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0 Department of Biology (Ecology, Evolution and Marine Biology), University of California, Santa Barbara, California 93110-9610 USA; and Department of Biology, Louisiana State University, Baton Rouge, Louisiana 70803 USA
Received for publication March 23, 1999. Accepted for publication August 27, 1999.
ABSTRACT
Floral development using scanning electron microscopy is compared in several taxa of the Brachystegia subtribal group of caesalpinioid tribe Detariae. This group is characterized by missing sepals and/or petals. In Aphanocalyx djumaensis, Monopetalanthus durandii, and two Brachystegia species, one sepal is initiated in median abaxial position. In the first two, one or two additional sepal rudiments may initiate late. Brachystegia species have all five sepals, which remain scalelike. In Aphanocalyx and Monopetalanthus, one petal initiates adaxially and medianly (a position atypical for the first initiated petal in the family); additional petal rudiments may form in lateral sites. In Brachystegia, five petals are initiated unidirectionally on a meristem ring, but all are suppressed after initiation. In all taxa, ten stamens are initiated on a ring meristem: unidirectionally in Monopetalanthus, bidirectionally in Brachystegia, vs. in erratic order in Aphanocalyx. Carpel and petal initiation are concurrent. Different organ whorls overlap in time in Monopetalanthus and Brachystegia. In all, the floral apex characteristically is elongate radially and narrow tangentially after bracteole initiation. Two ontogenetic features, the meristem ring and the radially elongate post-bracteole floral apex, appear to be possible synapomorphies for the Brachystegia group.
Key Words: Aphanocalyx • Brachystegia • Detarieae • development • Fabaceae • flower • legume • Leguminosae • Monopetalanthus • ring meristem
The Caesalpinioid tribe Detarieae sensu lato (s.l.) includes ~80 genera, half of the total in the legume subfamily Caesalpinioideae, and yet it is the least known tribe of the four in the subfamily. The taxa of Detarieae share a tendency toward "repeated and spectacular modification of the flower" (Cowan and Polhill, 1981a
), with a continuous range of floral modification among Detarieae sensu stricto (s.s.) and the former Amherstieae. Tribe Amherstieae is currently subsumed into Detarieae, mainly because no apomorphies separate the two. The tribe is currently under intensive study by several investigators who are using a variety of approaches to study systematic relationships within Detarieae s.l.
Bracteoles are a significant character in Detarieae (Cowan and Polhill, 1981a
). The type of aestivation of the paired bracteoles was thought by Léonard (1957) to separate tribe Amherstieae (valvate) from Detarieae s.s. (imbricate). The bracteoles in Amherstieae tend to be large, showy, and attached closely below the flower, assuming the enclosing protective function of the sepals or even of petals; bracteoles of Detarieae s.s. are generally imbricate, and neither large nor showy. Increasingly, however, these differences are being shown to be inconsistent and insufficient as a basis for separation. Cowan and Polhill (1981a), while keeping the two tribes separate, favored combining the two into a single tribe, Detarieae s.l. Léonard (1952) established eight informal groups of genera within the African members of Cynometreae/Amherstieae in his key to genera; this arrangement was thought by Cowan and Polhill (1981a, b) to approximate monophyletic groups most closely. They added two more groups for extra-African taxa. The three genera herein belong to one of Léonard's informal groups, the Brachystegia group. Breteler (1995) points out that the bracteoles assume the protective function in the Brachystegia group, where perianth parts are few or missing. He supports maintaining tribe Amherstieae under the new name of Macrolobieae, which would include all of the taxa studied here.
The long-term aim of this work is to examine and compare floral ontogeny of representative taxa throughout tribe Detarieae and thereby to re-assess the systematic value of Léonard's groups in the tribe. In this first paper of a series on Detarieae, floral development will be compared in four taxa, representing Léonard's Brachystegia group: Aphanocalyx djumaensis, Brachystegia (two species), and Monopetalanthus durandii. All three genera are remarkable for loss of perianth, but that loss has occurred via different pathways. Incomplete developmental series of additional members of the Brachystegia group, Didelotia africana and Librevillea klainei, were also examined and compared. Of special interest in the Brachystegia group are specializations leading to loss of either sepals or petals, or both. The second aim is to point out a significant developmental distinction concerning bracteole ontogeny among Detarieae.
