Botanical Journal of the Linnean Society, 72: 115‑148. With 8
plates and 3 figures
Reproduced here with the
permission of the author
The floral anatomy of Victoria Schomb.
E. L. SCHNEIDER
Planchon (1850‑52) and Henfrey (1852) were among the first to recognize that in Victoria the flowers arise in a successive, helical arrangement, alternating with a homodromous spiral of leaves. Of further interest is the observation that each flower primordia occupies a precise position (the anodic side) with respect to the axil of the older leaf. These observations have been the subject of repeated controversy and speculation as to whether the flowers should be interpreted as extra‑axillary organs or as non‑median axillary organs (see Cutter (1961), Chassat (1962) and Weidlich (1974) for additional aspects of this matter).
The peduncles, which in Victoria arise from vertical rhizomes, can be readily identified from leaf bases (petioles) by their lack of associated adventitious roots (Plate 1A). The length of the peduncle varies in relation to the depth of the water in which it grows. The range of lengths of the mature peduncles of V. cruziana var. trickeri observed at Lotusland was 1‑1.25 m. A prominent feature, not only of the peduncles, but also of the petioles, ‑ leaves and flowers, is the presence of large persistent spines (Plate 1B). In V. amazonica the spines taper gradually from small cylindrical bases which are soft and fleshy. In V. cruziana, however, not only are the spines generally shorter, but they are usually fleshy and laterally compressed, contracting rapidly to small sharp points. In all specimens studied each of the largest spines was frequently associated with a single vascular supply.
Terminal on the submerged peduncles are the erect, showy, fragrant flowers (Plates 1C and 2A), which attain diameters averaging about 25 cm when fully expanded. Although the flowers of V. amazonica are generally larger, and of a slightly different colour at flowering, no essential morphological differences are apparent among the species. All flowers studied were actinomorphic, perfect and epigynous, and each consisted of a very large number of floral parts. Although they appear externally to be in whorls, close observation and dissection reveals that the floral parts are attached in a greatly suppressed helical arrangement. As will be discussed later, this condition probably reflects a shift and condensation from a more primitive spiral ranalian phyllotaxy.
The calyx consists of four slightly keeled petaloid sepals, each being approximately 12 cm long and 7‑8 cm wide. In V. amazonica these sepals are spiny to near the tip, whereas in V. cruziana the spines are generally restricted to the bases of the sepals (cf. Plates 1C and 2A).
The petals, which are thinner and more delicate in texture than the other floral parts, range from 50 to 70 in number and are obtuse to oblong‑ovate in shape.
Although there is a gradual transition from the outermost floral parts to the innermost, there is an abrupt change from the inner petals to the outer staminodia (Plates 1C and 2B). In this region there are no intermediate forms.
dorsiventrally flattened stamens are numerous (150‑200). The stamens are
petal‑shaped to subulate with paired pollen sacs, slightly to moderately
imbedded below the adaxial surfaces. The stamens (Moseley, 1958) are not
differentiated into filament and anther as in typical angiosperms, although
this condition is approached by the inner stamens. While the outer stamens
grade over centrifugally into about 20 subulate staminodia, the inner stamens
grade over centripetally into approximately 25 inner staminodia (paracarpels of
Caspary (1855) or 'guard cones' of Knoch (1899)).
The stamens and staminodia, as viewed longitudinally, are arched in an S‑shaped fashion. This architecture of the flower (Plates 1C and 2B) will be discussed later in relation to its pollination mechanism.
The gynoeciurn is composed of 25-40 coherent, syncarpous carpels, the number being slightly variable for any given species. The carpels are radially arranged in a single whorl around the base of the floral apex, leaving the latter free as an upper prolonged portion (Plate 2B, Fig. 1). A continuous cup‑like sheath of tissue, usually interpreted as being receptacular (the nature of which will be discussed later), encloses the carpels peripherally. This sheath of tissue is fused to the dorsal regions of the carpels. The ventral region of each diverges radially in a gradual slope. This sloped region forms a cup‑like area, 7‑10 cm in diameter, which becomes stigmatic. This stigmatic area is papillose and essentially continuous, but the divisions between the carpels are marked by grooves which represent the opposing outer ventral surfaces of the individual carpels. The carpels are prolonged distally into separate stylar processes (Plate 2B, Fig. 1). Each stylar process, which represents a food body or possibly a nectary, is adnate at maturity to the tissue which sheaths the dorsal carpellary (ovary) wall. At that time, however, extensive aerenchyma develops within the sheathing tissue and gives the stylar processes the appearance of being free, not adnate.
