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Structure and Development |
New York Botanical Garden, Bronx, New York 10458 USA
Received for publication February 28, 2003. Accepted for publication July 1, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: floral development • gynoecium • pseudomonomerous • Vochysiaceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Conti et al., 1996
; Savolainen et al., 2000
; Soltis et al., 2000
), a relationship supported by a suite of anatomical, embryological, and developmental characters (Conti et al., 1997
; Litt, 1999
).
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), therefore it will not be discussed here. The other seven genera are grouped into two tribes that differ in characters of the ovary and fruit (Dumortier, 1829
; Stafleu, 1952
)(Table 1). According to published descriptions, Vochysieae (Vochysia, Salvertia, Qualea, Callisthene, and Ruizterania, a segregate of Qualea) have a superior trilocular ovary that develops into a loculicidal capsule, whereas Erismeae (Erisma and Erismadelphus) have an inferior unilocular ovary that matures into an indehiscent winged fruit.
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), was discovered after this work was completed. It has clear affinities with Erismeae; however, little material is available and it was not included in this study.
Vochysiaceae flowers are unusual, but the placement of the family as sister-group to Myrtaceae raises even more questions about the morphology and evolution of these flowers. Whereas flowers of Myrtales are generally polysymmetric, with those of Myrtaceae often having numerous stamens, those of Vochysiaceae are decidedly monosymmetric (or even asymmetrical) and have a single, frequently large, fertile stamen. Thus, there is little obvious morphological common ground between the two families. However, the inclusion of Vochysiaceae in Myrtales casts the inferior ovary of Erismeae in a new light, as epigyny is characteristic of the order. This indicates that the superior ovary of Vochysieae may be secondarily derived. Relatively few examples of such independent derivations of a superior ovary are documented (e.g., Eyde and Tseng, 1969
; Igersheim et al., 1994
; Chase et al., 1995
; Gustafsson and Albert, 1999
; Kuzoff et al., 2001
; Soltis and Hufford, 2002
).
A review of the literature also raised an additional question about the gynoecium of Erismeae. Whereas the ovary of both genera, Erisma and Erismadelphus, has a single locule, Kopka and Weberling (1984)
reported additional aborted locules in transverse sections of floral buds of Erismadelphus but not of Erisma. Therefore, the unilocular ovaries of the two genera might not be equivalent and the character might not be a synapomorphy of the Erismeae. Their study was limited, however, and included neither observations of development nor extensive sampling. In light of this information on the relationships and the floral structure of Vochysiaceae, it was appropriate to examine floral development, anatomy, and morphology in this family.
In this paper, we report our observations of floral development and vascular anatomy in the Vochysiaceae gynoecium. In particular, we attempted to determine: (1) whether there is evidence that more than one carpel is involved in the development of the gynoecium in Erisma and Erismadelphus and (2) if there is anatomical or morphological evidence that the ovary of Vochysieae is not homologous with the superior ovaries of other nonmyrtalean taxa.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Furthermore, Salvertia and Ruizterania do not differ from Vochysia and Qualea, respectively, in features of the gynoecium. Thus, we assume that in these two genera, the development and the vasculature of the ovary do not differ significantly from what is observed in Vochysia and Qualea, respectively.
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Vochysieae
The flowers of the genera in this tribe (Vochysia, Salvertia, Qualea, Ruizterania, Callisthene) are described as perigynous (de Sainte-Hilaire, 1820
; Warming, 1875
; Baillon, 1878
; Stafleu, 1948
), the floral organs being inserted on a short hypanthium that surrounds the superior, trilocular ovary. In flowers of Vochysia (100+ species), the fourth sepal is approximately four times the length of the other sepals, and the corolla is almost always composed of three petals (Figs. 1, 2), although a very few species (none included in this study) have one or none. The fertile stamen is in the plane of symmetry, in front of the middle petal; two staminodes are nearly always present and are in front of the two lateral petals. The ovary contains two ovules in each of the three locules. Flowers of Salvertia (one species, not included in this study) differ in having sepals that are nearly equal in size and five petals.
