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.
DISCUSSION – Continued
flower of Victoria
Onto genetically, the inferior
ovary of Victoria described herein
has been shown to be formed in the following manner. From the floral apex, the
sepals, petals, outermost staminodia and stamens are initiated in acropetal
order. Following the initiation of these appendages, there is a cessation of
meristematic activity of the floral apex and the concomitant transfer of
meristematic activity to a peripheral position in the form of an intercalary ring
meristem. Activity of this promeristem around the original floral apex results
in the formation of a cup‑shaped meristem from which the innermost
stamens and staminodia arise distally. Along the inner sides of this cup arise
radiating discontinuous meristematic ridges, herein shown to give rise to the
stylar processes, the distal ventral carpellary regions and the distal locular
regions. Once established, these distal locular regions are extended
basipetally by the activity of the circular or ring intercalary meristem. This
developmental sequence, together with additional ontogenetical aspects and
evidence from mature floral vascular anatomy, can be used to explain
satisfactorily the phylogeny and extant nature of the flower of Victoria.
Troll (1933) considered that all members of the Nymphaeaceae (sensu lato), except the Nymphaeoideae, possess apocarpous gynoecia. He considered that the gynoecia of the Nymphaeoideae (Nymphaeaceae sensu stricto*, Nymphaea, Victoria, Euryale, Barclaya, Nuphar) are distinguished by (1) the formation of the carpel primoridia below the free end of the growing point (floral axis) and (2) the marked radial dimensions of the carpels, which are laterally confluent with alternating radial strips of receptacular tissue. In this latter case, the gynoecia would be considered pseudo‑coenocarpous (Wilson & Just, 1939). In addition, Troll regarded Victoria and Euryale to be exceptional among the Nymphaeoideae in possessing epeltate carpels. Troll explained that peltation does not occur in these two genera, as it does in ‑the remaining genera, because of the repression or inhibition of the Querzone (i.e. cross‑zone = transverse, adaxial (ventral) meristem). It is ironic to this writer that Troll considered that these two genera, but not the others, lack a Querzone. Although in accord with Troll's interpretation of the carpels as epeltate in both Victoria and Euryale, he believes that previous studies on Nymphaea and Nuphar (Moseley, 1961, 1971, respectively), coupled with the present investigation and a concurrent investigation of Euryale, support the view that peltation does not occur in the Nymphaeoideae. Moseley (1961, 1965, 1971) has conclusively dismissed the idea that peltation occurs in the carpels of Nymphaea and Nuphar. The basic arguments expressed by Moseley can be utilized herein to show that, even though Troll (1933) was correct in considering the carpels of Victoria as epeltate, he 'read' this carpel form in the wrong phylogenetic direction. If one agrees with Troll's interpretation, that epeltate carpels are the result of repression or inhibition of a Querzone, this implies acceptance of a typological or Gestalt form (viz. the peltate carpel). Such an idea would seemingly deny the basic concept that any organ must be the descendant of a series of gradually evolving organs which were part of a previously existing sequence of organisms. In summarizing the evidence refuting the occurrence of peltation (or any potential to express peltation) within the genera of the Nymphaeoideae described, attention is called to the following evidence. The young carpels in Victoria, as in Nymphaea (Moseley, 1961), are essentially crescent‑ or horseshoe‑shaped up to the time of anthesis, and then post‑genital fusion occurs. This ‑condition is contrary to the peltate theory, in which the ventral carpellary regions are generally congenitally fused. The presence of the prominent ventral carpellary suture lined by two protodermal. (epidermal) layers is, in addition, an obstacle to the acceptance of peltation. Further evidence from vascular anatomy also weakens the peltate theory in that ovules receive their vascular supplies, either directly or indirectly (via the reticulum), from both ventral and dorsal carpellary veins. Furthermore, according to the peltate theory the ventral carpellary veins should be rotated by 180' in such a manner that all bundles (dorsal and ventral carpellary bundles) have their xylary regions face inward. In Victoria, as in Nymphaea and Nuphar, however, the ventral carpellary veins are only rotated by 90º. This implies that the mature utricular or ascidiform shape is attained, morphologically, by a simple folding (conduplicate) or inrolling (involution) and fusion, rather than by the processes envisaged in the peltate theory.
