(American Journal of Botany. 2002;89:888-907.)
© 2002 Botanical Society of America, Inc.
Comparative floral ontogeny in Detarieae (Leguminosae: Caesalpinioideae). 2. Zygomorphic taxa with petal and stamen suppression1
Shirley C. Tucker2
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, California 93106-1467 USA; and Department of Plant Biology, Louisiana State University, Baton Rouge, Louisiana 70803 USA
Received for publication June 29, 2001.
Accepted for publication December 13, 2001.
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ABSTRACT
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Marked floral zygomorphy and a reduced number of petals and/or stamens are the character traits that distinguish the taxa described (species of Afzelia, Berlinia, Gilbertiodendron, Macrolobium, Neochevalierodendron, Paramacrolobium, Phyllocarpus, and Tetraberlinia). All have an "Omega"-shaped floral apex after bracteole initiation, bracteoles large when initiated, helical sepal initiation, unidirectional petal initiation (simultaneous in Afzelia, not determinable in Tetraberlinia), and unidirectional stamen initiation. Floral zygomorphy is expressed primarily by one petal being much larger than the others and by suppression of several of the stamens. Five petals are initiated in all; suppression begins in late development. Either two petals (Neochevalierodendron, Phyllocarpus) or four petals (Afzelia, Berlinia, Macrolobium, Tetraberlinia) are suppressed. All ten stamens are initiated; at midstage, suppression begins in either three stamens (Afzelia) or seven stamens (Gilbertiodendron, Macrolobium, Paramacrolobium). Other expressions of zygomorphy may include diadelphy, stamen filament connation late in development, or displacement of the carpel from a central position to the adaxial side of the hypanthium. There is no loss of organs similar to that which occurs in some other Detarieae.
Key Words: Afzelia • Berlinia • Caesalpinioideae • Detarieae • Fabaceae • floral development • flower • Gilbertiodendron • Leguminosae • Macrolobium • Neochevalierodendron • Paramacrolobium • Tetraberlinia • zygomorphy
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INTRODUCTION
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The tribe Detarieae sensu lato is the largest of the four in the legume subfamily Caesalpinioideae. It includes about 80 genera, approximately 50% of the total for the subfamily. Despite its size, the tribe has been the least well known, probably because most are tropical trees, few of which have been brought into cultivation. This lack of knowledge is being remedied by a concerted effort using several approaches: systematics and floristics (Breteler, 1995
; Breteler and Wieringa, 1999
; Wieringa, 1999
; Mackinder, 2000
), molecular systematics (Bruneau et al., 2000
, 2001
), comparative study of wood (Gasson, Trafford, and Matthews, 2000
), vegetative anatomy (Herendeen, 2000
), pollen (Banks and Klitgaard, 2000
; Banks, Klitgaard, and Crane, 2001
), reproductive biology (Lewis, Simpson, and Neff, 2000
), and comparative floral development (Tucker, 2000a
, b
, c
, d
, 2001a
, b
, 2002
).
Comparative floral ontogeny provides a basis for understanding the mechanisms that bring about the floral distinctions among related taxa. These may be heterochronic, differences in timing of shared events in development, or they may be qualitative differences, events that occur in one taxon but not in another. Both types of differences have been found in floral ontogeny of various taxa of Detarieae. One goal of this paper and other related papers is to determine which developmental character states are shared among the majority of Detarieae and which character states distinguish Detarieae from other groups of legumes. Since this group is characterized by flowers having fewer than the full complement of floral organs (21 organs) typical of most legumes, another goal is to determine whether the missing floral organs in this group result from loss (noninitiation) or suppression after organ initiation. This kind of information can only be obtained from complete ontogenetic series for each species, preferably from scanning electron microscopy (SEM). Finally, a third aim is to correlate our conclusions with those resulting from other lines of evidence.
The invaluable compendium (Polhill and Raven, 1981
) resulting from the first Legume Congress at Kew utilized and amended the classification by Léonard (1952
, 1957
) for tribe Detarieae, a notoriously confusing assemblage of caesalpinioid legumes. My comparative floral ontogenetic studies of Detarieae have shown strong correlations for some parts of Léonard's groups (i.e., Brachystegia group; Tucker, 2000a
), but not any significant intergroup distinctions. Bruneau et al. (2000)
, using molecular evidence, did not find support for Léonard's groups. The developmentally based criteria that I have used for the detarioid "Omega"-type assemblage (Tucker, 2001a
, b
) considered here include having a radially elongate and tangentially narrow postbracteole apex, rapid enlargement of bracteoles directly after their initiation so that they appear relatively large, 21 floral organs initiated, and nonhelical sepal initiation. In the first paper of this series (Tucker, 2002
) detarioid taxa with relatively moderate organ suppression were included. This second paper includes species having significant organ suppression, especially of petals and stamens. The Léonard groups represented here are the Berlinia group (Tetraberlinia), Hymenostegia group (Afzelia and Neochevalierodendron), and Macrolobium group (Gilbertiodendron, Macrolobium, and Paramacrolobium).
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MATERIALS AND METHODS
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Materials
Species studied and their provenance are listed in Table 1.
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Table 1. Sources for plant material in the present study. Vouchers are in Herbarium Vadense (Wageningen, The Netherlands) and the Royal Botanic Garden Herbarium, Kew
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Methods
Material collected by Breteler and colleagues was killed in liquid fixative (FAA: five parts formalin: five parts acetic acid: 90 parts 70% alcohol) in the field and transferred and stored in 70% ethanol. Material from the spirit collection of the Royal Botanic Garden, Kew, UK, was preserved in Kew Mixture. Young buds and inflorescences of all sizes of each species were processed for SEM. Before dissection, they were dehydrated to 95% ethanol. Bracts and larger floral organs were removed from each piece under a dissection microscope. The resultant buds were further dehydrated through an ethanol-acetone series, critical point dried with CO2, mounted on aluminum stubs with carbon conductive adhesive tabs (T. Pella, Redding, California, USA), and coated with gold-palladium. The micrographs were taken with a JEOL JSM-6300V (JEOL Co., Tokyo, Japan) scanning electron microscope in the Geology Department at the University of California, Santa Barbara, California, USA.
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RESULTS
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All the species included have strongly zygomorphic (monosymmetric) floral symmetry. Each of the species described and illustrated is typical of several that were studied; comments describe any noteworthy developmental differences for those not illustrated. The taxa are described in three groups, in order of increasing organ suppression (Fig. 1a–d).
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Fig. 1. Diagrams of the four floral types studied, showing progressive reduction in petal and stamen numbers. (a) Flower with five petals, of which three are large, and ten functional stamens. (b) Flower with five petals, of which only one is large, and ten functional stamens. (c) Flower with one large petal and four rudimentary petals, and seven functional stamens. (d) Flower with one large petal and four rudimentary petals and three functional stamens.Figure Abbreviations: A = outer or antesepalous stamen, a = inner or antepetalous stamen, Ab = abaxial side, Ad = adaxial side, Ar = rudiment of outer stamen, B = floral bract, Bl = bracteole, C = carpel, F = floral apex, G = gynoecium, P = petal, S = sepal, S1–S5 = sepals in order of their initiation, St = stigma, Sy = style
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Three large petals, ten large stamens, basally connate (Neochevalierodendron stephanii and Phyllocarpus septentrionalis)
Neochevalierodendron stephanii (A. Chev.) J. Léonard (Figs. 2–27) is a monotypic tree species of tropical Africa (Gabon). The racemes are axillary or terminal, the bracts are caducous; the bracteoles are broadly rounded-ovate, petaloid, caducous, and do not cover the bud (Fig. 2a). Flower buds are pale green. The flowers (Fig. 2b, d, and e) are zygomorphic with four, free, imbricate, glabrous, coriaceous sepals that are pink inside. Among the five petals, three are large and suborbicular, cordate, short-clawed, imbricate, and densely tomentose adaxially, while the other two are minute. The largest petal is pinkish at center toward its base. The ten uniform stamens are pink and have filaments connate basally and anthers dorsifixed, opening lengthwise. The stipitate ovary is adnate to one side of the tubular hypanthium (Fig. 2c). There is an elongate style that is coiled in bud, and a capitate papillate stigma. Nectaries, pads on either side of the large petal base at anthesis (not shown in this work), attract ants that nest on branchlets (Hutchinson, 1964
; Cowan and Polhill, 1981a
, p. 128; and label data by F. J. Breteler).