The remaining three genera of Vochysieae (Qualea, Ruizterania, Callisthene) each have one petal, although some species of Qualea (50 species) also have two minute rudimentary petals (Fig. 2). The fertile stamen is not directly in front of the petal but is slightly offset towards the fifth sepal, and these flowers are asymmetrical (Figs. 2, 33). Two staminodes in antepetalous positions are present in some species of Qualea and Ruizterania. Each of the three locules of the ovary contains numerous ovules. Ruizterania (13 species, not included in this study) and Callisthene (eight species) differ from Qualea in features of anther ornamentation and of fruit dehiscence and seed shape, respectively (Stafleu, 1952
, 1953
; Marcano-Berti, 1969
; Martins, 1981
)(Table 1).
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; Kopka and Weberling, 1984
; Kawasaki, 1998
; Litt and Cheek, 2002
). Erisma (16 species) flowers have one petal, although they may have up to four rudimentary petals (Fig. 2). The fertile stamen is in front of the petal (in the plane of symmetry). Staminodes (most often two) are also common and are antepetalous as in the Vochysieae. The single locule of the gynoecium contains two ovules. Erismadelphus (two species) differs from Erisma in having five petals (Fig. 2) and only one ovule (Keay and Stafleu, 1953
). The spur in Erismadelphus is particularly broad and saclike, so that the ovary is free for perhaps a third of its circumference (Figs. 41, 42).
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Material for scanning electron microscopy was dissected in 95% ethanol, dehydrated in an ethanol/acetone series, critical-point dried, sputter coated with gold/palladium, and viewed at 5 kV with a JEOL 5410LV.
Material for serial sectioning was dehydrated in an ethanol/toluene series, embedded in paraffin, and sectioned with a rotary microtome at 10–15 µm. Buds that were particularly difficult to section were softened by exposing their tips in the paraffin block and soaking them for at least 1 wk in 2 : 5 glycerin : ethanol (70%) with acetic acid added to 10% of the total volume. Material that was particularly rich in tannins was treated with Stockwell's bleach (Schmid, 1977
) before staining. All material was stained with Johannson's safranin and counterstained with either chlorazol black E or fast green followed by orange G, or counterstained with astra blue only. All available species of Qualea, Callisthene, Erisma, and Erismadelphus were used. Species of Vochysia were chosen to represent as many of Stafleu's taxonomic sections and subsections as possible given the available material (Table 2).
The available material of Erismadelphus was not suitable for scanning electron microscopy (SEM); thus, for this genus, we obtained data from serial sections only. SEM data are also available only for a very few stages of floral development in Callisthene. Relatively complete series of developmental and anatomical data were obtained for multiple species of Qualea, Vochysia, and Erisma.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), but this latter usage leads to confusion and implies homology of these outer tissue layers to the free floral cup. Although this homology is commonly accepted among morphologists, it generally cannot be proven. Thus, we will restrict our use of the term to the floral cup of a perigynous flower.
Organogenesis
General aspects of floral development will be presented next, followed by descriptions of the development of the gynoecium.
Calyx
In all taxa, the five sepals are initiated in a 2/5 spiral, clockwise or counterclockwise (Figs. 3, 4). The floral apex becomes noticeably concave with the initiation of the sepals and remains so throughout the remainder of floral development, although it may be relatively flat in some Qualea species (Fig. 9). The sepals broaden rapidly. Aestivation is quincuncial, although this pattern may become difficult to observe as the extent of overlap of the sepals increases. In almost all Vochysiaceae, the fourth sepal is overgrown by the fifth and completely surrounds the inner organs. In Vochysia, Ruizterania, and some species of Callisthene, it is also significantly longer than the other four sepals, which are subequal in size.
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; Warming, 1875
; Stafleu, 1952
; Cronquist, 1981
), whereas Kopka and Weberling (1984)
interpreted it as an extension of the floral axis. Recent work has shown that the spur develops in a position that is ambiguous and cannot be unequivocally designated receptacle as opposed to calyx (R. Carmo-Oliveira, Universidade Federal do Uberlândia, personal communication). However in species of Qualea, the first and second sepals, which flank the fourth, are inserted below the level at which the spur emerges. In some species these sepals enclose the spur until anthesis. Furthermore, the spur abscises with the calyx (A. Litt, personal observation, and P. Oliveira, Universidade Federal do Uberlândia, personal communication). These lines of evidence support the hypothesis that the spur is part of the calyx and not the floral axis.
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).
The sepals of the two species of Callisthene bear structures at the base of their adaxial surfaces that are reminiscent of colleters (see also Martins, 1981
)(Fig. 6). In C. major they are small and roughly triangular, whereas in C. fasciculata they are elongate, in some cases reaching the tip of the sepal. These flattened structures, also possibly glandular, were irregular in number and shape and were also found between the petiole and the axis (Figs. 7, 8).