There is no doubt that the central core of tissue found in the gynoecium during development and at anthesis is receptacular. This theory is supported by evidence from both ontogeny and vascular anatomy. The original floral apex is meristematic in the very young flower and is responsible for sepal, petal and outer stamen initiation. Following this sequence of events, the meristem becomes quiescent and activity is shifted laterally to an intercalary meristem from which the remaining floral parts are initiated. In addition to this evidence, there is a central system of vascular bundles which typically extend from the receptacular vascular plexus into the projecting apex as normally orientated, collateral bundles. Although these bundles may anastomose with the ventral carpellary bundles to varying degrees, they remain distinct and leave little doubt as to the nature of the tissue which they supply.
Whether or not the carpels of Victoria are ensheathed by an outer cup of receptacular tissue, as suggested by Troll (1933), is less certain. There is, however, evidence which refutes Troll's contention that between adjacent carpels there are radial strips of receptacular tissue (= septal tissue). It has been shown that the vascular (gynoecial) strands in the outer wall of the gynoecium represent two normally orientated vascular bundles. These strands are double from their point of origin in the receptacular plexus to their termination in the stylar processes and innermost staminodia. The inner vascular bundles have been interpreted as the dorsal carpellary vascular bundles for reasons cited previously, namely that (1) the number of gynoecial strands, hence dorsal bundles, generally corresponds to the number of locules (carpels), (2) the septum common to adjacent locules typically receives vascular supplies from the inner as well as the outer bundles, and (3) the ventral carpellary veins are associated with the inner gynoecial bundles both at their point of origin and at their site of termination in the stylar processes. The outer appressed bundle in each gynoecial strand has been interpreted as a compound bundle which represents the fused, proximal parts of the vascular supplies to the appendicular organs (i.e. sepals, petals, staminodia and stamens). That the receptacle is involved to some degree in the formation of the outer ovary wall is unquestionable. That it is receptacular stelar tissue, such as the type revealed in certain members of the Santalaceae (Smith & Smith, 1942a,b), Rosaceae (Jackson, 1934) and Cactaceae (Boke, 1964) by the presence of a recurrent vascular bundle, however, is an unfounded idea. It has been shown that diffuse zonal growth occurs outside the procambial strands and thus involves receptacular cortical tissue rather than receptacular stelar tissue. The extent of appendicular tissue is difficult to determine, but this writer contends that the more distal parts of the outer ovary wall are better considered appendicular while the more proximal portion should be considered receptacular.
The nature of the septal regions, considered receptacular by Troll (1933), is clearly carpellary in origin. Developmentally, it has been shown that the carpel primordia have their origin from the circular intercalary meristem which surrounds the original floral apex. It has further been shown that this meristem is a continuous ring. Although the radiating ridges, which Troll considered to be the carpel primordia, appear to be free (apocarpous) basally, the carpels are congenitally fused. There is no indication of phylogenetic or postgenital fusion. Since the septal regions all originate from the intercalary meristem, as do the locular regions, they are best considered to be carpellary in nature. This hypothesis is supported by the occurrence of two systems of vascular bundles in each septum, both of which are close to an adjacent locule. Each bundle of each system is orientated at 90' from the normal orientation of the dorsal carpellary bundle and, hence, represents half of the ventral carpellary supply to any one carpel (locule).
