacent walls project very slightly five, or no bundles can be found. A into the locule. \Vager (1928) studied single bundle serving each petal can be the morphology and anatomy of the seen in female Limnobium spongia. This genus and his illustrations of the female bundle passes independently from the flower agree with those of Harvey. receptacular plexus through the ovary The male flowers also possess three wall and into the petal. It is likely that sepals and three petals. There are three all the genera have similar single-trace fertile stamens and three filiform starni­ petals but in most of them this trace has nodia (Harvey, 1842). Structures similar become obscured by fusion or by branch­ to these staminodia arc seen in the male ing within a stylar plexus, or has been flowers of dioccious species of Blyxa; lost altogether. The loss of the corolla of Hartog (1957) called them stylodia. Thalassia and Halophila is probably cor­ AfAl/)/,XJ.1 RUW..4 I<'E:\])LE- This is a related with underwater pollination and little-known monotype from north-wes­ not with the marine habitat. Enhalus, tern Australia. Rcndlc's illustration of a the third marine genus, is pollinated at cross-section of the ova.rv shows that 110 the surface and has one of the showiest trace remains of the projecting carpel corollas in the family. 30 PH'y'TO:\lORPHOLC)GY [ March

No evidence of more than one bundle of stamens are also sterilized in some in a stamen is seen in the fertile stamens cases. His study of numerous flowers led but there are three bundles in the stami­ him to conclude that there are three nodia of H vdrocliaris morsus-ranae and general types of staminodia and that some Siraiiotcs. in male Hvdrocharis flowers of them are outside the fertile stamens, some of the stamens, particularly those of with numerous transitional forms exist­ the penultimate whorl, are bisporangiat«. ing among the types and between the That this bisporangiate condition is not staminodia and fertile stamens and nec­ the primitive condition but is brought taries. He concluded that these struc­ about by the failure of two sporangia tures could not be interpreted as any­ to develop, rather than by all ontogenetic thing but androecial in nature. Rohr­ or phylogenetic splitting of a stamen, bach (1871) interpreted them as axial is sllggrstcd by the frequent develop­ structures not related to the androecium. ment of partially or completely deve­ Mv observations on the vascularization loped third and fourth sporangia in sta­ of these structures in Stratiotcs add fur­ mens in which but two would be expected. ther credence to Daumann's interpreta­ The reduction of the androccium in tion of them as starninodia. It must be both male and female flowers is roughly emphasized that the features attendant correlated with an increase in speciali­ upon the inferior ovary have somewhat zation of pollination mechanisms and obscured the pattern of vascularization with a decrease in size of flower. The to the perianth and androecium in the entomophilous genera generally have more female flower. and larger stamens and staminodia, and Other transformations of stamens into well-developed perianth, while the hydro­ ncct.ariferous staminodia can be seen in philous members have fewer stamens and female Boottia cordata and Ottelia alis­ rather inconspicuous perianths. inoides. In these the nectaries occur in The androecium of the tricarpcllate groups but each nectary has an independ­ genera comprises fewer members, gene­ ent vascular supply from the stylar rally, and the ultimate in reduction is plexus (Fig. 5). These structures arise reported in male M aidenia in which the below and after the stamens (Ottelia) or flower consists solely of a single stamen. :-: taminodia (Boottia). A tendency toward In most of the tricarpellatc g-enera the fasciation can occasionallv be seen in male flowers contain three functional the fertile stamens or non-nectariferous stamens and some have what appear to staminodia of these genera (Figs. 1, 6). be staminodia. 1n ~V ech.mandra and The morphological nature of the 6­ Vallisncria the single remaining whorl armed fleshy structure at the center of of stamens is partly sterile. the male flowers of Boottia cordata and The tendency toward sterilization of Hvdrocharis morsus-ranae is obscure. stamens is pronounced in the Hydrochari­ H.