Corolla and androecium
Petals are initiated when the sepals (at least the first three) are already quite large and broadly overlapping (Figs. 9, 10). Stamens are initiated when the petal primordia are still relatively small. In most species, the petals and stamen/staminodes arise on the vertical flank of the floral cup, and in early stages, the organs, particularly in Vochysia and Erisma species, grow horizontally (Fig. 11) and perpendicular to the surface on which they insert. As the organs enlarge and the ovary begins to elongate, the petals and stamen/staminodes become more vertically oriented (Fig. 12). Vochysiaceae anthers are characterized in general by a relatively massive connective, and the style lies between the two thecae. In Vochysia, the connective also forms a conspicuous, large-celled cap over the stigma (Fig. 13).
The position of the thecae on either side of the style is important in the secondary pollination presentation of Vochysia (Yeo, 1993
; Oliveira, 1998
). In all species observed so far, the anthers shed their pollen onto the style before anthesis. As the bud opens, the stamen abscises or is broken off at the base and falls out of the flower, leaving the exserted style (but not the stigma) covered with pollen.
It is common in the development of Vochysiaceae flowers for packing and twisting to occur within the developing buds. It is not unusual for the style and/or the filament to be curved, for the anther to become bent at an angle relative to the filament, or for the single petal of Erisma and Qualea species to be highly crumpled in bud. The limbs of staminodes and the lateral or rudimentary petals are generally displaced, presumably to maximize space-packing efficiency (Fig. 12). In open flowers of many species the style and filament are strongly twisted, variably in some species (e.g., Ruizterania cassiquiarensis) and predictably in others (e.g., Qualea grandiflora).
Gynoecium
In all taxa, the gynoecium is first visible, after all other floral organs have been initiated, as a ring primordium on the floral apex (Figs. 14, 17). Early development is similar in all species, and differences among the taxa do not become apparent until near maturity when the difference in ovary position between Erismeae and Vochysieae becomes apparent.
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Erisma (Figs. 17, 18)
A ring primordium is formed as well, but the opening in the center is oval or round (Fig. 17). As development proceeds, it narrows to a longitudinal slit (Fig. 18). In other features, the development of the inferior ovary of Erisma is indistinguishable from that of the ovary of Vochysia, Qualea, and Callisthene.
Vasculature
The following descriptions are based on serial sections, presented here in acropetal sequence. General observations of floral vasculature and anatomy will be presented, followed by descriptions of the vasculature of the gynoecium.
In all species of Vochysiaceae the floral vasculature, which has the internal phloem characteristic of the vasculature of the vegetative structures of this family, is derived from a cylinder of vascular tissue in the pedicel. Medullary bundles were observed in Vochysia, Erisma, and Erismadelphus (Fig. 19); these appear to anastomose with the vascular cylinder or in some cases contribute to the vasculature of the gynoecium. In the base of the flower, the vascular cylinder separates entirely into or splits off discrete bundles that supply the floral organs (Figs. 20, 21, 28, 34). These bundles extend through the hypanthium (in Vochysieae) or the outer layer of the ovary/floral cup (in Erismeae) to enter the sepals. In Qualea, Callisthene, and Erisma, all of which have one petal, one bundle branches to supply the petal and the fertile stamen (Figs. 30–32, 37, 38). Rudimentary petals and staminodes, when present in these species, were not observed to contain vascular tissue. In Vochysia and Erismadelphus, with two staminodes and three and five petals respectively, three or five of the "floral cup" bundles branch to supply the petals and stamen/staminodes (Figs. 23, 24, 42, 43).
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Vochysieae gynoecium
In all species of Vochysieae the vascular cylinder of the pedicel produces branches that enter the hypanthium (or the sepals directly), and the remainder of the cylinder supplies the gynoecium (Figs. 20–22, 28, 29). In most cases the vascular tissue that enters the gynoecium forms three dorsal carpel bundles and three major synlateral carpel bundles. These latter are located at the outer edge of each of the three septa and may be as large as or larger than the dorsal bundles (Figs. 22, 23, 29, 30). Arcs of numerous small bundles between the dorsal bundles form an anastomosing network that supplies the ovary wall (Fig. 31). In most species the major synlateral bundles divide, each producing a bundle that travels through the septum to lie at its inner margin. These ventral carpel bundles (Figs. 22, 29) supply the ovules of the two adjacent carpels.