The ovary is plurilocular, the number of locules corresponding to the number of carpels. Placentation is laminar, with ovules arising over most of the septa but not over the ventral suture. The ovules (Khanna, 1967) are anatropous, bitegmic and crassinucellate with short and massive funiculi. Each ovule is supplied by a single vascular bundle which extends up the funiculus and terminates in the chalaza. Each ovule in addition, has a funicular aril.
The fruit of Victoria is, technically, a spiny berry (Plate 2C). As the fruit develops, all the floral organs decay away, leaving only the basal cup and floral‑organ scars. The outer ovary wall remains firm during fruit development, but the inner tissues become soft, with their cells separating from one another. Dehiscence is irregular, with the fruit simply opening by the expansion (growth) of the funicular arils surrounding the seeds and the swelling of the mucilage contained inside each aril.
Anatomy of the peduncle and the receptacle
The structural anatomy, of the peduncle in Victoria, although characteristic for this genus, is reminiscent of the peduncle organization described in other genera of the Nymphaeaceae sensu lato (e.g. Nymphaea (Conard, 1905; Moseley, 1961), Nuphar (Moseley, 1965) and Nelumbo (Wigand & Dennert, 1888; Esau, 1975; Esau & Kosakai, 1975a,b)).
The length of the peduncle can be attributed to two developmental processes. The first, and temporary, process can be seen during very early development. At the base of the young receptacle, cells are formed by horizontal divisions. Cells are then added to the peduncle basipetally, forming vertical columns of cells. Later, during floral organ initiation, an intercalary meristem differentiates at the base of the peduncle. The horizontal divisions of this meristem add to the existing vertical columns of ground cells, vascular tissues and air canals. This intercalary meristem is responsible for most of the length attained by the peduncle. As was noted in the earlier literature (e.g. Conard, 1905), intercalary meristems also function in maintaining the positions of leaves and flowers on the surface of the water. It is probable that an increase of water level increases tension upon the meristem and stimulates production of additional cells.
When divisions of cells cease, expansion in the diameter and length of the petiole and peduncle occurs. This expansion is brought about by both latitudinal and longitudinal cellular enlargement.
At maturity, the peduncles examined had each attained a diameter of approximately 2 cm. Although essentially cylindrical, they tend to be dorsiventrally flattened at the base.
One of the most striking structural characteristics in the peduncle of Victoria (and other members of the Nymphaeaceae sensu lato) is the presence of large, symmetrically arranged air canals. These air canals, which have their origins from both the temporary, proximal receptacular meristem and the basal intercalary meristem, are continuous through a peduncle. Diaphragms were not evident in longitudinal views of the peduncle canals but were plentiful in the canals of the roots.
Near the meristems, the air canals can be seen to be schizogenous in origin. Initially, separation of cells along the middle lamellae occurs, forming intercellular spaces. The expansion of these spaces involves division of cells perpendicular to the circumference of the space and their enlargement circumferentially, as demonstrated by the regular arrangement of anticlinal cell walls around the periphery of the canals. In the species studied, four large, centrally arranged canals were evident. Encircling these four canals were usually 16 regularly arranged canals, eight on the same radii as those of the large canals and eight alternating with them. Arms of asterosclereids were observed within these air canals.
The ground tissue, which forms the matrix among the
air canals and surrounds the vascular bundles, consists of compact, moderately
thickened (in comparison to the rhizome) parenchyma. During development, the
cells separate to some degree in the comers, resulting in numerous small
intercellular spaces. Enclosing the ground tissue is a poorly defined
epidermis, with numerous trichomes. The epidermal cells covering the emerging
spines are more tabloid than those of the peduncle proper, and their walls are
extremely thickened and impregnated with lignin‑like material. No stomata
were evident on the peduncle material studied.
Beneath the epidermis there is a single subepidermal layer with cells distinguishable by their larger size and somewhat columnar arrangement. Centripetal to this layer is a small‑celled zone of angular collenchyma which gives elasticity to the peduncle. The collenchyma zone is followed internally by the larger cells of the ground tissue.
Dispersed nearly symmetrically throughout the ground tissue are vascular bundles. Transverse freehand sections, stained in 0.5% Toluidine Blue 0, taken at both the distal and proximal ends of the peduncle, revealed that the vascular bundles run essentially parallel, with some rotation but little anastomosing, throughout the length of the peduncle. Although the origin and orientation of the vascular supply from the rhizome to the peduncle has not been studied here, a recent investigation on rhizome vascularization in the Nymphaeaceae (sensu stricto) has been made by Weidlich (1974).