MATERIALS AND METHODS
Inflorescences and flower buds of various sizes of Aphanocalyx djumaensis, Brachystegia boehmii, Monopetalanthus durandii,2 Didelotia africana, and Librevillea klainei were liquid-preserved in the field in Gabon and Zambia by F. J. Breteler, J. J. Wieringa, and colleagues (Table 1). Material of Brachystegia glaucescens was collected in the National Botanic Garden, Harare, Zimbabwe by B. Browning and S. Katini. Buds were transferred to 95% alcohol and dissected in the laboratory, further dehydrated through an ethyl alcohol series, critical point dried with CO2 in a Tousimus Samdri-780 drier, and mounted on aluminum stubs with carbon conductive adhesive tabs (T. Pella Co., Redding, California, USA). They were coated with gold-palladium in a Denton Desk-1 sputter coater, and micrographs were taken at 25 kV with a Hitachi S-415A scanning electron microscope (SEM) in the Department of Biology, University of California, Santa Barbara, California, USA.
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Reduced numbers of sepals and/or petals are marked in the three genera to be described: Aphanocalyx (Figs. 1a–f), Monopetalanthus (Figs. 2a–f), and Brachystegia (Figs. 3a-f). Ontogenetic pathways differ in various ways.
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The flowers of A. djumaensis (Fig. 1a, b) lack a calyx, or sepals are represented by three minute teeth at most (two in Fig. 1c). The abaxial median sepal is most often present; the one or two additional sepals are in lateral adaxial positions, to either side of the vexillar petal. There is usually a single obovate-cuneate petal (Fig. 1a–c, e) in adaxial position (the vexillar petal), which overtops the bracteoles. Occasionally one or two additional petals, much smaller than the first, are formed in lateral "wing" positions. No petal primordia form in the lateral abaxial positions of "keel" petals. There are ten fertile stamens (Fig. 1a, b) with small versatile anthers and filaments either free or slightly united basally. The gynoecium (Fig. 1f) has a short centrally attached stipe, filiform style, capitate stigma, and an ovary containing two ovules. The fruit becomes compressed, dehiscing by two woody valves (Hutchinson, 1964
).
Organogeny
In Aphanocalyx djumaensis, the floral meristems arise in axils of bracts that are initiated in acropetal, helical succession in the raceme (Fig. 4). Each floral meristem at the time of bracteole initiation is tangentially broad and narrow in the median sagittal plane, which bisects the flower and its subtending bract. The two opposite bracteoles arise successively and laterally (Figs. 5, 6), in the plane perpendicular to the median sagittal plane. The bracteole bases are broad at their initiation, together occupying ~90% of the apical circumference (Figs. 6, 7). The two bracteoles are in contact adaxially, but not abaxially. The floral meristem after bracteole initiation is obovate in polar view (Fig. 7), widest toward the adaxial side but with a narrow isthmus abaxially.
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Stamen primordia are initiated next, in erratic order, on the periphery of the quadrangular floral apex (Fig. 9). In Fig. 9, a lateral antesepalous stamen primordium appears to have been initiated first; two other primordia of the same whorl are also evident in adaxial positions (at arrows). At least two stamen primordia of the inner, antepetalous whorl have also been initiated (at arrowheads, one at lower right and one immediately above the stamen labelled "A"). Initiation of the two whorls of stamens overlaps in time, and the order even within each whorl is atypical. Despite the erratic order, the ten stamens formed are in regular antesepalous and antepetalous sites (Figs. 10–12), the former being consistently larger than the latter at any one time.