1. Vochysia (Figs. 19–25)—No significant variability was observed in the species of Vochysia. In transverse section, the ovary is three-lobed; a furrow marks the center of each locule, where the fruit will dehisce (Fig. 24). The ovary is adherent to the floral cup at its base: the locules extend below the level at which the ovary becomes completely free from the surrounding tissue (Figs. 21, 22). Thus, the vasculature to the gynoecium becomes organized at the same level at which branches are being supplied to the floral cup. In Vochysia, the bundles at the inner edge of each septum come together to form a ring in the center of the gynoecium (Fig. 23), which then separates into three bundles that lie one in front of each locule. These bundles supply the two ovules of each locule (Fig. 24). The three synlateral bundles and the three smaller dorsal bundles continue into the style (Fig. 25).
2. Qualea and Callisthene (Figs. 26–33)—In transverse section, the ovaries of these genera are more or less circular and unlobed (Figs. 30, 31, 33). There is no evidence that the locules extend below the level at which the ovary becomes free from the surrounding floral cup, as in Vochysia. In both Qualea and Callisthene, the base of the flower and ovary are mildly to strongly slanted, with the side opposite the spur being higher (Fig. 26). The ovary becomes free on the spur side at a lower level, and thus the vasculature to the ovary also becomes separate from that of the floral cup at a lower level on that side (Figs. 26, 27). Furthermore, the slant of the ovary means that in most species the vascular cylinder cannot continue straight into the ovary but must curve towards the horizontal as the ovary emerges at an angle from the base of the flower (Fig. 26). Thus sections through the ovary often contain vascular tissue that appears to be branching horizontally but in fact is bending to enter the ovary (Fig. 27). The species described next differ in details such as the number of bundles in the style and the configuration of the ventral carpel bundles.
a. Q. parviflora, Q. dichotoma (Figs. 28–30)—There are no significant deviations from the pattern described for Vochysieae. In the ovary wall of Q. parviflora, the dorsal carpel bundles are relatively inconspicuous as opposed to the larger synlateral carpel bundles (Fig. 30).
b. Q. lineata, Q. rosea, Q. mori-boomii (Fig. 31)—The origin of the ventral bundles is slightly different in these species in that numerous lateral bundles contribute to them. There is no conspicuously larger synlateral bundle at the outer edge of each septum, as in Vochysia or other Qualea species (Fig. 31). The style of Q. lineata contains a ring of discrete bundles. The three dorsal bundles are conspicuously the largest, with numerous small bundles between. In the style of Q. rosea, which is significantly twisted in the bud, there is a continuous six-pointed ring of vascular tissue. The style of Q. mori-boomii contains only three bundles, the dorsal carpel bundles.
c. C. major—The available material of C. major was not adequate to determine the details of the vascular supply to the gynoecium, however the structure of the flower and the pattern of vasculature in this species is similar to that seen in Qualea.
d. C. fasciculata (Figs. 32–33)—The ovary of this species is more elongate and slender than that of other species of Vochysieae that were examined in this study. Although the base of the ovary is slanted, the vascular tissue does not have to curve appreciably to enter the ovary as it does in Qualea species. After the dorsal and synlateral carpel bundles branch off from the vascular tissue in the base of the gynoecium, a triangular mass of vascular tissue remains in the center. This coalesces into a ring, which appears to supply the numerous ovules of each of the three carpels (Figs. 32, 33). The synlateral bundles and the dorsal bundles extend into the style.
Erismeae gynoecium
In these epigynous flowers the vascular cylinder separates into discrete bundles, which extend the length of the ovary and supply the three outer whorls of floral organs. These bundles also produce numerous small branches that form an anastomosing network surrounding the single locule of the ovary (Figs. 37, 41). There is no clearly identifiable dorsal carpel bundle, although in some cases a bundle can be interpreted as such.
1. Erisma (Figs. 34–40)—Four species of this genus had no evidence of aborted carpels. The shape and orientation of the single locule and details of the vasculature varied among the species examined.
a. E. bracteosum, E. floribundum (Figs. 34–39)—In these species, the spur is inserted at the top of the ovary (Figs. 36–38). The locule is oriented somewhat diagonally in the bud, although it may be more symmetrically oriented in E. floribundum. The placenta is more or less in front of the position of the fifth sepal or between the second and fifth in E. floribundum. This position is either clockwise or counterclockwise from the spur (used as a point of reference) depending on the direction of sepal initiation.