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Fig. 2. Drawings and floral diagrams of Neochevalierodendron stephanii. (a) Floral bud and bracteoles. (b) Floral diagram. (c) Gynoecium and hypanthium in longitudinal section. (d) and (e) Large bud with perianth removed, showing stamen connation at base, gynoecium, and elongate hypanthium. Scale bar = 2 mm in (a) and (c); scale bar = 3 mm in (d) and (e) (scale bar is between the two)
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Neochevalierodendron stephanii, organogeny
The inflorescence apical meristem initiates bracts in acropetal and helical order (Fig. 3). Each bract subtends a floral apex that at first is narrow radially and wide tangentially (Fig. 4). The floral apex first initiates paired bracteoles, one slightly larger and preceding the other (Fig. 5). The bracteoles enlarge rapidly and envelop the floral bud from an early stage onward (Figs. 6 and 7). The narrow postbracteole floral apex broadens to become almost circular and initiates the first sepal primordium abaxially and nonmedianly, the second adaxially (Figs. 7 and 8). Order of sepal initiation is helical, as seen in Fig. 9. The petals initiate unidirectionally, beginning with two on the abaxial side (Figs. 9 and 10). The next two petal primordia are initiated in lateral positions (Figs. 10–12), together with carpel initiation. Initiation of the fifth petal primordium was not observed. After all five are present (Fig. 13), they begin to enlarge at different rates (Figs. 14–16).
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Figs. 3–14. Neochevalierodendron stephanii. Floral organogenesis (scanning electron micrographs). Abaxial side is at base in all except Figs. 3, 8, and 14
. Subtending bracts have been removed in all, bracteoles removed in Figs. 3, 6, and 8–14
, and some or all sepals removed in Figs. 9–14
. Scale bar = 50 µm in Figs. 4, 5, and 8–12
; scale bar = 100 µm in Figs. 6, 7, 13, and 14
; scale bar = 200 µm in Fig. 3
. 3. Polar view of inflorescence tip with helically arranged floral buds, most of which have bracteoles. 4. Floral apex initiating opposite bracteoles. 5. Floral apex after initiation of two bracteoles. 6. Initiation of first sepal primordium nonmedianly on abaxial side. 7–8. Polar and lateral views showing initiation of second sepal primordium on adaxial side of floral apex. 9. Initiation of first two petal primordia (at arrowheads) on abaxial side. Sepal primordia arch inward over the floral apex. 10. Floral bud with at least three petal primordia initiated, two abaxially and one laterally. 11–12. Polar and abaxial side views of a floral bud, showing carpel initiation at center. Four petal primordia are visible, with the two abaxial ones larger than the lateral two. 13. Polar view with petal primordia broadening and all five antesepalous stamen primordia (A) initiated. The three more abaxial are larger than the two adaxial ones. 14. Lateral adaxial view of young flower with petal primordia heightening. The cleft is forming in the carpel primordium
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The carpel primordium is initiated centrally, concurrently with the petal primordia (Figs. 11 and 12) and enlarges as a hemispherical dome at first and then becomes slightly flattened adaxially (Fig. 13). The adaxial cleft becomes apparent (Figs. 14–16) at an approximate height of 120 µm.
Stamen initiation is unidirectional in the outer whorl, beginning abaxially (Fig. 13); the members of the second stamen whorl appear to initiate simultaneously (Figs. 15 and 16). The abaxial and two lateral outer stamen primordia appear slightly larger than the two adaxial in their whorl, but this difference does not persist. Similarly, the abaxial members of the inner stamen whorl exceed the others in size at early stages (Fig. 19). No overlap in time of initiation between whorls was noted.
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Figs. 15–27. Neochevalierodendron stephanii. Floral organ development (scanning electron micrographs). Sepals removed in all except Fig. 15
, petals removed in Figs. 17–21 and 23
. Scale bar = 100 µm in Figs. 15–20
; scale bar = 200 µm in Figs. 21–26
; scale bar = 1 mm in Fig. 27
. 15. Polar view of young floral bud at midstage, with all organs initiated. The sepals are laterally confluent although the lobes remain distinct; they have not overarched the rest of the flower as yet. Primordia of petals and both whorls of stamens are approximately equal in size and undifferentiated. Some antepetalous stamen primordia are at arrowheads. 16. Polar view showing petals of different sizes enlarging and starting to overlap marginally. The carpel cleft is beginning to form. 17–19. Polar, adaxial side, and lateral views of a young flower with petals removed to show the five small undifferentiated antepetalous stamen primordia (a), alternating with the five antesepalous stamen primordia (A) that are inclined inward and that are enlarging distally. 20. Adaxial side view showing carpel primordium with margins appressed, and stamen primordia of both whorls still undifferentiated. 21. Polar view showing outer, antesepalous stamen primordia beginning to differentiate by enlarging distally to form anthers. 22–23. Side and adaxial views, some petals removed, to show anthers of outer stamens (A), each with microsporangia delimited by a median adaxial groove (at arrow) and developing lateral sutures (one at arrowhead). The anthers are basifixed at this stage. Trichomes are abundant on the base of the carpel. 24–26. Large floral buds in side views just before anthesis. 24. Petals are imbricate over and around the stamens. The anthers of both stamen whorls are differentiating microsporangia with median adaxial grooves (arrow) and lateral grooves (arrowhead); filaments are present only in the outer stamens (A). 25–26. Adaxial side and polar views of a young flower with all but two petals removed. The style and abundant tomentum are forming on the carpel. Anthers are differentiating with microsporangia in both outer (A) and inner whorls (a) of stamens. 27. Large floral bud in side view just before anthesis. Sepal at rear is sparsely hairy. Petal is glabrous. Stamen anthers are dorsifixed in both outer whorl (long filament) and inner whorl (short filament).
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Neochevalierodendron stephanii, organ development
The bracteoles cover the floral bud during sepal initiation (Fig. 3). The sepals enlarge in the order of their helical initiation, and the adaxial two become confluent so that they appear to be a single sepal, and the calyx appears tetramerous. The sepals are free, imbricate, and are attached to the rim of the hypanthium. The two lateral petals enlarge and overlap the enlarged vexillary petal (Fig. 24), while the two abaxial petals remain as linear rudiments (Fig. 22). One of the large petals is seen in bud in Fig. 27. At anthesis the two abaxial petal rudiments are minute or absent. The flower in N. stephanii conforms to the minimal type of organ reduction in Fig. 1a, with two petals smaller than the other three, but with all ten stamens functional.