The anomalous duplicate vascular supply to each petal, stamen, stylar process, septal region, etc., as earlier described, is admittedly disturbing; but Moseley (1961), upon finding a similar situation in Nymphaea, has offered a tentative interpretation which explains this phenomenon. His basic contention is that since the Nymphaeaceae have been in existence since at least the Lower Cretaceous (Arnold, 1947) and possibly the Jurassic (Simpson, 1937), the two vascular systems (i.e. the appendicular strand and the dorsal strands) have had a long association and as a result have become secondarily modified into a close functional unit. The selective pressure for such a modification is unknown, of course, but a physiological advantage to such a system should be considered. Additionally, an anomalous increase in vasculature is also found in the petals, staminodia and stamens, as described by Heinsbroek & Van Heel (1969). On the basis of the observations presented herein, this writer cannot agree with the tentative conclusions of Heinsbroek & Van Heel that these floral organs, based on the adaxial (and abaxial) peripheral systems, are structures of unknown homology. If one agrees, as does this writer, with Moseley's (1958) theory of the bidirectional evolution of these organs, the peripheral bundle system loses some of its morphological significance and is explicable in functional terms. This hypothesis is supported by the relationship between increased organ size and the concomitant increase in vasculature, not only of the peripheral systems but of the central system. Although the occurrence of such anomalous vasculature, in the flower of Victoria does not lend support to the basic assumptions concerning floral anatomy in general, or to the nature of gynoecial strands, petals, stamens and staminodia in particular, neither does it invalidate our current understanding. It is this writer's contention that at the present time the anomalous vasculature of Victoria (and Nymphaea) is better explained by neoclassical interpretations rather than Anthocormic ones (Meeuse, 1974), etc.
Based on the evidence gathered from both ontogeny and mature vascular anatomy, this writer offers the following hypothesis (modified from Moseley, 1961) for the evolution of the Nymphaeaceous (sensu stricto) flower.
Primitively, the floral organs were separate and helically‑ arranged on a conical receptacle, with the carpels in a more distal position (Fig. 3). From such a fundamentally ranunculaccous type of flower, the following changes could have occurred. Initially there was a tendency for extreme reduction or telescoping, not only of the floral axis‑evidence for this is provided by the receptacular vascular plexus‑but also of the inflorescence (see Moseley, 1971; Stebbins, 1970, 1973; Gottsberger, 1974) and vegetative axis. Such reduction would result in a semi'‑herbaceous or herbaceous form. At or prior to this time the carpels must have become conduplicately folded, as is indicated by the orientation of the ventral carpellary bundles in Nuphar, Nymphaea and Victoria. Initially, the carpels were perhaps styleless, unsealed and with extensive stigmatic crests; but soon the upper portion of each carpel became sterile and prolonged into the stylar process, which was developed to the greatest extent in Victoria and some species of Nymphaea. Concomitant with the formation of stylar processes, the stigmatic tissue, rather than becoming confined to the stylar tip, retained its position on the margin and ventral surfaces of each carpel. Subsequently, the orientation of the carpels was altered and the locular and placental regions expanded radially. Although this change in carpel orientation is more marked in Nuphar and Nymphaea than in Victoria, these three genera all have radially extended locular regions. The stamens, prior to this time, had undergone bidirectional evolution, toward more conventional types centripetally and toward sterilization centrifugally.
Coinciding with these several changes was the trend toward the production of perigynous (Nymphaea) and epigynous flowers (Victoria and Euryale) while hypogyny was retained in some members (e.g. Nuphar). Perigyny and epigyny probably resulted from the basipetal transference of meristematic activity (phylogenetically) from the original apex to an intercalary position early in the ontogeny of a flower. This meristem raised the sepals, petals and stamens on a cup either partially above (perigyny) or totally above (epigyny) the locular region. As these appendages were elevated, the apical meristem must have remained active and produced the carpels.