A single petal primordium is initiated (Figs. 10–11) in adaxial median position, during initiation of the stamens. The petal primordium remains very small (Figs. 10–14) while stamens and carpel begin enlargement. In the two lateral adaxial wing-petal sites (arrows, Figs. 11–15), minute shelves of tissue become evident after stamen initiation is completed. No sign of petal rudiments is seen in the two abaxial "keel" positions (compare petal sites external to the antipetalous [a] stamen primordia in Figs. 13 and 15). A flat ridge also is present external to the adaxial petal primordium (at arrow, Fig. 10; above "P" in Fig. 11). It is not an organ, but rather appears to be a remnant of the floral apex that projected acutely at that site (Fig. 7) before organogeny began.
Organ enlargement and differentiation of Aphanocalyx
In organogenetic stages, only one sepal primordium, the abaxial one, was seen to initiate. It persists in a primordial condition (Fig. 16) at the beginning of midstage, when the stamen primordia are 50–73 µm high and the carpel primordia are ~85 µm high. In late bud stage, the sepal rudiment is ~130 µm high (Fig. 23). Occasionally one or more additional sepal rudiments are visible in late stages of development; lateral adaxial sepals are seen in Figs. 18–23. No lateral abaxial sepal primordia were observed at any stage. In some flowers, the rudiments of petals and sepals may form a basal sheath of varying height around the adaxial side of the flower, but the individual organs cannot be discerned.
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Stamen primordia are undifferentiated through a height of 50–70 µm (antepetalous and antesepalous members, respectively; Fig. 16). The primordia broaden distally, and anther and filament become distinguished in members of both stamen whorls at heights of 60 and 90 µm, respectively (Fig. 17). The anthers become broadly orbicular (Fig. 18–21), and the dorsal groove forms (at arrow, Fig. 19) between incipient microsporangia. This groove remains rather shallow (Fig. 23) compared to the median ventral groove (Fig. 24). Introrse lateral grooves form next (arrows, Figs. 20, 22), that will become dehiscence sutures. Carpel enlargement includes appression and closure of the carpel margins by a height of ~140 µm (Figs. 18, 22). Later stages of carpel development were not recorded.
Monopetalanthus (Figs. 2a–f, 25–46)
Monopetalanthus Harms includes eight species of large trees of tropical West Africa (Hutchinson and Dalziel, 1954–1958
). The inflorescences are short axillary racemes that resemble strobili in bud. In M. durandii, the inflorescence bracts are broadly ovate, imbricate, and deciduous. The paired bracteoles (Fig. 2a, c) associated with each flower are white inside and form an oval, spreading, densely velvety involucel that persists through flowering.
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Organogeny of Monopetalanthus
In Monopetalanthus durandii flowers are initiated by the inflorescence apical meristem (Figs. 25, 26,) in the axils of bracts initiated in helical acropetal succession (Fig. 25). In each axil, the floral apex initiates two bracteoles in succession (Figs. 27, 28). These bracteoles have a wide base of attachment, occupying ~90% of the apical circumference (Figs. 26, 29,). The bracteoles rapidly cover the floral apex (Fig. 26). The bracteole margins are not in contact, but their margins are closely adjacent adaxially. The floral meristem after bracteole initiation is elongate in the sagittal plane that bisects both floral apex and its subtending bract (Fig. 29); it narrows to a point adaxially, to a narrow isthmus of meristem abaxially (Figs. 28, 29).
The first floral organ initiated is the sepal primordium in median abaxial position, on the narrow isthmus of meristem (Figs. 29, 30). It is the only sepal primordium visible until midstage in ontogeny, after all other organs have been initiated. The next organ to appear is the vexillar petal, initiated in median adaxial position (Fig. 30). This petal primordium arises above and inside a flat narrow shelf of tissue (Fig. 31, arrow), which positionally may represent the confluent margins of two adaxial sepal primordia, although they are not recognizable as primordia at this time.
The floral apex broadens and becomes circular, as the carpel primordium is initiated as a dome at its center (Fig. 31). A ring meristem (Figs. 31, 32) surrounds the carpel primordium. The carpel primordium is at first hemispherical, but soon becomes higher abaxially, while the adaxial side is sloping (Figs. 33, 34). The carpel, by a height of ~115 µm (Figs. 35–37), is adaxially flattened, and trichomes are beginning to form around the base. The adaxial cleft is visible at ~125 µm height (arrowhead, Fig. 38).