The stamens of the outer, antesepalous whorl enlarge and differentiate before those of the inner, antepetalous whorl. All are canted inward toward the carpels (Figs. 17–19). In the outer whorl, three primordia enlarge first: the median abaxial and the two laterals (Figs. 18 and 19); these three are persistently larger than the other two outer stamens and larger than the innerwhorl stamens during development, but all become equalized in size at maturity. The outer stamens enlarge distally as anther formation begins (Fig. 21). The microsporangia develop, delimited by a median adaxial groove (Figs. 22 and 23) and the lateral grooves (Fig. 23). The inner, antepetalous stamen primordia follow the same process of differentiation, beginning with distal enlargement (Fig. 22). In midsized buds, the outer five stamens still exceed the inner five in size (Figs. 25 and 26) but toward anthesis (Fig. 1d–e), all ten are alike. The anthers are inverted in large buds.
As the carpel heightens, its margins extend and then become appressed (Fig. 20) and finally fused (Figs. 21 and 23). Trichomes form adaxially near the base (Fig. 21) and then become more abundant around the base (Figs. 23 and 25). The gynoecium becomes short-stipitate and attached to the adaxial side of the hypanthium (Fig. 2c–e). The style is elongate and coiled in large buds (Fig. 2d–e), and the stigma is capitate.
Phyllocarpus septentrionalis Donn Smith
Phyllocarpus (Barnebydendron Kirkbride) includes two species of tall trees in tropical America in the Detarium group of Léonard. Flowers are purple or red in short racemes or fascicles at the nodes of leafless 1-yr.-old branches. The bracts and small free bracteoles are caducous. The flowers are zygomorphic with a short calyx tube, four imbricate subequal sepal lobes, and three imbricate obovate petals. The ten diadelphous stamens have a connate sheath split on the upper side; the anthers are uniform, versatile, and ovate. The ovary is stipitate and free, the style filiform, the stigma clavate, and no hypanthium is present (Baillon, 1872
; Hutchinson, 1964
; Cowan and Polhill, 1981a
, p. 133).
Floral development of Phyllocarpus septentrionalis resembles that of the previous species including acropetal, helical order of flower initiation in the racemose inflorescence, the "Omega-type" narrow postbracteole floral apex, massive bracteoles, helical initiation of five sepals, nearly simultaneous initiation of five petals, and unidirectional initiation of the five antesepalous stamens.
One large petal, nine or ten stamens (Berlinia and Tetraberlinia)
The genus Tetraberlinia (Cowan and Polhill, 1981b
, p. 138) includes four species of tropical African forest trees in Guinea and Congo. Wieringa (1999)
showed that Tetraberlinia is close to Aphanocalyx and Monopetalanthus, previously studied (Tucker, 2000a
).
Tetraberlinia tubmanniana J. Léonard (Figs. 28–56)
Tetraberlinia tubmanniana is a large forest tree bearing compound racemes (Wieringa, 1999
) that contain 4–14 flowers on each of several side branches. The bracteoles are ovate, asymmetric, and velvety pubescent (Wieringa, 1999
). The zygomorphic flowers (Fig. 28a and e) have five white to pale greenish sepals, densely pubescent outside, with the adaxial two nearly completely fused. The five petals include a large adaxial yellow petal, 6–8.5 mm long with a short wide claw; the limb is rectangular and ciliate margined. The lateral petals are white and linear to 4.5 mm long. There are ten uniform stamens with filaments 12–15 mm long, of which nine are basally connate. The ovary is stipitate with an elongate style and a heart-shaped stigma; the stipe is inserted at the base of the cupular hypanthium (Fig. 28d; Wieringa, 1999
). Tetraberlinia is included in Berlinia by Hutchinson (1964)
and is in the Berlinia group (Cowan and Polhill, 1981b
, p. 138). It is placed in the Macrolobium group of Breteler and Wieringa (1999
; Wieringa, 1999
). Wieringa's phylogenetic analysis (1999)
shows Tetraberlinia as the monophyletic sister group to Bikinia/Aphanocalyx.
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Fig. 28. Drawings and floral diagrams of Tetraberlinia tubmanniana. (a) Open flower with bracteoles. (b) Large undissected bud. (c) Flower bud starting to open. (d) Longitudinal section of flower showing gynoecium attached basally in hypanthium. (e) Floral diagram. Scale bar = 2 mm in (a)–(d)
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Tetraberlinia tubmanniana, organogeny
The inflorescence apical meristem initiates bracts acropetally and distichously (Fig. 29). In each bract axil a floral apex is initiated, which is at first radially narrow and tangentially wide (Fig. 29). Two bracteoles are initiated in succession by the floral apex (Figs. 30 and 31). The narrow postbracteole floral apex broadens somewhat and is "Omega"-shaped (Fig. 31; see Tucker, 2000a
for explanation), with small projections adaxially and abaxially. The bracteoles enlarge massively at this time (Fig. 32) and remain in contact with the floral apex around its entire periphery.
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Figs. 29–44. Tetraberlinia tubmanniana. Floral organogenesis (scanning electron micrographs). Abaxial side is at base in Figs. 31, 32, 35–38, and 40–42
; it is marked in most of the others. Subtending bracts have been removed in all except Figs. 29 and 30
, bracteoles removed in all except Figs. 29, 30, and 32
; and one sepal has been removed in Figs. 38, 39, and 42–44
. Scale bar = 50 µm in Fig. 34
; scale bar = 100 µm in Figs. 29–31, 33, and 35–44
; scale bar = 300 µm in Fig. 32
. 29. Polar view of inflorescence tip. The inflorescence meristem is at arrowhead. A bare floral apex is at base, and an undissected floral apex with bracteoles is at top. 30. Side view of floral apex with one bracteole removed. 31. Floral apex after initiation of two bracteoles (removed). 32. Part of floral bud inside one of enlarged bracteoles with very thick wall and trichomatous covering. 33–34. Polar and lateral views showing initiation of first sepal primordium nonmedianly on abaxial side. Note in Fig. 34
that floral apex is truncate, with a raised rim all round. 35. Second sepal primordium is initiating nonmedianly on adaxial side. 36–37. Polar and oblique lateral views showing two confluent sepal primordia on adaxial side and raised lateral ridges that may represent the two lateral sepal primordia. The median adaxial and one lateral petal primordium have initiated, but the abaxial petal sites are obscured by a sepal. The initiating carpel primordium is at center. 38–39. Polar and lateral side views of floral bud with all five petal primordia, the carpel, and three antesepalous stamen primordia initiated (A = the median abaxial and the two lateral antesepalous stamen primordia). The sepal primordia remain little evident, as a lateral ridge (at arrowheads). 40–41. Adaxial side and lateral side views of floral bud with large abaxial sepal primordium covering the abaxial half, but other sepal primordia represented merely by lateral ridges. The adaxial median petal primordium has grown very little, although it was first to initiate in its whorl. The two adaxial stamen primordia of the antesepalous whorl have initiated (at arrowheads). 42–43. Polar and lateral views of floral bud showing primordia of the five petals, five antesepalous stamens (A), and spaces for the five antepetalous stamens (some at arrowheads). The carpel primordium is highly convex. 44. Polar view of floral bud with the sepals beginning to enlarge (the largest one removed) and grow over the inner organ primordia. Petal and stamen primordia are similar and undifferentiated. The carpel primordium is developing an adaxial cleft
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Sepal initiation is helical. The first sepal is initiated abaxially and nonmedianly (Fig. 33), and the second is initiated adaxially and nonmedianly (Fig. 35). The periphery of the floral apex at this time becomes truncate, forming an undulating ridge (Fig. 34). The last three sepals are probably initiated in close succession, although the primordia are so broad and low that they are difficult to distinguish close to initiation (Figs. 36–40). All sepal primordia except the adaxial one remain suppressed for a time and form a shallow calyx cup with a sinuous margin (Figs. 41 and 42, et seq.).