The vascular bundles on the adaxial side of the floral bud produce small branches that anastomose in the center with some of the medullary bundles. An arc of bundles is thus formed, which coalesces into one bundle that supplies the two ovules (Figs. 34–36). The bundles that form the network surrounding the locule anastomose into a ring of several bundles that enter the style and further anastomose to form three (sometimes four or five) bundles that surround the stylar canal (Figs. 38, 39). In E. floribundum, the bundles are conspicuously off-center, and this is also variably the case in E. bracteosum (Fig. 39).
b. E. uncinatum and E. japura (Fig. 40)—In these species the spur is inserted at the base of the ovary, thus the ovary is free on that side of the flower (Fig. 40). The locule is symmetrical, lying on the midline of the bud with the placenta in front of the petal (between the third and fifth sepals)(Fig. 40). In E. japura, the bundle that supplies the two ovules is formed from an arc of bundles in the same way as in E. bracteosum and E. floribundum. In E. uncinatum, one vascular bundle branches from the bundle that will eventually become the median bundle of the fifth sepal; this bundle supplies the two ovules. The small bundles surrounding the locule anastomose to form several bundles that enter the style, but the exact number of bundles in the style could not be determined accurately. One bundle is larger than the others, which form an arc surrounding the transmitting tissue.
2. Erismadelphus (Figs. 41–44)—One species, Erismadelphus exsul, was available for this study. Examination of serial sections revealed one aborted locule in two of the four specimens available (Figs. 41, 42). The fertile locule is irregularly shaped, although it should be noted that these observations were made on rehydrated herbarium material. In contrast to Erisma, in which the placenta is in front of the position of the fifth sepal or thereabouts, the placenta in Erismadelphus exsul is between the positions of sepals one and three (Figs. 42, 44). As with Erisma, this position may be either clockwise or counterclockwise from the spur.
As the vascular cylinder separates into discrete bundles, one bundle remains separate and supplies the ovule (Figs. 41, 42). No bundles occupy the position of a ventral carpel bundle of the aborted carpel.
There is no bundle associated with the fertile locule that can be identified as a dorsal carpel bundle. There is a bundle that can be followed into the style in the position where one might look for the dorsal bundle of the aborted carpel. However, the curve of the style makes tracing this bundle difficult (Figs. 42, 43). This appears to be the only vascular bundle in the style, although in some specimens this could not be determined.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Ontogeny of the flowers of Vochysiaceae is basically similar, despite their morphological differences at maturity. The manner in which the organs of all whorls are initiated and the broad outlines of their development are fundamentally similar, whether the ovary is superior or inferior, trilocular or unilocular, or the corolla includes three petals or one. Vasculature is also similar among the genera. The biggest difference is in the epigynous Erismeae, which have no discrete dorsal or other regularly organized carpel-wall bundles as in Vochysieae. Instead, a network of anastomosing bundles surrounds the locule and forms the bundle(s) that will enter the style (Figs. 37, 38, 41, 42)(as in Hufford, 1989
). At first glance, the vasculature of Qualea and of Callisthene major appear to differ substantially from that of C. fasciculata and Vochysia. The observed differences, however, reflect the slant of the ovary in the former species as well as the more slender shape of the ovary of C. fasciculata. If the tilt is taken into account, it can be seen that in all species of Vochysieae the vascular cylinder of the pedicel enters the gynoecium more or less directly, after splitting off branches that will supply the other floral organs.
In a few cases, the observed patterns follow established subgeneric taxonomic groupings, although a phylogenetic analysis testing the monophyly of these groups is not yet complete. Qualea rosea, Q. lineata, and Q. mori-boomii all have similar patterns of gynoecial vasculature, differing only in the number of bundles in the style. Qualea mori-boomii is a segregate of Q. coerulea (Marcano-Berti, 1989
), and Q. coerulea was included with Q. lineata and Q. rosea by Stafleu (1953)
in his series Calophylloideae (section Qualea, subgenus Qualea)(Table 2). Based on his taxonomy, Q. mori-boomii would also be placed here. However, Stafleu (1953)
placed fully 27 of his 59 species in this series (27 of 46 when the segregate genus Ruizterania is excluded). Furthermore, the buds and flowers of these three species are larger—considerably larger in the cases of Q. rosea and Q. lineata—than those of Q. parviflora and Q. dichotoma. This size difference may produce differences in vasculature. Thus, the observed similarities in vasculature may reflect an evolutionary relationship or may reflect independently derived similarities in floral development and structure.