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Order of the inner whorl of stamens was not determined, as no organogenetic stages were obtained for this whorl. However, the five inner stamen primordia form in the expected antepetalous sites, despite lack of petal primordia external to and preceding them in time. The five inner stamen primordia are all visible in Figs. 35–36, smaller than, and alternating with, the outer stamen primordia.
The narrow shelf of tissue outside the adaxial petal extends laterally below and outside the bases of the adjacent stamen primordia (arrows, Figs. 35, 36), as stamens and carpel enlarge. The shelf extends farther around the sides as growth continues (at arrows, Fig. 37), but never reaches around the abaxial side. No organs were seen to initiate in the two abaxial petal sites. The shelf becomes indented to delimit individual primordia of lateral sepals and petals (Figs. 38, 40). In most flowers, some but not all of the sepal and petal rudiments may be present; for example, in Fig. 40, a petal primordium is missing at the site marked by an arrow. The petal and sepal rudiments remain minute, together forming a short, shallowly indented collar around the stamen bases (Fig. 46).
Organ enlargement and differentiation in Monopetalanthus
The abaxial sepal initiated first remains small from midstage (Figs. 37, 40) to late stage (Fig. 43), when it is narrow, acutely tipped, ~400 µm high, and covered by trichomes. The large adaxial petal becomes broadly obovate with a narrowed base (Fig. 42) at 670 µm height. The additional perianth members are mere rudiments; of these, the most commonly seen in large buds (in addition to the large adaxial petal and the abaxial sepal) are two adaxial sepal rudiments, ~200 µm high, on either side of the adaxial petal (Figs. 42, 46). In addition, lateral sepal and petal primordia are seen occasionally at midstage (Fig. 40), but not in older flowers. The two abaxial petals are always missing.
Antesepalous stamen primordia are ~75 µm in height before starting to differentiate by distal expansion (Fig. 39). The antepetalous stamen primordia begin to enlarge distally at ~53 µm high (Fig. 40). All stamen primordia of a whorl differentiate essentially synchronously. With enlargement, anthers becomes dorsifixed (Fig. 43) and develop introrse lateral sutures. The outer stamen filaments are basally flared (Figs. 45, 46). As the carpel enlarges, its trichomes elongate and appear more densely packed (Figs. 39–42, 44, 45). The adaxial suture is still visible distally across the flattened summit (at arrow, Fig. 44).
Brachystegia (Figs. 3a–f, 47–
83)
Brachystegia includes ~70 species of tropical African trees. Complete series were obtained for B. boehmii and B. glaucescens. The flower of Brachystegia glaucescens is illustrated (Fig. 3a–f); B. boehmii has a similar appearance. The inflorescences are usually terminal racemes or panicles with early-deciduous bracts (Hutchinson, 1964
). The bracteoles (Fig. 3a, c) are thick, valvate, and persist below the open flowers. In Brachystegia boehmii, the inflorescence is a raceme (Fig. 47) with acropetal, helical order of initiation of flowers, each in the axil of a bract. The flowers (Fig. 3a, b, e) have five small sepals but no petals (Thompson, 1924
; Hutchinson, 1964
). Two of the sepals become laterally confluent (Fig. 3b, d). The ten stamens (Fig. 3a, b) have filaments inverted in bud (Fig. 3e) and versatile anthers (Thompson, 1924
). The gynoecium is stipitate and centrally attached (Fig. 3f). The elongate, glabrous style is coiled in bud (Fig. 3f), and the stigma is capitate.
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The first sepal primordium forms abaxially and nonmedianly (Fig. 50) and the second sepal adaxially and subopposite the first (Fig. 50). While the latter appears median, it is canted to one side. Initiation of the last three sepals is delayed (Fig. 57–59) until after all stamens are initiated. The two laterals form, and the last sepal is initiated in adaxial but off-median position (Fig. 59).