The vascular bundles in the peduncle are wholly primary in origin and very numerous. As viewed in cross‑section, the bundles vary in size, composition and form. They occur, principally, in three positions: (1) centrally, along the septa separating the four major air canals, (2) peripherally, outside all the air canals, and (3) intermediately, between the large central air canals and the surrounding smaller air canals. Although the vascular bundles are collateral, three basic variations are distinguishable: (1) small bundles, each of which consists of a strand of phloem with or without protoxylem, (2) medium‑sized bundles, each of which is larger than the former and always associated with one or frequently two protoxylem lacuna, and (3) large strands equal to or usually larger than the previous ones, each consisting of two phloem areas, one flared outwardly, the other inwardly from the protoxylem elements. These large strands represent two (medium‑sized) apposed collateral bundles on the same radius, with the inner bundle inversely orientated.
During peduncle development, the protoxylem elements become stretched and protoxylem lacuna are formed. Isolated annular rings occur centripetally in the lacuna and helical wall‑thickenings occur centrifugally in normally orientated bundles. These positions are reversed where the bundles are inversely orientated.
Because Kosakai (1968) reported the probable presence of vessel elements with scalariform perforation plates in the primary xylem of the root, particular attention was paid to the nature of the tracheary elements in the peduncle. Although the xylem in Victoria is greatly reduced, not only in amount but in the extent of wall‑thickening, long elements with either annular or helical thickenings were easily discernible. In addition, reticulate elements (Bierhorst, 1960) were observed in some of the larger bundles. No perforated elements were observed.
The phloem, which is separated from the tracheary elements by at least one layer (more commonly three to four layers) of parenchyma cells, consists of sieve elements, companion cells and phloem parenchyma. The sieve elements in Victoria are moderately elongated with transverse or slightly inclined end walls, each of which has a simple sieve plate (type III of Zahur, 1959). The associated companion cells are recognizable as the smallest elements in the phloem. In addition, companion cells occur in a one‑to‑one ratio with the sieve elements. The parenchyma cells of the phloem exhibit no unusual features at the light microscope level of observation, although tannin was a common component of several of these cells.
Laticifers are common in the peduncle. The laticiferous cells are dispersed throughout the ground tissue and are also commonly associated with the vascular bundles. The occurrence of sclerified cells, astrosclereids in particular, is well known among members of the Nymphaeaceae (sensu stricto). They are distributed throughout the ground tissue and have arms extending into and across the air canals. Their function is thought to be one of support (Bukowiecki & Furmanowa, 1964). More recently, Schanderl (1973) has suggested that in Nymphaea and Nuphar the sclereids act as condensers of water vapour.
At the distal end of the peduncle is the receptacle. Striking anatomical changes occur within the lower receptacular region. Initially, the smaller peripheral bundles undergo radial to tangential divisions, the resulting bundles sloping typically centrifugally or infrequently centripetally. These bundles may divide again or, more frequently, fuse with similar bundles which then divide one or more times. These last bundles, which also slope centrifugally, supply the larger spines and ascend the periphery of the receptacle until they fuse with the vascular supply to the sepals.
The medium‑sized peripheral bundles typically follow the preceding pattern; but, sometimes, they slope centripetally, with or without a preceding division, to join the larger bundles of the peripheral system. Associated with these anastomosing bundles is an obvious change not only in the ground tissue but also in the xylem of the vascular bundles. The ground tissue at successively higher levels in the receptacle becomes aerenchymatous and has numerous asterosclereids (Plate 3A). Within the vascular bundles the xylem becomes extensive and the protoxylem lacunae fail to develop. Numerous elements with annular and helical thickenings can be found.
The small intermediate bundles of the peduncle slope centrifugally and fuse with the large bundles of the peripheral system and, frequently, with the medium‑sized bundles of the same area. At this level, two alternating concentric rings of bundles are found (Plate 3B), one in the intermediate system, the other in the central system. The bundles of the inner concentric ring either retain their identity or slope outward and fuse with those of the outer concentric ring. The small bundles of the central region then join the medium and large bundles, and the septa separating the four major air canals become aerenchymatous in such a manner that the canals become essentially continuous (Plate 3C). At this level there are no laticiferous cells. The major bundles of all the peripheral regions then anastomose and form a large entangled vascular ring around the common aerenchymatous centre (Plate 3C). This vascular ring will hereafter be termed the receptacular vascular plexus. The configuration of the vascular plexus in Victoria is slightly different from those described in Nuphar and Nymphaea. In Victoria, the plexus is more condensed into a definite ring which, in longitudinal view (Plate 2B, Fig. 1), appears circular. This writer agrees with Moseley's (1961) interpretation of the vascular plexus as probably signifying that a considerable condensation of the floral axis has occurred. The major bundles which form the vascular plexus lose their identity, but the major remaining bundles of the central system retain their identity and eventually contribute to the residual stelar tissue of the floral apex or the ventral carpellary supply (Fig. 1, Plate 3C).