Stafleu (1954)
recognized two sections in Erisma, each including half the species. Erisma japura and E. uncinatum both belong to section Rixa, and E. floribundum and E. bracteosum to section Erisma. The similarities and differences seen in locule and placenta orientation in these species thus conform to Stafleu's notions of relations within the genus. However, a cladistic analysis of the 16 species, based on 21 morphological features, did not show these sections to be monophyletic and placed E. uncinatum and E. japura in different clades (Kawasaki, 1992
). Erisma bracteosum and E. floribundum are placed in the same clade. Additional work on gynoecium structure in Erisma is needed to determine the pattern of character evolution within the genus and tribe Erismeae.
The data collected also highlight the similarities between Qualea and Callisthene and accentuate the differences between these two genera and Vochysia, with which they have been allied in tribe Vochysieae. All three have a trilocular ovary, but it is partly inferior in Vochysia and completely superior in the other two (Figs. 21, 22). Vochysia also does not have the strongly slanted receptacle seen in Qualea and Callisthene (Fig. 45). In fact, it is not entirely clear that there is a hypanthium in Qualea and Callisthene. If one changes the frame of reference and views the base of the ovary as horizontal, the putative hypanthium becomes a broad receptacle (Figs. 45–47).
Symmetry in Vochysiaceae
In all species, sepals are initiated in a spiral sequence, either clockwise or counterclockwise (Figs. 3, 4). Subsequent organs are initiated with reference to the sepals, thus the single petal of Qualea, Erisma, and Callisthene is always between the third and fifth sepals (Fig. 2) and opposite the spur, as is the center petal of Vochysia. The stamen in Vochysia and Erisma (and Salvertia and Erismadelphus) is located in front of this petal, in the plane of symmetry. In Qualea and Callisthene (and Ruizterania), the stamen is displaced towards the fifth sepal; thus, these flowers are asymmetrical (Fig. 2). Because the sepals are arranged in left-handed and right-handed spirals, the fifth sepal is either to the left or the right of the petal, and thus the stamen is also either to the left or the right of the petal. There has been speculation that these left-handed and right-handed morphologies may be significant for pollination, but both are found on the same plant and therefore can provide no special opportunity for cross-pollination. However if there were not right- and left-handed flowers there would in fact be no effective transfer of pollen from stamen to stigma.
Flowers of Erisma and Erismadelphus are superficially bilaterally symmetrical, with the stamen in the median plane, but in two of four species of Erisma, and in Erismadelphus, the single locule of the ovary is not symmetrically oriented (Figs. 36, 42). In Erismadelphus, Erisma bracteosum, and Erisma floribundum, the placenta may be positioned to the left or the right of the spur, as with the stamen of Qualea. This again presumably reflects the spiral initiation of the sepals. Any structure that is off the plane of symmetry will be found clockwise from the spur in some flowers and counterclockwise in others.
Gynoecium of Erismeae
Locule number
The functionally unilocular ovaries of the two genera of Erismeae differ structurally. Erismadelphus has at least one aborted carpel in the gynoecium (Figs. 41, 42), and the vasculature of the style is derived from a bundle that is associated with the aborted carpel rather than with the fertile carpel (Fig. 42). Two aborted carpels were reported by Kopka and Weberling (1984)
. In the limited material available for this study, one aborted carpel was seen, but inconsistently. In contrast, aborted carpels were never seen in Erisma, and there is no evidence from vasculature to indicate that any might exist. Developmental data are not available for Erismadelphus, but development of the ovary of Erisma is consistent with the notion that the gynoecium consists of a single carpel. In all Vochysiaceae, the gynoecium is initiated as a ring primordium; in Vochysieae, the depression in the center of the ring, and subsequently the opening at the apex of the developing ovary, is triangular or three-parted. This is not the case in Erisma, in which the depression is oval and the opening is longitudinal. The presence of aborted carpels in Erismadelphus flowers makes this an important genus from which to obtain developmental data.