Petal initiation was not observed. Some petal primordia were, however, identifiable later as points external to antepetalous stamen primordia (Fig. 60–62). The petal primordia remain as rudiments, small cushions of tissue ~13 µm high (Figs. 60–62), external to the bases of the antepetalous stamens.
The carpel is initiated concurrently with formation of the ring meristem (Figs. 51–52) and rapidly becomes highly convex (Fig. 53) and remains so to a height of ~40 µm (Fig. 56). An adaxial cleft becomes evident by a height of ~50 µm (Figs. 57, 58). The gynoecium develops a basal stipe attached centrally at the base of a shallow hypanthium (Fig. 64).
Antesepalous stamen primordia are initiated on the ring meristem, the two laterals first (arrows, Figs. 53–54), the abaxial member of the whorl presumably next, based on relative sizes of the five antesepalous primordia a little later (Fig. 60). The two adaxial antesepalous members are initiated last (Figs. 56–57). The order in the antesepalous whorl appears bidirectional, starting with the laterals. Inner or antepetalous stamens alternate with the antesepalous stamens and apparently overlap with them in time of initiation, since both sets appear at the same time. Initiatory stages were obtained only for the upper half of the flower; in Figs. 54–56, antepetalous stamen primordia are initiated in lateral positions adaxially. The vexillary antepetalous stamen is the last to be initiated (Fig. 57). All five antepetalous stamen primordia are present in Figs. 58, 60–61).
Stages showing subsequent development and differentiation were scarce in the collections. Ciliate-margined sepals enclose the floral bud (Fig. 63), and appear scale-like at anthesis (Fig. 3a, d, e). Differentiated stamens have tetrasporangiate anthers (Fig. 64) and filaments that are inverted in bud (Fig. 3e) and elongate greatly at anthesis (Fig. 3a). The carpel differentiates as a gynoecium with hair-covered ovary, stipe, coiled style, and capitate stigma (Fig. 3f). No petals are seen at anthesis.
In Brachystegia glaucescens, the early part of floral organogeny is similar to that described above. Floral structure of B. glaucescens differs slightly from that of B. boehmii in that all five petals were seen to be initiated, but the primordia are resorbed by the time of stamen initiation. Minute ledges persist inside the calyx, possibly representing rudiments of petals.
Flowers are initiated singly in the axils of helically arranged bracts in the racemose inflorescence (Fig. 65). Each floral apex is at first tangentially broader than high (Fig. 66), Paired bracteoles arise in succession at the sides of the floral apex (Fig. 67). The floral apex heightens after bracteole initiation and retains a radially elongate form (Fig. 68) (resembling an "omega" in outline) between the bracteole bases.
The first sepal primordium forms abaxially and nonmedianly (Figs. 69, 70) and the others in a helical succession: second sepal adaxially and nonmedianly (Fig. 70). This second sepal primordium incorporates an adaxial point of the apical meristem, although it is not at the center of the sepal, which remains asymmetrical in position. The third sepal is initiated laterally (Fig. 71), the fourth on the opposite lateral side (Figs. 72–74), and the fifth after some delay, adaxially and nonmedianly (Figs. 75–77; initiation not shown). Figure 76 shows the fifth sepal present adaxially, beside the second with its asymmetrical "point." The two adaxial sepals become confluent later.
The floral apex at the time of petal initiation is unequally pentagonal (Figs. 72–73). Petal primordia are initiated (Figs. 72–74), probably simultaneously, but they fail to develop further. In Fig. 78, the abaxial petal primordia are no longer visible, probably resorbed during antepetalous stamen initiation. The tiny ledges exterior to the antepetalous stamen primordia may represent petal rudiments (arrowhead, Fig. 81).
The carpel is initiated by conversion of the remainder of the floral meristem (Figs. 74–75). A ring meristem, a broad flat rim that includes the petal-primordial points, forms at the same time around the carpel base. The carpel remains a convex dome to a height of ~40 µm (Fig. 80). An adaxial cleft becomes evident (Fig. 81) by ~80 µm height.