The order of petal initiation was not determined, because the abaxial petal sites were obscured in the only floral bud found at this stage (Figs. 36 and 37). The adaxial and one lateral adaxial petal primordium have initiated, but it cannot be determined whether the abaxial ones have initiated. After all five petal primordia have initiated (Figs. 38 and 39), they are equal in size, although the adaxial one is broad and flat while the other four have increased more in height.
The timing of carpel initiation was not determined precisely; it is initiated concurrently with either the petals or the outer stamens (Figs. 36 and 37). The carpel primordium is relatively small at initiation in this species, approximately the same size as individual stamen or petal primordia at the same time. In related detarioid genera, the carpel is usually about twice the basal diameter of any other floral organ just after initiation. The carpel in this species enlarges at first as a hemispherical dome (Figs. 38 and 39).
The outer, antesepalous stamens are initiated bidirectionally, starting with two laterals (Figs. 38 and 39). After the single abaxial and two adaxial members have initiated in the same whorl, they appear equal in size (Fig. 42). The stamen primordia of the inner antepetalous whorl begin initiation on the abaxial side (Fig. 39), so are unidirectional, although they all appear equal in size very early (Fig. 42). Initiation overlaps in time between the two whorls. The innerwhorl stamen primordia are rapidly covered by the enlarging outer floral organs, but some can be seen in Figs. 50, 53, and 54. No ring meristem is present, although it does occur in taxa thought by Wieringa (1999)
to be closely related to Tetraberlinia. The ring meristem will be considered more at length in the Discussion.
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Figs. 45–56. Tetraberlinia tubmanniana. Floral organ development (scanning electron micrographs). Sepals removed in all except Figs. 45 and 46
; other organs selectively removed to reveal inner structure. Scale bar = 100 µm for Figs. 45–47
; scale bar = 200 µm for Figs. 48–50
; scale bar = 1 mm for Figs. 51–56
. 45–46. Side and adaxial views of floral bud at midstage. Sepal lobes of variable heights are being raised up on a short calyx tube. The petal and stamen primordia are undifferentiated. The carpel cleft is beginning on the adaxial side. 47–48. Successive stages, adaxial and lateral side views, of floral bud with petal primordia heightening and developing a lamina. 49. Polar view of floral bud, two petals removed. Microsporangia are developing in the anthers of antesepalous stamens. 50. Side view of floral bud, petals removed, showing antesepalous (A = outer) stamens with basifixed anthers. Antepetalous (a = inner) stamen primordia are less differentiated than those of the outer whorl. The style and basal trichomes are forming on the carpel. 51–53. Adaxial, lateral, and abaxial views of young flower showing the largest petal adaxially and four smaller, linear petals (at arrowheads) laterally and abaxially. Stamen anthers are now dorsifixed in both antesepalous and antepetalous whorls, and stamens are erect. The gynoecium has a densely hairy ovary and a coiled glabrous style. 54–55. Lateral and polar views of large bud, sepals removed, showing the large, enveloping vexillary petal on the adaxial side, and the stamen anthers inverted. 56. Adaxial side of stamen with microsporangia delimited by a median groove (at arrow) and lateral sutures (at arrowheads) between microsporangia, and a cluster of trichomes at filament base
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Tetraberlinia tubmanniana, organ development
The bracteoles become very thick and enclose the floral bud during development (Figs. 28b and 32). The sepals form a confluent calyx cup with short lobes (Fig. 45) in early stages. The abaxial sepal remains largest, with the two laterals beginning to overlap the center by midstage (Figs. 44 and 46). Close to anthesis, the sepal lobes are graded in size and relatively large (Fig. 28c) compared to the calyx cup.
The petal primordia remain short and undeveloped until after all other organs are present. Laminar growth becomes evident as the petals grow in height (Figs. 47 and 48). Four of the petals remain short (Figs. 51–53, at arrowheads), while the fifth enlarges (Figs. 28e and 51–55). At anthesis only one petal is evident (Fig. 28a).
The outer, antesepalous stamen primordia are larger than the innerwhorl stamen primordia at any one stage and also begin differentiation first. Anthers and filaments begin differentiation in the outer stamens (Figs. 49 and 50); later stages with elongate filaments and mature anthers are seen in Figs. 53–56. The innerwhorl stamens begin differentiation (Fig. 50), follow the same ontogeny as the outer stamens, and appear fully differentiated in Fig. 54. The anthers of all stamens change from erect (Figs. 52 and 53) to inverted positions (Fig. 54) in bud, and then become versatile at anthesis (Fig. 28a). All ten stamens are functional and alike in the flower at anthesis.
The carpel is a high-convex mound at a height of about 80 µm (Fig. 43). The adaxial side flattens (Fig. 44) and then the cleft becomes visible at an approximate height of 120 µm (Fig. 45). The margins become appressed and remain so during subsequent development. At a height of about 270 µm the tip becomes attenuate as the style starts to form (Fig. 50). In the large bud, the style is linear, glabrous, coiled, and folded over the summit (Figs. 28a and 53). Trichomes begin to form over the ovary at a height of about 270 µm (Figs. 49 and 50), and close to anthesis the trichomes completely obscure the outline of the ovary (Fig. 53). Tetraberlinia tubmanniana conforms to the type of organ reduction in Fig. 1b, with four petals reduced in size but no reduction among the ten functional stamens.
Berlinia grandiflora (Vahl.) Hutch. & Dalziel
This species is similar to Tetraberlinia in its floral ontogeny so is not illustrated. The genus Berlinia sensu lato Hutchinson includes 15 tree species from tropical Africa (Cowan and Polhill, 1981b
) and is in the Berlinia group. The genus is being monographed by Mackinder (2000)
, who divides it into two groups based in part on petal number (one vs. five).
Berlinia grandiflora is a small tree 4–10 m high. It has racemose, helically arranged inflorescences with coriaceous, caducous bracts; the bracteoles are large, green, glaucous outside, enclosing the floral buds, then spreading and persistent in flower. The large showy zygomorphic flowers have five sepals that are thin, imbricate, pale green outside, and cream-white inside. The five petals include a large standard petal (6–7 cm long), white with a yellow spot at center, clawed with a broadly circular limb, and two to four small linear white petals. Nine stamens are attached to a short filament tube at base that is open adaxially, and the adaxial median stamen is free. The stamens have elongate white filaments and uniform oblong dorsifixed anthers. The stipitate ovary is adnate to the elongate hypanthium (Thompson, 1924
; Hutchinson, 1964
; Cowan and Polhill, 1981b
). Berlinia grandiflora is interesting in having synchronous early floral bud development in its racemose, few-flowered inflorescences. Order of organ initiation is helical among sepals, unidirectional among stamens, with each whorl starting on the abaxial side. An exception in one flower had the first stamen primordia lateral in the outer whorl, quickly followed by the abaxial median stamen that is usually the first in that whorl. Late stages of floral development were not available.