The only suggestion in Erisma of a multi-carpellate condition is the asymmetrical position of the locule and the placenta in E. bracteosum and E. floribundum. This position is similar to what one might expect if the carpel were one of several in the gynoecium. Nonetheless, it does not of itself provide direct evidence of other carpels. Phylogenetic analyses have not yet resolved relationships within Erismeae, but it is difficult to refrain from speculating that the different morphologies within the family represent stages in a reduction series. The starting point would be a tricarpellate gynoecium such as that of Vochysieae, with Erismadelphus (aborted carpels) and species such as E. bracteosum and E. floribundum representing intermediate stages. Erisma uncinatum and E. japura, with a single, symmetrical locule, would represent the final stage.
Pseudomonomery
Ronse De Craene and Smets (1998)
noted that in 95% of unicarpellate taxa, the carpel is oriented toward the inflorescence axis. Away from the axis is uncommon, and taxa in which the position is variable are rare. Clarke (1859)
, in a comment on the Vochysiaceae, stated that "one of the most remarkable characters in this family is that the carpel when single is posterior." However, this description was based only on Erisma, as Erismadelphus had not yet been described (Mildbraed, 1913
). Clarke was following common usage in applying the term "posterior" to the spur-side of the flower in Vochysiaceae, although it is the second, not the spurred fourth sepal, that is in front of the axis (Fig. 2). Based on this usage, Clarke's description is correct for E. uncinatum and E. japura because in these species the locule is oriented away from the spur (Fig. 40). However, in E. floribundum and E. bracteosum, the locule is oriented obliquely, more towards the axis (Fig. 36). Thus, Erisma in fact is one of the rare taxa in which there is variability in the position of the locule.
Eckardt (1937)
used Clarke's description, along with the fact that other Vochysiaceae were trilocular, to conclude that the gynoecium of Erisma is pseudomonomerous. Eckardt used this term to describe a unicarpellate gynoecium that is derived by reduction from a syncarpous one, in contrast to a "true" unicarpellate gynoecium derived by reduction from an apocarpous one. Pseudomonomery sensu Eckardt (also Eames, 1961
; Hufford, 1989
) therefore refers to an evolutionary derivation, not a morphological condition, although Eckardt does present morphological evidence of the derivation for the taxa that he observed. Ronse de Craene and Smets (1998)
defined pseudomonomery in morphological terms, using it to refer to an ovary in which several carpels are initiated but all abort except one. However, their actual application of the term was variable because they incorporated information from the literature, in which usage is inconsistent.
Authors since Eckardt (1937)
have followed his lead in describing the ovary of Erismeae, including Erismadelphus, as pseudomonomerous (e.g., Cronquist, 1981
; Takhtajan, 1997
). However, there are two problems with using the term in this historical sense. First, it is applied to gynoecia that differ in structure. There may be physical evidence of reduction in carpel number (as in Erismadelphus), or there may be no such evidence (as in Erisma). When the same term is used to describe both, information is lost, and a reader might conclude that the ovaries are the same. Second, it is inappropriate to use assumed evolutionary derivation in describing characters. To avoid circularity, the pattern of character state changes is best deduced from the results of a phylogenetic analysis, rather than assumed a priori.
We recommend restricting the use of the term "pseudomonomery" to the morphological condition described by Ronse De Craene and Smets (1998)
and Weberling (1981)
, in which there is only one fertile locule in the mature ovary, but in which there is direct evidence that more than one carpel is initiated. This requires examining the ontogeny and morphology of the ovary (Weberling, 1981
; Ronse De Craene and Smets, 1998
). Using this criterion, the gynoecium of Erismadelphus is pseudomonomerous, whereas that of Erisma is not. We suggest describing the gynoecium of Erisma as monomerous rather than unicarpellate. Monomerous refers to a gynoecium composed of a single unit, without indicating the specific nature of the unit. In Erisma the ovary is never distinct from the surrounding floral tissue and no discrete carpel can be identified, only a single locule. To date there is no evidence for more than one structure in the ovary, thus monomerous is an accurate description of what can be observed. Because eight species of Erisma were not examined in this study, future work may demonstrate evidence in some species of more than one carpel.
Ovary position in Vochysieae
Mature morphology
Serial sections of Vochysia buds show that in this genus the base of the gynoecium is not free from the surrounding floral periphery, that is, the ovary is not wholly superior. The locules of the three carpels can be seen in sections in which the ovary is still continuous with the surrounding floral tissue (Figs. 21, 22), thus mature flowers of Vochysia are epigynous to a small degree.