Antesepalous stamen primordia are initiated on the ring meristem next, with the two laterals initiating first (Fig. 76), then the abaxial member of the whorl (Figs. 77, 79). The last two members of the whorl are initiated on the adaxial side; the order in this whorl is bidirectional, beginning laterally. Inner or antepetalous stamens are initiated, starting with the two on the abaxial side (Figs. 78–80), alternating with the antesepalous stamens. After all five are initiated (Fig. 81), the order appears to be unidirectional.
Subsequent development and differentiation stages of the flower were not available for B. glaucescens. Later stages show nearly mature stamen anthers (Fig. 82) and stigma and style (Fig. 83). The main differences in the two species, then, are: the ring meristem is well developed in B. boehmii, but less well developed in B. glaucescens. Petal initiation directly follows sepal initiation in B. glaucescens, while in B. boehmii petals are initiated after stamen and carpel primordia.
Additional members of Brachystegia group examined
Some older stages of Didelotia africana and of Librevillea klainii, also in the Brachystegia group, can be compared with the preceding taxa. In Didelotia africana, the flowers have a pair of large bracteoles colored brilliant orange inside. Rudiments of five sepals and five petals surround the bases of the five stamens and the gynoecium. The rudiments are scarious, ovate, and acutely pointed and are in two whorls, each whorl basally connate.
In Librevillea klainii, the flowers have large, persistent, reflexed bracteoles and no perianth in most flowers. Some buds had a single small sepal. There are nine or ten stamens and the gynoecium. Both Didelotia africana and Librevillea klainii are consistent with the other taxa examined here that were represented by complete ontogenetic series, in showing either complete loss of perianth members or strong reduction of perianth members if any are initiated. Because no organogenetic stages were available for study, it remains a question whether Didelotia and Librevillea share the apomorphies of the "omega type" bracteole apex and the ring meristem.
DISCUSSION
Loss or suppression of sepals or petals
One petal is the only perianth organ of consequence in Aphanocalyx djumaensis and Monopetalanthus durandii, and species of Brachystegia lack petals altogether at anthesis. Loss of organs has been noted only rarely in other legumes: all petals missing in Ceratonia (Tucker, 1992
), four of the five petals missing in Ateleia (Tucker, 1990
) and in Swartzia (Tucker, 1989
, and unpublished data), and certain stamens missing (Gleditsia in Tucker, 1991
; Saraca and Swartzia in Tucker, 1989
; unpublished data). More common are examples in which organs appear to be missing at anthesis, but exist as rudiments. Examples include four of the five petals in Amorpha (Tucker, 1987a
, 1988c, 1989), certain petals and stamens in Bauhinia (Tucker, 1988b
), and stamens in neuter flowers and carpels in the staminate flowers of Neptunia (Tucker, 1988a
).
A hypothesis was proposed (Tucker, 1988c
) that organ loss in one organ whorl tends to disrupt the next successive whorl. For example, the flower of Ateleia has only one petal primordium, after which the floral apex produces a ring meristem (very rare in legume flowers) on which stamen primordia are initiated in erratic, atypical order and positions (Tucker, 1990
). Ceratonia (Tucker, 1992
) lacks petals altogether, and the stamens initiated directly after the sepals are highly atypical in their mode of initiation and in their positions. In Gleditsia triacanthos, flower-subtending bracts are missing; many aspects of its subsequent floral initiation are atypical for legumes (Tucker, 1991
). In Dialium guineense each flower has a single petal, followed by initiation of only two stamens that are initiated in unusual positions (Tucker, 1998). The flowers of Achlya (Berberidaceae) lack subtending bracts, sepals, and petals; stamen number and order of initiation are highly erratic (Endress, 1989
). In most of these examples, it is loss of perianth organs that is most disruptive of subsequent organ initiation.