One large petal; seven large stamens (Afzelia) (Figs. 57–88)
Afzelia quanzensis Welw. is in the Hymenostegia group (Cowan and Polhill, 1981a
) and includes 13 to about 30 species of trees of tropical southeast Asia, tropical Africa, South Africa, and Madagascar. The flowers are in few-flowered terminal panicles or racemes (Léonard, 1952
). The tomentose, ciliate-margined bracteoles are ovate, concave, valvate, and subpersistent. They enclose the floral buds to a length of about 4 mm. They separate as the bud enlarges, and the sepals become protective. The flowers (Fig. 57a) are large (about 5–6 cm high), zygomorphic, with four elliptic or obovate imbricate sepals, the outer two of which are largest and are the only ones visible externally in bud. There is one large petal (Fig. 57a and d), clawed, bilobate, and unguiculate, red, 2–4 cm long and 2–3 cm wide, while the other petals are rudimentary or absent. There are seven functional stamens (Fig. 57a, c, and d) in A. quanzensis, with elongate declinate filaments and ovoid anthers, plus two staminodes in our material (Fig. 57c). Léonard (1952)
reported seven free fertile stamens in A. quanzensis plus two filiform staminodes, so there is some variation as to the number and degree of stamen suppression. The filaments are long exserted, and the anthers are small, oblong, and dorsifixed with longitudinal dehiscence (Fig. 57a). The gynoecium has a stipitate pubescent ovary, elongate style, and a small truncate subcapitate stigma; the gynoecial stipe is laterally adnate to the elongate hypanthium (Fig. 57b; Thompson, 1924
; Léonard, 1952
; Hutchinson, 1964
; Cowan and Polhill, 1981a
).
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Fig. 57. Drawings and floral diagrams of Afzelia quanzensis. (a) Open flower. (b) Bud in longitudinal section showing gynoecium attached to one side of hypanthium. (c) Bud with perianth removed to show three stamen rudiments (Ar and arrowheads). (d) Floral diagram. Scale bar = 10 mm in (a); scale bar = 5 mm in (b); scale bar = 3 mm in (c)
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Afzelia quanzensis, organogenesis
The inflorescence apical meristem initiates bracts and their subtended floral buds in acropetal, helical succession (Fig. 58). Each floral apex is at first tangentially wide and radially narrow (Fig. 59) before it initiates paired bracteoles laterally (Fig. 60). The massive bracteole bases nearly surround the floral apex (Fig. 61), which is narrow, tapered, and truncate both abaxially and adaxially (Fig. 61). Sepal initiation is in a modified helical order. The first sepal is initiated abaxially and medianly (Figs. 61 and 62) and the second and third adaxially (Figs. 62–64). The two lateral sepals are initiated last (Fig. 65). The shape of the post-sepal floral apex is broader than high, primarily because of the large size of the abaxial and adaxial sepals. Petal initiation is simultaneous (Figs. 66 and 67). The carpel is initiated concurrently with the petals (Figs. 66 and 67).
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Figs. 58–76. Afzelia quanzensis. Floral organogenesis (scanning electron micrographs). Abaxial side is at base in Figs. 59–69 and 71
; adaxial side is at base in Figs. 72 and 74–75
. Subtending bracts have been removed in all, bracteoles removed in Figs. 58 and 62–76
, and some or all sepals removed in Figs. 65–76
. Scale bar = 50 µm in Figs. 59 and 60
; scale bar = 100 µm in Figs. 61–73
; scale bar = 200 µm in Figs. 58 and 74–76
. 58. Polar view of inflorescence tip. 59–60. Initiation of two opposite bracteoles. 61. Bracteoles enlarging to cover floral apex. 62–63. Polar and oblique views of initiation of first sepal primordium nonmedianly on abaxial side of low-convex floral apex. 64. Second and third sepal primordia are initiating on adaxial side. 65. Polar view of floral apex with last two sepal primordia (at arrowheads) initiated in lateral positions. Two adaxial sepal primordia are becoming laterally confluent. 66–67. Polar and lateral views of floral bud with five petal primordia (at arrowheads) and carpel primordium initiated. 68. Near-polar view of floral bud with five antesepalous stamen primordia initiated; the three more abaxial are larger than the adaxial two. 69–70. Polar and abaxial side views. In Fig. 69
, three antepetalous stamen primordia have initiated (at arrowheads), the two abaxial first and a lateral more recently. In Fig. 70
, the relative heights of the undifferentiated organ primordia can be seen. 71. Polar view at midstage, with all organs initiated. An adaxial carpel cleft has formed. 72–73. Adaxial and lateral side views, showing petal primordia becoming laminar. Of the five antesepalous (outer) stamen primordia, the three more abaxial are larger than the two adaxial. 74–76. Two adaxial views and oblique lateral view. In Fig. 74
, the five petal primordia differ in height and arch inward. In Figs. 75 and 76
, the adaxial petal is removed to show the two suppressed antesepalous stamen primordia (at arrowheads), and one of the four antepetalous stamen primordia, still undifferentiated. In Fig. 76
, two of the three large antesepalous stamens have started to enlarge distally as the potential anther
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Nine stamens are initiated in two successive whorls; the outer has five, the inner four, lacking the adaxial member. Although no early initiation stages were found for the outer antesepalous whorl, the order is probably unidirectional, based on the fact that the abaxial and two lateral members exceed the two adaxial members in size when all have been initiated (Fig. 68). This size differential continues through subsequent stages of primordial enlargement. Order of initiation of the innerwhorl antepetalous stamen primordia is also unidirectional. Abaxial sites of the first two innerwhorl stamens are visible before sites can be discerned for the lateral pair of the whorl (Fig. 68, at arrowheads). In Fig. 69, the two abaxial innerwhorl stamen primordia are larger than the two lateral members of the same whorl. In slightly older buds, the four innerwhorl stamen primordia appear equalized in size and thereafter remain approximately the same size through development.
Afzelia quanzensis, organ development
The sepals become relatively thick, with the abaxial and two adaxial ones elongating more than the lateral two (Fig. 66). These lateral sepals (Fig. 70) remain the smallest through midstage. The two adaxial sepals become laterally confluent so that the calyx appears tetramerous (Fig. 57a and d).
The five petal primordia are initially equal in size and shape (Fig. 71), but at midstage the median adaxial petal (vexillary petal) grows marginally (Figs. 74 and 79), more so than the other four. In Fig. 80 the vexillary petal, 0.5 mm in height, is incurved marginally; the much narrower and shorter lateral petals (Fig. 79) are not touching. With further enlargement, a claw and a large enveloping limb become visible (Figs. 81, 83, 84, and 86) in the vexillary petal. The other four petals do not enlarge further but persist as rudiments (Figs. 86 and 87 at arrowheads).