~hrbach (1871) thought it represents, taceac. The bisporangiate condition of in Ilydrocharis, two or three undeveloped the male Hvdrocharis morsus-ranae flower, staminodia. He based his conclusion and the complete lack of sporangia on on its origin below the floral apex but the innermost stamens of the same flower, above the last-formed whorl of well defin­ suggests that it is the innermost stamens ed staminodia. Daumann (1931a) found which are sterilized first. Further evi­ several specimens in which this central dence of this is seen in male Booitia cordata body appeared to envelop a rudimentary where the innermost whorl of definable gynoecium. He concluded that it re­ androecial structures is represented by presents the fused members of the inner large and forked staminodia, and in male androccial whorl and sometimes also a Stratiotes where the innermost whorl is rudimentary gynoccium. These inter­ sometimes represented by rudimentary pretations suggest that, with the deve­ stamens. lopment of unisexuality, the nectaries Daurnanri's (1931a, b) study of Hydro­ of the incipient male flowers retained, or charis rnorsus-ranae and Straiiotes, how­ possibly assumed, an uppermost position ever, suggests that the outer whorls within the androecium but that in the 1968 K.\(' L _. llYDROCH.\IUTACEAE 31 female flower they remained crowded Under this interpretation transitional toward the outside. Further evidence conditions can he seen in Hydrocharis in support of this interpretation is the morsus-ranae in which both sexes possess fact that these structures, regardless of paired androecial organs, and in male their position, always arise after all other Stratioies flowers with their paired anti­ stamens or well-defined staminodia have scpalous stamens. The female Siratiotcs arisen. Furthermore, I observed that flower, with its numerous grouped stami­ the vascular supply to the uectaries of nodia, is then interpreted as a primitive female B ooiiia cordata, and Otielia alis­ type. moides is derived from the stylar plexus On the basis of my observations in the slightly above the supply to the stamens H vdrocharitaccae and in the related or to other staminodia. I am, therefore, Butornaceac I suggest that the solution led to conclude that these ncctaries are to the problem of the origin and actually the uppermost portion of the significance of paired stamens is to be androecium. found in the progressive reduction of Meristic reductions in the male and stamen fascicles and not in the addition female flowers have generally paralleled of new organs through phylogenetic each other. Those genera with the most splitting. There is external evidence of numerous fertile stamens in the male fasciation in the female flowers of Stra­ flowers tend to have female flowers with tiotes. Other evidence of fasciation is numerous staminodia, e.g. Stratiotes, seen in the androecia of Bootiia cordata Reduction in the number ·of androecial and Otielia alismoides, with their fused members has produced constant but ncctarics, stamens, and staminodia. rather a large number of stamens and Until 1930 the standard interpre­ staminodia in Bootiia, Lininobiuni and tation of the hyclrocharitaceous gynoe­ Ottelia. In these and other genera conti­ cium was that it is syncarpous and uni­ nuing basipetal sterilization and loss of locular with split parietal placentae. stamens are seen. The result is that in Rohrbach (1871), Ascherson & Gurke the tricarpellatc genera there arc three (1889), Svcdelius (1904), and Cunnington or no staminoclia in tho female flowers (1912), among others, espoused this inter­ and four, three, one or none in the male pretation. In 1931 Troll, in the first flowers. Further modifications, such as comprehensive survey of the gynoecium sterilization of one or two of the remaining in the family, interpreted the gynoe­ fertile stamens, have produced such forms cium as apocarpous and the so-called as male Vallisneria. split placentae as wings of adjacent car­ Antisepalous pairs of stamens or starni­ pels. He postulated the development of nodia are seen in Oiiclia alismoidcs and the hvdrocharitaceous from a buto­ in the female flowers of B oottia cordata, maceo~s type of gynoecium by a termi­ Hvdrocharis morsus-ranae, Limnobium nation of apical growth accompanied spongia, Thalassia hemprichii and in by continuation of growth of a torus. male Stratioics. Thev abo occur occa­ In this process an ovary would be pro­ sionally in the female~ flowers of Hydrilla duced in which the carpels are united by and Vullisneria. There arc no stami­ the central portions of their abaxial sur­ nodia in the female flower of Enhalus, faces to axis tissue. The lateral portions and the arrangement of the stamens in of the carpels and their ventral margins the male flower of Thalassia hemprichii are not fused according to this interpre­ is unknown. A comparison of the male tation. Therefore, the carpels are free and female flowers of Stratiotes with those from each other, although each is united of Boottia cordata and Lininobiuni sjJongia, to a common wall, and an apocarpous but and with the bisexual flowers of Ottelia in Icrior gynoecium exists. alismoides, suggests that an tiscpalous Mv observations on the morpho­ stamen pairs arc an intermediate condi­ logy' and the vasculature of the gynoe­ tion and that, with the development of cia of most genera, while agreeing in unisexual flowers, the normal (unpaired) many ways with Troll's, suggest that condition is attained in the male flower. some modifications of his interpretations 32 PHY'l'O:\IORPHOLOGY [ .:\tarch