In contrast, the ovary of Qualea and Callisthene does not appear to be inferior to any degree. In sections of flowers of these genera, the locules are not apparent until the ovary is completely free, and there is no clear-cut morphological evidence to distinguish the superior position of the ovary of Qualea and Callisthene from that of other taxa. However, the slanted base of these flowers and of the ovary as well as the presence of the spur on one side make it difficult to determine the exact position of the base of the ovary (Fig. 45). Likewise, it is difficult to identify what should be considered hypanthium as opposed to receptacle, if in fact there is any difference between them. Thus it is possible to interpret the ovary as being slightly adherent on one side to the receptacle.
Our results indicate that there are three distinct floral plans within Vochysiaceae: Erisma and Erismadelphus clearly are epigynous; Vochysia is partly epigynous and partly perigynous (the ovary is adherent at its base, but free from the hypanthium above); Qualea, Callisthene, and Ruizterania are perigynous. There are qualifications to these basic descriptions: the ovary in flowers of Erismadelphus, E. uncinatum and E. japura, is free on the spurred side of the flower, and Qualea, Callisthene, and Ruizterania flowers can perhaps be considered hypogynous if they are tilted (Fig. 46).
Ontogeny: floral apex shape and ovary position
In spite of these differences in the structure of the mature flowers, the early stages of development of the gynoecium are the same in all species of Vochysiaceae and conform to a pattern generally but not exclusively associated with an inferior ovary (Boke, 1963
, 1964
; Kaplan, 1967
; Gustafsson and Albert, 1999
; Kuzoff et al., 2001
). The gynoecial primordium, in this case a ring primordium, arises on a concave floral apex; it is therefore initiated as an inferior ovary, beneath the level of the other floral organs. Subsequent differential growth results in the ultimately superior (or nearly superior) position of the ovary in Vochysieae. This is in contrast with the pattern seen in most species with superior ovaries, in which the floral apex is convex. In these species, the ovary is initiated and remains above the level of the other floral organs (Gustafsson and Albert, 1999
).
The term "pseudosuperior" has been suggested to designate ovaries that appear superficially to be superior but in fact are inferior up to one-fourth of their length and that develop on a concave floral apex. At maturity, these ovaries have a small inferior region that can be detected only when examined carefully (e.g., with scanning electron microscopy)(Kuzoff et al., 2001
; D. Soltis, University of Florida, personal communication). However, the shape of the apex in the developing flower and the ovary position in the mature flower are not always correlated (Soltis and Hufford, 2002
). In addition, although a concave floral apex is considered characteristic of epigynous flowers, it is also seen in perigynous flowers (e.g., Evans and Dickinson, 1999a
, b
). This may indicate a relationship between epigyny and perigyny, or it may suggest that the significance of the correlation of a concave floral apex with epigyny has been overemphasized.
In Vochysiaceae, all taxa share the same state for the early development character (concave floral apex) but differ in the mature ovary position character: in Erisma and Erismadelphus, it is inferior; in Vochysia, it is semi-inferior; in Qualea and Callisthene, it is superior. Thus, the genera of Erismeae fit the common pattern for an epigynous flower, and the ovary of Vochysia fits the definition of pseudosuperior. However, the situation in Qualea is not as clear: the ovary is initiated on a concave apex, but the mature position is fully superior. To avoid confusion we have chosen to treat early and late ontogenetic stages as two separate characters. Thus, all Vochysiaceae share the early ontogenetic character of concave floral apex, but they differ in the late character in having inferior, semi-inferior, or superior mature ovaries.
By examining development in a phylogenetic context, we can better understand the different ovary positions and locule numbers found in Vochysiaceae flowers. First, developmental data indicate that the superior or nearly superior ovary seen in Vochysia, Qualea, and Callisthene is not homologous with the superior ovary in other families. Second, the status of Vochysiaceae as a monophyletic family indicates that the different ontogenetic trajectories that produce the different anthetic morphologies share a common evolutionary history. Finally, the inclusion of Vochysiaceae in Myrtales and the sister-group relationship with Myrtaceae suggest that this history involves derivation from a flower with an inferior, multilocular ovary.
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FOOTNOTES |
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2 Current address: Yale University, Department of Molecular, Cellular, and Developmental Biology, P.O. Box 208104, New Haven, Connecticut 06520 USA (amy.litt@yale.edu)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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