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Figs. 77–88. Afzelia quanzensis. Floral organ development (scanning electron micrographs). Sepals removed in all, as well as other organs selectively removed to reveal inner structure. Scale bar = 250 µm in Figs. 77 and 78
; scale bar = 300 µm in Figs. 79, 80, and 85
; scale bar = 500 µm in Fig. 81
; scale bar = 1 mm in Figs. 82–84 and 86–88
. 77–78. Oblique and adaxial views of floral bud with large adaxial petal removed. Three large antesepalous stamens (A) are developing microsporangia and filaments are dorsifixed. Inner antepetalous anthers (a) also are differentiating microsporangia. Arrowheads indicate suppressed antesepalous stamen primordia. 79–80. Side views showing adaxial or vexillary petal twice the size of the other four. The three large antesepalous stamens (A) have differentiated anthers and filaments. 81–82. Polar views of large floral bud, with calyx removed and showing the three large functional stamens. In Fig. 81
the large adaxial petal envelops half the circumference, and in Fig. 82
, the petal is removed to show the coiled style and two of the inner, antepetalous stamen anthers. 83–84. Adaxial and lateral side views of floral bud, calyx removed. The large adaxial petal now has an expanding limb and a broad claw at base. 85. Gynoecium with glabrous ovary and coiled style in large bud. 86–88. Side views of large buds just before anthesis, showing the three largest antesepalous stamens and four slightly smaller but also functional antepetalous stamens. The young flower in Fig. 86
has the large adaxial petal plus two of the four petal rudiments (at arrowheads). Petal rudiments also are indicated in Figs. 87 and 88
. In Fig. 88
, some organs have been removed to show the gynoecium with glabrous ovary and coiled style
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Seven of the nine stamens become functional. They are in two alternating whorls; the outer antesepalous members differentiate before the inner antepetalous ones. In the outer stamen whorl, the order of initiation is unidirectional. The median abaxial and the two lateral primordia exceed the two adaxial in size at every stage. At midstage, the difference in height is about 165 µm for the three larger, about 90 µm for the two smaller (Figs. 72 and 73). The larger stamen primordia enlarge distally to begin anther formation (Figs. 75 and 76), and filaments appear basifixed. Later the stamens arch inward (Fig. 77), and anthers become dorsifixed by differential growth (Figs. 79 and 80). The three large outer stamens have their anthers closely appressed against the developing carpel in stages shown, so the microsporangia, delimited by the median dorsal and lateral grooves, are difficult to see (Fig. 78). The other two antesepalous stamen primordia remain small undifferentiated pegs (Figs. 75 and 76, at arrowheads) on either side of the vexillar petal during subsequent development. Differentiation of the four functional innerwhorl stamen primordia is not shown, but their differentiation is similar to that of the three functional outerwhorl stamens, except that the filaments remain short until just before anthesis, when all are alike (Fig. 57a).
The carpel develops a cleft at a height of about 220 µm (Figs. 71 and 72). The margins remain appressed during subsequent enlargement (Figs. 75 and 76). With enlargement, a laterally compressed glabrous ovary and an elongate coiled style develop (Figs. 57a, 82, 85, and 88). Differential growth in late stage reorients the gynoecium to the adaxial side of the short hypanthium (Fig. 57b). The flower of Afzelia quanzensis corresponds to the type of organ reduction in Fig. 1c, with the corolla reduced to one petal and the androecium somewhat reduced, with seven functional stamens.
One large petal; three large stamens (Gilbertiodendron, Macrolobium, and Paramacrolobium)
Gilbertiodendron (Figs. 89–122)
Two species were studied; the early stages are similar, so are shown for only one species. Some older stages are present in one but not available in the other. The genus includes 26 tree species of tropical Africa and is in the Macrolobium group. Inflorescences in the genus are paniculate to racemose, axillary, terminal, or on old wood. Small helically arranged bracts subtend individual flowers.
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Fig. 89. Drawings and floral diagrams of Gilbertiodendron brachystegioides and G. klainei. (a) Open flower with a showy vexillary petal, four linear petals and five linear sepals, three functional stamens, two staminodia, and gynoecium. (b) Floral bud, with one bracteole removed, showing linear sepals and part of the vexillary petal. (c) Bud with perianth removed showing three large stamens and gynoecium. (d) Intact floral bud enclosed in bracteoles. (e) Floral diagram. Scale bar = 2 mm in (a) and (d); scale bar = 1 mm in (b); scale bar = 0.5 mm in (c)
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Gilbertiodendron klainei (Pierre ex Pellegr.) J. Léonard and G. brachystegioides (Harms) J. Léonard are large forest tree species. In the latter the large petal is white, gradually turning brown; the anthers are greenish black with white filaments, and the ovary is green. Flowers are slightly fragrant to fetid. Both species have helically arranged bract-subtended flowers in racemes and paired indurate bracteoles enveloping the bud (Fig. 89b and d) through a height of about 7–8 mm high. The flower is zygomorphic and has five equal narrowly tapered scarious sepals, slightly imbricate in bud (Fig. 89a and e). The five petals include one larger, fanlike, and clawed (Fig. 89a and b); the other four are equal, strap-shaped, and similar to the sepals. The three large stamens (Fig. 89a, c, and e) have dorsifixed anthers with longitudinal dehiscence and filaments attached on a short fleshy tube. A few of the other stamens may persist as rudiments at anthesis (Fig. 89a). The ovary is shortly stipitate, adnate to one side of the receptacle. The stigma is capitate, and the style is coiled in bud (Fig. 89a and c). The two species are alike in inflorescence structure and flower structure except in color. Bracteoles of G. klainei are pale pink inside, purplish to brownish red outside. The flower (Fig. 89a) has five sepals, four small white petals, and one large yellowish white to gold petal. Stamen filaments are white, anthers are pale brown with creamy white slits. The style is white, and the stigma is wine red. Flowers are fragrant at night (Wieringa, 1999
, and label data by Wieringa; see Table 1).
Gilbertiodendron klainei, organogenesis
The sequence and stages are similar in the two species with minor differences, so only G. klainei is described and illustrated. The apical meristem of the inflorescence initiates bract primordia in helical acropetal succession (Fig. 90). A floral apex, wide tangentially and narrow radially, initiates in each bract axil. Paired bracteoles are initiated by the floral apex in rapid succession (Fig. 91) and grow rapidly to surround the floral apex before and during floral organogenesis (Fig. 98). The postbracteole floral apex is narrow and tapered adaxially and abaxially, although the abaxial side of the apex is usually truncate (Fig. 92).
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Figs. 90–104. Gilbertiodendron klainei. Floral organogenesis (scanning electron micrographs). Abaxial side is at base of figure in all except Figs. 101 and 104
. Subtending bracts have been removed in all, bracteoles removed in Figs. 92–104
, and all sepals removed in Figs. 102–104
. Scale bar = 50 µm in Figs. 91–94
; scale bar = 100 µm in Figs. 90 and 95–104
. 90. Lateral view of inflorescence apex (at arrowhead) initiating floral bract primordia and helically arranged floral buds, bracts removed. 91. Floral apex after initiation of two bracteoles. 92. "Omega"-shaped floral apex after bracteole initiation. 93. Initiation of first sepal primordium on abaxial side. 94–95. Oblique and polar views of floral bud. At least four petal primordia (at arrowheads) and the carpel primordium have been initiated. 96. The five sepal primordia are numbered in the helical order of their initiation. All five petal primordia have been initiated (at arrowheads) and the carpel mound is now convex. 97–99. Polar and oblique views of a floral bud. The floral meristem has expanded so that there are larger spaces between petal primordia. One antesepalous stamen primordium is shown initiating in lateral position (at arrowhead in Fig. 99
); the median abaxial outerwhorl stamen site is obscured by a sepal primordium. 100–101. Sepal primordia are starting to enlarge and arch inward. The two lateral antesepalous stamen primordia are initiated (at arrowheads). In Fig. 101
the carpel primordium is in a small depression, the start of the hypanthium. 102. Polar view of floral bud with sepals, carpel, and some other organs removed to show the five outer antesepalous stamen primordia (the three more abaxial being larger), and four inner antepetalous stamen primordia recently initiated and equal in size. 103. Polar view of floral bud showing carpel cleft beginning. 104. Side view of floral bud at midstage with all organs initiated but before differentiation begins
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Sepal initiation is successive in a 2/5 quincuncial helix. The first sepal primordium is initiated on the abaxial side, nonmedianly (Fig. 93). The second sepal primordium is initiated nonmedianly on the adaxial side (Fig. 94), and the third and fourth are lateral (Figs. 95 and 96). The fifth sepal primordium is adaxial and nonmedian (Fig. 96). The sepal primordia become marginally confluent to form a shallowly lobed calyx tube (Figs. 97, 99, and 100).