Complementary to the extreme telescoping of the conical floral axis was a shift of the helical phyllotaxy toward a whorled condition, although this condition has not been achieved, at least in the Nuphar‑Nymphaea‑Victoria complex. As a consequence of reduction, the floral appendages became closely arranged, and varying degrees of connation and adnation resulted among the respective parts. Although this writer is hesitant to support Moseley's (1961) interpretation that the presence of the residual stelar bundles (in Nymphaea and more so in Victoria) may be accounted for by a loss of some of the carpels (because of the inverse correlation between carpel number and amount of residual tissue between these two genera), an alternative suggestion is difficult to envisage. Perhaps the extensive size of the receptacular core is directly related to the amount of vasculature. In either case, the floral axis with its residual vascular tissue is interpreted, as a true floral axis rather than a pseudo‑axis (see Guedes (1973) for aspects of this matter). The appendicular organs became initially connate, at least basally, and then adnate to the surrounding organs. As a result, an outer sheath was formed which, together with the receptacle, became adnate to the carpels. As a result of this adnation, the dorsal carpellary vascular bundles became close to the appendicular bundles. Although these paired bundles have not fused, their position with respect to the carpels has shifted, usually to opposite the septal regions.
The concept described here must be considered only tentative. At present it represents a satisfactory explanation for the evolution of the nymphaeaceous (sensu stricto) flower. This writer must stress, however, that this conclusion is based only on evidence gathered on the Nuphar‑Nymphaea‑Victoria complex. Results from current work on Euryale and planned investigations concerning Barclaya and the newly described and most interesting Ondinea may call for revisions of this hypothesis.
Familial status of the Nymphaeaceae
The general dissatisfaction with the concept that the Nymphaeaceae sensu lato represent a natural family is well known. (For various classifications of these genera see Goleniewska‑Furmanowa (1970) and Simon (1971).)
writer prefers to defer support for any one classification until further data
have been assembled, the relationships between Victoria, Nuphar and Nymphaea
seem to be clear. From the evidence he has obtained, this writer is in
accord with the suggestion of Simon (197 1), based on serological data, that Victoria is closely related to Nymphaea and Nuphar, Close affinity between Nymphaea
and Victoria has, in addition,
been shown by Bukowiecki et al. (1972).
This writer, contrary to the views of Li (1955), finds support for the view
that Victoria is closely related to
these two genera and especially to Nymphaea.
This close relation to Nymphaea (and
Euryale) is supported by studies in
palynology (Ueno, 1962; Meier, 1964), karyology (Sokolovskaya & Melikyan, 1964) and morphology (Vinogradov, 1967;
As a final remark it may be worth adding that, despite the repeated suggestions in the literature that the Nymphaeaceae are derivatives of ancestors which may have given rise to the monocotyledons, this writer does not find evidence to support such suggestions. The recent study of Kosakai, Moseley & Cheadle (1970) supports that statement.
* The newly described genus Ondinea, den Hartog has also recently been placed within this taxon (den Hartog,
The writer wishes to express
appreciation to Professor Maynard F. Moseley, for his initiative in making this
investigation possible and his advice and helpful criticisms during the
progress of the research and preparation of the manuscript, and also to
Professors Cornelius H. Muller and Dale M. Smith for their continued advice and
He also wishes to express his gratitude to Madame Ganna Walska, owner of Lotusland, for her permission to visit her estate and make repeated collections of Victoria cruziana var. trickeri, and to the directors of the following institutions for seeds of Victoria: Jardin Botanique National de Belgique, Bruxelles; Berlin Botanic Gardens; Botanic Garden of the Friedrich‑Schiller‑Univ. Jena, Goethealle; Rotterdam Botanical Garden; Quinta da Boa Vista, Rio de Janeiro, Guanahara; Jardin Botanique de la Ville et de l'Universite, Besancon; Hortus Botanica Principalis Academiae Scientiarum URSS, Moscow; Hortus Botanicus Bogoriensis, Bogor, Java.
The research was aided by a Grant‑in‑Aid of research from The Society of the Sigma Xi and a Patent Fund Grant from the University of California, Santa Barbara.