are necessarv. Evidence from vascular in Fig, 18 as ventral bundles which are anatomy suggests that the fusion of fused. However, their position so close abaxial carpel surface to non-carpcllary to the carpel margin, unlike the ventral tissue of the ovary wall is more complete bundles of other genera of the family, in some genera than in others. For suggests that they arc merely placental example, in Limnobium spongia and bundles, or perhaps false ventral bundles Thalassia liem prichii the bundles which in the sense of Moseley (1965). The supply the pcrianth and staminodia are larger size and well defined course of not fused with the dorsal and ventral these bundles seems to set them apart bundles of the carpels as they are in from other placental bundles. Bootiia cordata and Olielia alisnioidcs. Kausik (1940) concluded, OIl the basis In Blvxa alter nijoiia the bundles to the of anatomical studies in Enhalus, that porianth and androccium arc not fused the outer portion of the ovary wall is with those of the carpels, but in B, auberi! made of the fused basal portions of the the dorsal and petal bundles are fused petals and sepals. He noted that the and the sepal bundles arc independent. outer bundles of the ovary wall serve InElodea and Hydrilla the vascular supply the perianth and not the carpels and to the pcrianth and starninodia is derived he considered this to be evidence for from three bundles, each of which repre­ the appendicular nature of the ovary. sents the fusion of two 'ventral bundles :My observations on Enhalus agree with and the perianth and androccium supplies. those made by Kausik. Furthermore, In Booitia cordata, Oilelia alismoidcs I have observed similar conditions in the and all the tricarpellatc genera, the vas­ o th er genera. On the basis of currently cular supply to the ovules of one carpel accepted concepts of the inferior ovary wall is abo the supply to t11O-;e of the (Douglas, 1944, 1957; Eames, 1961) I con­ adj acent carpel wall. On this basis the sider the inferior ovary of the Hydrochari­ ventral bundles of adjacent carpels arc taccae to be appendicular in derivation. presumed to be fused and thus to indicate In six of the multicarpellat.e genera a partially syncarpous gYTloccium in and in V'allisneria americana, the vascular the~'c genera. In young specimens these supply to the ovules is connected in fused ventral bundles divide once just several places with both the dorsal and below the separation of the fused styles. the ventra] bundles. Similar connec­ Each branch continue:' to a st vlc of all tions liavc been reported for a few dicoty­ adjacent carpel. Further evidence of ledons and the author has observed them syncarpy can be seen in Ottclia alismoidcs in Butonius. In these genera, except for where adjacent carpel walls arc obviouslv Valli ..sncria, the main source of the vascu­ fused for' a short distance, and in Eludc'a lar supply to the ovules is not directly canadensis where ad] accnt carpel walls from the ventral bundles but directly form low ridge:-:. on the ovary wall. In from the rcccptacular plexus. It IS Enhalus and in Straiioies the ventral probable that these placental bundles bundles are not fused and the gynoecium arc derived from a single principal bundle is apparently apocarpous (Fig. 12). The below the level at which that bundle gynoecium of Thalassia hemprichii ap­ gives rise to th c dorsal and ventral bundles pears to be an intermediate form in which but that such a pattern is obscured at some ventral bundles arc free and others anthcsis. arc fused. The general primitiveness of the multi­ Other evidence of syncarpy in the carpellatc genera, and a similar primitive­ Hvdrocharitaceac is seen in Limnobium ness ill Limnocharis, suggests that these spongia where the total fusion of adjacent genera possess the most basic type of carpel 'Nalls is obvious (Fig, 18). The ovule supply in both the Hydrochari­ fusion is so complete that the placental taccac and the Butomaceae. Using this bundles supplying the ovules in one car­ as a working hypothesis it is possible to pel also supply those of the adjacent car­ derive the Vallisneria type by a reduction pel wall. (have somewhat tentatively in number of ovules ,vith a consequent designated the bundles labelled "nn:" reduction in vasculature but nevertheless 1968 ] IC\UL -- HYDROCHARTTACEAE 33