Petal initiation is unidirectional, with the first four appearing simultaneously (Figs. 94–96) and the adaxial petal lagging in time of initiation. The five petal primordia remain small and uniform in size through midstage (Figs. 100 and 101). The carpel is initiated concurrently with petal initiation (Figs. 94 and 95).
The order of initiation in each of the two whorls of stamens is presumed to be unidirectional. The first outerwhorl stamen primordium, median on the abaxial side, was obscured by a sepal in all preparations, but is assumed to have initiated first on the basis of its relative size in Fig. 102. The laterals are initiated next (Figs. 98 and 99 at arrowhead for one lateral primordium and Fig. 100 for both laterals). The two adaxials are formed last (Fig. 102). The order among the inner antepetalous stamen primordia is presumed to be unidirectional from the abaxial side, based on the abaxial sites being slightly larger than the others in early stages (Figs. 100 and 101). The inner stamen primordia rapidly become equalized in size shortly after their initiation (Figs. 102 and 103). No overlap was observed in time of initiation between whorls.
Gilbertiodendron klainei, organ development
The bracteoles become massive and surround the developing floral bud during early organogenesis (Fig. 98). They ensheathe the floral bud throughout development (Fig. 89b and d). The sepals form a calyx cup with five lobes (Fig. 101); the two adaxial sepals do not become confluent, as in many other Detarieae. The sepals become linear-lanceolate (Fig. 119) in large bud. At anthesis, the sepals are linear, acutely tipped, relatively thin and membranous, and are flared outward (Fig. 89a).
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Figs. 105–122. Gilbertiodendron klainei (105–121) and Gilbertiodendron brachystegioides (122). Floral organ development (scanning electron micrographs). Sepals removed in all except Figs. 113 and 119
, as well as other organs selectively removed to reveal inner structure. Scale bar = 100 µm in Fig. 110
; scale bar = 200 µm in Figs. 105–109 and 111–113
; scale bar = 500 µm in Figs. 114–116
; scale bar = 1 mm in Figs. 117–122
. 105. Polar view of floral bud with all petals expanding and open carpel cleft. Three of the antesepalous stamen primordia (the three most abaxial) exceed the other two in size. 106–107. Abaxial and adaxial side views of floral bud showing petal primordia elongating and tapered. In Fig. 107
the contrast can be seen between the enlarged antesepalous stamens (lateral) and the two adaxial members of that whorl. One of the antepetalous inner stamen primordia is visible and even smaller (at arrowhead). The carpel, about 335 µm high, shows ovules initiating between the gaping margins. 108. Carpel about 520 µm high, showing open margins and ovules initiating within. 109. Side view of floral bud, carpel removed, showing the three larger antesepalous stamen primordia (A) with anthers forming; the smaller stamen primordia include two antesepalous (A) and three of the five antepetalous (a) primordia. 110. Antesepalous anther differentiating microsporangia with median adaxial groove (at arrow) and lateral grooves (at arrowheads). Tapered petal primordia and undifferentiated stamen primordia of both whorls are also visible. 111. Side view of carpel about 640 µm high and a large antesepalous stamen anther. 112. Polar view of receptacle with most organs removed including gynoecium, except suppressed stamen primordia of antesepalous (A) and antepetalous (a) whorls on the adaxial side. All the stamens are attached to a raised ridge around the sunken carpel base. 113. A stamen anther, adaxial side, showing the microsporangia delimited by a median groove (arrow) and lateral grooves (arrowheads). Two petals and parts of sepals also are present. 114. Adaxial lateral view of corolla around gynoecium. 115. Side view showing two of the three large antesepalous stamens visible, with dorsifixed anthers and gynoecium with reflexed style. Petals differ greatly in size. 116. Lateral view of carpel about 800 µm high, with sealed margins and forming a style. 117. Polar view of large bud with sepals removed and the coiled bare style visible above the hairy ovary. The adaxial vexillary petal envelops much of the bud, and the four narrow petals and a large stamen are visible. 118. Large flower bud in polar view, with vexillary petal surrounding most of the circumference. 119–121. Side views of large buds just before anthesis. 119. Abaxial side, showing one sepal, both sides of the vexillary petal, and stamens. 120. Adaxial side with large vexillary petal visible. 121. Abaxial side, showing two narrow petals arched around one of the large stamens. 122. Gilbertiodendron brachystegioides. Adaxial view showing the three large stamens and the gynoecium
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The five petal primordia are attached in the sinuses between the lobes (Figs. 100 and 101). Four of the five (the lateral and abaxial pairs) remain similar in size at midstage (Figs. 102–104). The vexillary petal (which later enlarges greatly) is shorter and broader than the others during development in G. brachystegioides, while in G. klainei it enlarges precociously before the others (Fig. 105). The petal primordia become tapered distally (Figs. 106 and 107). Three larger petals are seen in Figs. 114 and 115. At anthesis the vexillary petal is much larger than the others, fan-like with two lateral lobes and clawed (Figs. 117, 118, and 120). The four other petals are small in both, linear–lanceolate, and similar to the sepals in G. klainei (Figs. 89a, 117, and 121), and scalelike in G. brachystegioides.
Of the ten stamens initiated, only three become large and functional. These three are the lateral and abaxial median members of the outer, antesepalous whorl, which begin to enlarge precociously during midstage (Figs. 102 and 104). The strong variation in size among stamen primordia of the outer whorl is visible in Figs. 105 and 107. In Fig. 112, most organs are removed, showing the stamen rudiments; two (A) are in the outer antesepalous whorl and one (a) is in the inner antepetalous whorl. Stamen differentiation proceeds first in the members of the outer whorl and then in the inner whorl. Each stamen primordium enlarges distally to form the anther (Fig. 109), followed by formation of the microsporangia, delimited by a median adaxial groove and lateral grooves (Figs. 110 and 113). The anthers are basifixed early in their differentiation (Figs. 109 and 110), but become dorsifixed in late stage (Figs. 115 and 121) by differential growth. In bud (Fig. 122), only the three large stamens can be seen. The filaments elongate rapidly at anthesis so that the three large stamens become exserted. The six others remain small or reduced (Fig. 89e). All of the stamens, functional and reduced, are attached on a short, fleshy tube; earlier reports held that only the innerwhorl stamens were on a tube (Cowan and Polhill, 1981b
; Bruneau et al., 2000
).
The carpel primordium develops a cleft (Fig. 103) at the same time that the last whorl of stamens is initiated. With height increase, the carpellary margins expand in area. The margins are gaping and unfused during the start of ovule initiation at a carpel height of about 340–520 µm in G. klainei (Figs. 105–108), but they are appressed and then fused at this stage in G. brachystegioides (not shown). The margins become appressed and sealed by a height of about 640 µm (Fig. 111). The carpel becomes tapered and a style develops (Fig. 116) by a height of about 800 µm. The style is coiled in bud (Fig. 89c). Sparse trichomes develop on the adaxial and lateral sides of the carpel (Figs. 89a and 122). The gynoecium base is in a depressed pit in late stages (Fig. 112). The flowers of Gilbertiodendron species exemplify the high degree of organ reduction diagrammed in Fig. 1d, with four of the five petals and seven of the ten stamens reduced.