The taxa studied in the Brachystegia group provide examples in which some floral organs (sepals and/or petals) fail to initiate at their usual time, after which a ring meristem is formed by the floral apex. Order of stamen initiation on the ring meristem is erratic, although the arrangement at anthesis is typical in having two whorls. For example, in Brachystegia glaucescens (all petals are initiated but then resorbed), the lateral stamen primordia are initiated first, while in most caesalpinioid legumes the median abaxial stamen primordium forms first. In B. boehmii, the outer and inner whorls of stamens apparently are initiated concurrently, while in most related caesalpinioids, the outer whorl is initiated before the inner whorl. Some (but not all) of the perianth members in the Brachystegia group are initiated late, out of order and after all other organs have been initiated, and they remain minute and rudimentary. One can conclude that delayed initiation of early organs (perianth) is correlated here with atypical patterns of initiation of other later initiated organs.
Ring meristem
In all of the taxa examined of the Brachystegia group (Aphanocalyx djumaensis, Monopetalanthus durandii, Brachystegia boehmii, B. glaucescens), a ring meristem is formed prior to stamen initiation. The floral meristem becomes a raised circular ring around the central carpel primordium that has initiated. Ring meristems are reported in some taxa in legume subfamily Mimosoideae (Gemmeke, 1982
) and in several other plant families (e.g., Malvaceae [Sattler, 1973
], Zingiberales [Kirchoff, 1988
]) but are relatively rare among legumes; published reports include Ateleia (Tucker, 1990
) and Swartzia (Tucker, 1987b
), both members of the papilionoid tribe Swartzieae. At least three other taxa in Swartzieae (Baphiopsis parviflora, Cyathostegia matthewsii, and Mildbraediodendron excelsum; Tucker, unpublished data) have a ring meristem as part of floral initiation. This is the first report of its occurrence in caesalpinioid legumes.
In taxa of Swartzieae, the ring meristem is associated with increase in stamen number, 50–200 per flower, and their order of initiation on the ring is centrifugal. But in Ateleia (Tucker, 1990
) and the taxa studied herein, ten stamens or less are produced per flower, and the order of initiation is erratic around the ring, but it is not centrifugal.
Bracteole initiation
Differences in bracteole origin in Detarieae have interesting distributions among taxa that are correlated with assemblages of other developmental character states (Table 2). The bracteole aestivation of flower buds has been considered significant previously, but aestivation can be affected by changes throughout development. This distinctive feature concerns early-occurring processes in bracteole growth. My sampling is limited, so I can only say which taxa have each type among those available for examination.
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"Omega" type
In the "Omega" group, the floral meristem at bracteole initiation is elongate sagittally and narrow tangentially. The two bracteoles are very large from their time of initiation, occupying perhaps 90% of the circumference of the floral meristem. The two bracteoles are in contact adaxially and are separated abaxially by only a narrow isthmus of floral meristem. The post-bracteole floral meristem remains elongate in the radial plane, narrow in the tangential plane. The first sepal is abaxial and median; in some taxa it is the only sepal initiated. The first petal in some of these taxa is the second organ initiated and is the median adaxial one. Thus sepal and petal initiation overlap in time, and there is marked loss of the other perianth primordia, either sepals or petals. The "Omega" type (Table 2) and associated character states occur in Brachystegia, Aphanocalyx, Monopetalanthus (Brachystegia group); Berlinia, Microberlinia (Berlinia group); Macrolobium, Gilbertiodendron, Anthonotha (Macrolobium group); Detarium, Sindora, Tessmannia (Detarium group); Cynometra (Cynometra group). The distribution among Léonard's groups is not always clear-cut, especially in the Cynometra group, where Cynometra has the Omega type, Schotia the Circular type. However, several of Léonard's groups appear not to be supported by other evidence (Gervais and Bruneau, 1999
), so this paradox concerning distribution of the bracteole type in the Cynometra group may be resolved later.
Evaluation of Léonard's Brachystegia group
Léonard (1952) proposed eight informal "groups" of African Detarieae s.l., which were adapted and increased to ten worldwide by Cowan and Polhill (1981a). The taxa studied in the Brachystegia group share most of the morphological features considered significant in our study and hence support Léonard's concept of close relationship for that group. The taxa show either complete loss of most or all perianth members, or strong reduction of any perianth members that are initiated. "Loss" of character states may be considered difficult to assess as apomorphies, because they may represent either a primitive condition of absence, or a change from presence of the organ. However, because legumes are strongly monophyletic and because the great majority of taxa in the family have all 21 floral organs (five sepals, five petals, ten stamens, one carpel), one can assume that a loss of a particular organ is indeed an apomorphic shift from an ancestor in which the organ was present.