retaining connections to the dorsal bundle. suggest probable patterns of reduction. Further reduction could lead to the sub­ A basic type consists of free carpels whose marginal Blyxa auberti type in which walls project almost to the center of the there are no connections to the dorsal ovary. Each carpel has one dorsal and bundle and then, finally, to the Blyxa two ventral bundles. This is the Stra­ alternifolia type in which the dorsal tiotcs type (Fig. 70). The ovules are bundle, as such, has disappeared distributed all over these projecting walls altogether. In this scheme it is the but are not found along the margins or ventral bundles which gradually assume along the midrib. The dorsal and the the function of supplying the entire flower ventral bundles of each carpel are located while the other bundles have either dis­ on the same circumference, a situation appeared or have fused with them. The which strongly recalls that of Limnocharis possibility that the evolution of laminal in thcButomaceae. \Vhether this dis­ placentation in the Hydrocharitaceac was position of bundles is the primitive condi­ by a phylogenetic expansion of the fertile tion in the families or is merely due to area from the sub-marginal position crowding of numerous carpels 1s impos­ seems remote when the vasculature and sible to sav at this time. morphology of the carpels in the entire A step i~1 reduction of the gynoecium family are considered. is the slight fusion of adjacent carpels Figures 69-77 represent the various and the total fusion of their ventral bun­ types of gynoecia in the family. Thcy dles. This is the Boottia type (Fig. 69).

Figs. 69 -77 - Types of gynoecia in the Hvdrocharitaceae ; clear circles arc dorsal bundles, blackened circles ventral bundles, single or fused; hatched circles arc bun d lcs to pcrianth and an­ d roecium ; supply to pcria nth and audroccium not ShO\\'1l for rnulticarpcllate types; all bundles shown for tricarpellate tvpcs. Fig. 69. Boottia. x 10. Fig. 70. Enhalus and Siratiotes, X 12. Fig. 71. Limnohium and Hvdrocharis . x 15. Fig. 72. Blyxa auberti . X 50. Fig. 73. Elodea. X 65. Fig. 74. Blyxa aliernifolia, X 55. Fig. 75. V'allisneria, X 18. Fig. 76. Halophila. X 18. Fig. 77. Hydrilla. X 25. 34 PHYTO;VIORPHOIJOGY [ March

Genera with this type mayor may not type could produce the Elodea type have the pcrianth and androecium bundles (Fig. 73), the Halophila type (Fig. 76) fused with the carpel bundles. Further and finally the Hydrilla type, with a reduction results in the gradual fusion, corresponding reduction in the number toward the margin, of adjacent carpel of ovules produced and in the prominence walls. This is the Ottclia type (Fig. 3). of the projecting carpel walls. Or, the carpel walls may remain unfuscd The tricarpella.te genera arc the most beyond the ventral bundles but may reduced in carpel and ovule number and become reduced in size as in the Blvxcl­ in vasculature. V'allisneria represents a Vallisneria type (Figs. 72, 74, 75). 'The transitional type between the multi- and ovuliferous area is thus greatly reduced. tricarpellatc forms. Of the genera Complete disappearance of the project­ studied in detail here Hydrilla possesses ing walls could produce the Hvdrilla type the most reduced gvnoccium. (Fig. 77). The carpels of all Jgenera of the family An alternative pattern is suggested are always open; the ventral margins bv the Limnobium type (Fig. 71). In are not even closely appressed or held this the presumed ventral bundles arc together by hairs. There is no evidence near the carpel margins and the carpel of a tendency toward carpel closure. On walls project to the cen tcr of the ovary t he contrary, the tendency is toward and arc totally fused bv their abaxial grcClter openness by reduction of pro­ surfaces. Stages in the r'eduction of this j ccting walls.