Paramacrolobium coeruleum
This tropical tree genus is monotypic and is native to tropical West Africa. Its floral development is essentially similar to that of Gilbertiodendron brachystegioides so is not illustrated. The inflorescences are compact distichous corymbs with acute, glabrous floral bracts subtending flowers in two vertical rows. Order of flower enlargement in an inflorescence is unusual in that the uppermost lateral floral bud enlarges before those lower down in the inflorescence. The paired bracteoles are thick, fleshy, glabrous, elongate, valvate, fused, and persistent; they enclose the floral buds from the time the latter are extremely minute through the time of anthesis. The flowers have two persistent bracteoles, zygomorphic symmetry, four (rarely five) sepals (the adaxial one bifid and wider than the rest), and a short calyx tube. They have five petals, including one large petal and four rudiments, three functional stamens, 4–5 staminodia, and a stipitate gynoecium with capitate stigma. Hutchinson (1964)
says the nine stamens are fused basally, with 3–5 fertile and exserted, 4–6 small and staminodial. The gynoecium is attached to one side of the hypanthial tube.
Developmentally, Paramacrolobium coeruleum has a postbracteole floral apex that is elongate sagittally and narrow tangentially, although it is more circular than in most other "Omega"-type taxa. The bracteoles enlarge and enclose the floral bud early and completely. Organ initiation is helical among sepals (with the first abaxial and nonmedian), unidirectional among petals and antesepalous outer stamens, all starting on the abaxial side first. The carpel initiates concurrently with the petals. No initiation stages were observed of the antepetalous stamens. Three antesepalous stamens (the abaxial and two laterals) exceed the rest in size by midstage and maintain this advantage throughout development. They become the functional stamens; the rest become staminodia.
Macrolobium acaciifolium Benth. and M. crassifolium (Baillon) Léonard
Macrolobium includes 130+ species of trees, lianas, and large shrubs from tropical America and Africa. The inflorescence of M. crassifolium has bracts and subtended flowers helically arranged. The valvate, sepaloid, persistent bracteoles enclose the buds. Flowers are small, zygomorphic, and have four imbricate sepals (the adaxial two confluent). One petal is larger than the rest and orbicular, while the other petals are rudimentary. Three large fertile stamens have filiform filaments, dorsifixed versatile anthers, and longitudinal dehiscence; the other stamens are reduced as staminodia or are absent. The stigma is terminal, the style is filiform, and the ovary is short stipitate and laterally attached (Thompson, 1924
; Léonard, 1952
; Hutchinson, 1964
; personal observations). The genus is in the Macrolobium group (Cowan and Polhill, 1981b
) and is characterized by having racemose inflorescences, one large petal and 1–4 minute rudiments, three large stamens plus reduced staminodes, all stamens free and in one whorl, and an exserted stipitate gynoecium (Thompson, 1924
; Cowan and Polhill, 1981b
).
Organogenesis and development of Macrolobium species are very similar to those of species of Gilbertiodendron just described. The floral apex of M. crassifolium is the "Omega"-type at bracteole initiation, and the massive bracteoles enclose the floral bud early in development. Organogenesis is helical among five sepals and unidirectional in the petal and stamen whorls, all starting on the abaxial side. The carpel is initiated concurrently with the first-initiated antesepalous stamens. Three antesepalous stamen primordia (the median abaxial and the two laterals) are disproportionately large by midstage; these later become the functional stamens. The vexillary petal remains small until late in development in species of Macrolobium, as in Gilbertiodendron.
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DISCUSSION
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Order of organ initiation
All taxa studied here have an "Omega"-shaped floral apex after bracteole initiation, bracteoles large when initiated, helical sepal initiation, unidirectional petal initiation (except simultaneous in Afzelia and not determinable in Tetraberlinia), and unidirectional stamen initiation in both whorls. Five petals are initiated in all; suppression begins in late development. Either two petals (Neochevalierodendron, Phyllocarpus) or four petals (Afzelia, Berlinia, Macrolobium, Tetraberlinia) are suppressed. All ten stamens are initiated; at midstage, suppression begins in either three stamens (Afzelia) or seven stamens (Gilbertiodendron, Macrolobium, Paramacrolobium).
Shared character states
The taxa studied here have most of the same assemblage of early-ontogeny character states that were reported in the Brachystegia group of Detarieae (the "A" or "Omega"-type in Tucker, 2000a
). They have the "Omega"-type floral apex after bracteole initiation, precociously enlarged bracteoles just after initiation that encircle 90% of the circumference of the postbracteole floral apex, which tends to be tapered adaxially and abaxially. The character states that they share with the "circular apex" or "B" type group (Amherstia, Cynometra, Schotia, Tamarindus, Crudia, etc.; Tucker, 2000d
, 2001a
, b
) include helical initiation of sepals in most, complete calyx and corolla initiated, and no ring meristem (see following paragraph), which are probably plesiomorphic character traits. Zygomorphy and a reduced number of organs are the character traits distinguishing the present taxa from those Detarieae covered in a previous paper (Tucker, 2002
). The flowers of the present taxa are strongly zygomorphic at anthesis. This zygomorphy is primarily expressed as one petal much larger than the others and by suppression of several of the stamens: three stamens suppressed in Afzelia or seven stamens suppressed in Gilbertiodendron, Macrolobium, and Paramacrolobium.
Ring meristem
In a few detarioid taxa, the floral meristem forms a continuous raised ring around the center of the apex; organ primordia are initiated upon this ring. No ring meristems occur in any of the species included here. Tetraberlinia tubmanniana might have been expected to have one in view of its relationship as sister group to the Aphanocalyx/Bikinia clade in the phylogenetic analysis by Wieringa (1999)
. A ring meristem has been found in Monopetalanthus durandii (Bikinia durandii), Aphanocalyx djumaensis (both in the group studied by Wieringa) and two species of Brachystegia (Tucker, 2000a
), and Microberlinia bisulcata (Tucker, 2002
). The ring meristem innovation was suggested as a possible defining character for the Brachystegia group (Tucker, 2000a
) that includes these taxa except for M. bisulcata.
Effect on organogeny of suppressed vs. lost organs
Many of the taxa studied here have reduced numbers of floral organs (petals and stamens as diagrammed in Fig. 1a–d) at anthesis. However, in all, the full complement of organs is initiated in each whorl, and the reduced organ number is due to suppression after initiation. The "missing" organs can be seen to initiate, and rudiments are usually detectable even at anthesis. The contrasting effect on subsequent organogeny between organs that initiate and those that fail to initiate has been emphasized by Tucker (1988a
, b
, 2000c
).
Systematic relationships
Taxonomic relationships among genera of Detarieae continue to be unclear and confusing. The molecular- and morphology-based analyses by Bruneau et al. (2000
, 2001
) found none of the ten generic groups of Polhill (1994
, based on a smaller group proposed by Léonard, 1957
) to be monophyletic. Molecular data (Bruneau et al., 2000
, 2001
) indicate that Detarieae as a whole (including Macrolobieae) is monophyletic. The tribe Macrolobieae sensu Bruneau et al. (2000)
, after Amherstia, Humboldtia, Macrolobium, and Tamarindus are removed, is monophyletic and is derived from Detarieae s. str., but the Macrolobieae of Breteler (1995
; Breteler and Wieringa, 1999
), which includes the latter genera, is not monophyletic.
Three clades (A, B, C) were designated by Bruneau et al. (2000)
within Detarieae sensu lato. Their Clade C comprises the reconstituted tribe Macrolobieae and includes three taxa in the present paper: Berlinia, Gilbertiodendron, and Tetraberlinia</
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ABSTRACT
INTRODUCTION