Fortunately, the Brachystegia group also have other developmental novelties or apomorphies besides organ loss, e.g., the ring meristem that precedes initiation of individual stamen primordia, an extremely rare character among legumes, being present only in the Brachystegia group, Microberlinia (in the Berlinia group of Detarieae), two taxa of Mimosoideae (Gemmeke, 1982
), and papilionoid tribe Swartzieae (Tucker, 1987a, b
; unpublished data) of almost 300 legume taxa studied to date. Another developmental innovation that is probably an apomorphic state is the "Omega type" of apical meristem at bracteole initiation. It is judged apomorphic on the basis that the great majority of legume flowers that have a full complement of 21 organs (pentamerous whorls of sepals, petals, two stamen whorls, and a carpel) also have a circular floral apex. This "Omega type" character state of the floral apex is not unique to the Brachystegia group, but is shared with the Berlinia, Detarium, Cynometra pr. p., and Macrolobium groups.
Character states shared by the taxa studied in the Brachystegia group (represented by Aphanocalyx and Monopetalanthus in Table 2) include the helical racemose inflorescence, presence of bracteoles, median abaxial position of first sepal, ten stamens in two alternating whorls, early initiation of the carpel with the first petal, and no sepal fusion. All but the last two mentioned can be considered plesiomorphies. Ten stamens and a centrally attached carpellary stipe are shared by all examined taxa of the Brachystegia group.
The taxa studied differ primarily in character states concerning which organs are initiated, their order of initiation, and their timing. The species of Brachystegia have five sepals, initiated in helical order. Aphanocalyx has only one sepal initiated, while Monopetalanthus has three initiated, two of these belatedly as a barely visible sheath. All petals are initiated in Brachystegia species, but all are suppressed. In Aphanocalyx and Monopetalanthus only one petal is initiated in the usual succession, but on the adaxial side. One or two others may be initiated belatedly, adjacent to the first, but these remain rudiments. Petal initiation usually starts abaxially in other leguminous flowers having all five petals. Stamen initiation is erratic in direction in Aphanocalyx, unidirectional in Monopetalanthus, and bidirectional in Brachystegia. These developmental differences among taxa of the Brachystegia group are important as innovations associated with, or promoting, processes of generic and species evolution.
The assemblage of character states uniting the Brachystegia group of detarioid legumes (and shared with several other detarioid groups) may represent the result of a saltational event in evolution, similar to those suggested for nonflowering vascular plants by Bateman and DiMichele (1994). Severe limitation of size and activity of the floral apex, resulting in absence of most or all of the perianth, could have resulted in disruption of canalized pathways of development that allowed for new directions in evolution. Phylogenetic analyses are planned to explore the directions of character-state change among detarioid taxa.
FOOTNOTES
1 The author thanks Jo Anna Bass for technical assistance with scanning electron microscopy and photography, David Pierce for additional assistance with the SEM, Alison Shroeer for drawings, Bente B. Klitgaard for valuable comments, and the following for collections: F. J. Breteler, J. J. Wieringa, and colleagues, Herbarium Vadense, Wageningen, The Netherlands; and Barbara Browning and staff, National Herbarium, Harare, Zimbabwe. The research was supported by NSF grants BSR84-18922, BSR87-22514, DEB92-07671, and DEB-9420158 (DEB-9596281). Additional funding was provided by the Boyd Professor Fund at Louisiana State University. 
2 Note added in proof: Monopetalanthus durandii is now Bikinia durandii (F. Hallé & Normand) Wieringa. Source: Wieringa, J. J. 1999. Monopetalanthus exit. A systematic study of Aphanocalyx, Bikinia, Icuria, Michelsonia and Tetraberlinia (Leguminosae, Caesalpinioideae). Thesis, Wageningen Agricultural University. Wageningen Agricultural University papers 99-4. Wageningen, The Netherlands.
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