Liter-ature Cited

ASCIIERSON, P. & GURKE. 1\1. 1HH9. Hvclro­ ErCHLER, A. \V. 1875. Bluthcndiagramme. charitaceae. 1 n ENGLER, A. & PRc\NTL. K. Vol. 1. Leipzig. Die naturlichcn Pflanzcnfamilien. Vol. 2. HARTOG, C. DE='! 1957. Hydrocharitaceae. In Leipzig. V,\N STEENIS, C. G. G. J. (ed.) Flora Male­ BALFOUR, r. B. 1879. On the genus Halophila. sia.na. Vol. 5. Djakarta, Indonesia. Trans. Proc. bot. Soc. Edinb. 13: 290-343. 19.59. A k ey to the species of Halophile CASPARY. R. 1858. Die Hvdrillccn. .11). wiss, (Hydrocharitaceae), with descriptions of the Bot. 1: 377-513. . American species. Acta bot. rieerl. 8: CHEADLE, V. I. 1953. Independent origin of 484489. vessels in the monocotyledons and dicotv- HARVEY, \V. H. 1842. Account of a new genus ledons. Phytornorphologv 3: 23-44. ' of the natural order of Hvdrocharidcae from CUNND1GTON, H.:vI. 1912. AnatolllY of Enhalu« southern Africa. Hooker's J. Bot. 4: 230­ acoroides (Linn. f.) Zollo Trans'. Linn. Soc. 231. Land. B()t. 7: 355-372. 1(A1;SIK, S. B. 1940. Vascular anatomy of the DANDY, T. E. 1934. Note;; OIl Hvrlrocharitaccac. pistillate flower of Enhalus acoroides. Curr. 1. T'fle delimitation and' subdivision of Sci. 9: 182-184. Ottelia.. J. Bot, Lo n d , 72: 132-139. MOSELEY, lVI. F. 1965. Morphological studies 1959. Kev to the subfamilies, tribes, and of the Nvrnphaeaceae. lIT. The floral genera. {II HUTCHINSON, J. The Families anatomy o(Nupha1'. Phytomorphology 15: of Flowering Plants. Vol. 2. Oxford. 54-84. DAUMANN, E. 1931a. Zur Phylogenie dr-r RE:;DLE, A. 13.1916. Alaidenia: A new genus Diskusbildungen. Beitrage zur Kenntnis of Hvdrocharitaceae. J. Bot, Lond. 54: del' Nektarien. II. Beih. bot. Zb1. 48: 183­ 313-316. 208. RICHARD. L. C. 1811. Mernoire sur Ies Hvdro­ 1931b. Zur Morphologic und Okologie der r ha.r idces. Mern. Inst. Nat. Sci. Arts, 'Paris Blute von Straiiotes aloid.es L. Planta 14: 1R11: 1-88. 766-776. EOHRB.\CH, P. 1871. Beitrage sur Kenntnis DOUGL\s, G. E. 1944. The inferior ovarv. L einiger Hydrocharideen. Abh. naturforsch. Bot. Rev. 10: 125-186. Ges. Halle 12: 53-114. - 1957. The inferior ovarv. II. Bot. Rev. SALISBURY, E. J. 1926. Floral construction in 23: 1-41. ' the Helobiales. Ann. Bot. 40: 419- EAMES, A. J. 1961. Morphology of the Angio­ 445. sperms. New York. SAUNDERS, E. 1929. On carpel polymorphism. EBER, E. 1934. Karpellbau n n d Plazunta­ IIT. Ann. Bot. 43: 459-481. t.ionsverha.ltnisse in der Reihe der Helobiae. SOLEHEDER, H. 1913. Systernatisch-ana- Flora, leIla 127: 273-330. tornische Uritersuchung des Blattes 1968 1 T

VASCULARIZATION OF CYCAD LEAFLETS1

C. K. BRASHIER Department of Biology, General Beadle State College, Madison, South Dacota, U.S.A.

Abstract

A detailed investigation of leaflets of cycads, using eight represen­ tative species of eight genera, was made to study venation patterns, morphological and anatomical characteristics of the veins and as­ sociated tissues, and to point out similarities and differences found in this group. Vein patterns vary within this group from a completely closed svstem with all veins anastomosing toward the apex as shown in Encephalartos lehmanii to a completely open system with all veins ending blindly as found in Zamia [ntmila. Others have a mixed sys­ tem with some veins ending blindly and some anastomosing at the apex. Only two species studied have a midrib - (was reuoluta and Stangeria paradoxa. In every species the blade thickness at the vein is greater than the blade thickness between veins. In only one species. Zamia pumila, does the blade thickness at the vein exceed the total of the blade thickness between the vein and the vein thickness. Seven species have an endarch xylem located at the adaxial side of the bundle. One species has a mesarch xylem with the major part of the metaxylem differentiating centrifugally. The phloem is located on the abaxial side of the bundle with the metaphloem adjacent to the xylem and the crushed protophloem at the periphery of the bundle. The bundles, though primitive in vein patterns and type of veins, have an advanced anatomy.

Very little morphological or anatomical brief descriptions of the leaflet anatomy of investigation has been done on cycad each genus from observations of free-hand leaflet venation. Lamb (1923) determines and permanent cross-section preparations. genera and species by gross morphological Gaussen (1944) provides a general characters of the leaflets. She also gives description of the anatomy of cycad

1. Received for publication:l\larch 5, 1966.