| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
0 Department of Biology (Ecology, Evolution, and Marine Biology), University of California, Santa Barbara, Santa Barbara, California 93106 USA; and Department of Biology, Louisiana State University, Baton Rouge, Louisiana 70803 USA
Received for publication September 16, 1999. Accepted for publication January 3, 2000.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: Amherstia • Brownea • Caesalpinioideae • Detarieae • development • Fabaceae • flower • Leguminosae: ontogeny • Tamarindus.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). In a search for unifying character states to characterize the tribe, floral organ initiation and development are being compared across representative taxa in the caesalpinioid tribe Detarieae s. l. This second paper in the series (see Tucker, 2000
, on the Brachystegia group) examines three taxa having a simple caesalpinioid flower type with all 21 organs initiated (five sepals, five petals, ten stamens in two whorls, and one carpel): species of Amherstia, Brownea, and Tamarindus. Amherstia and Brownea have large, showy flowers. Developmentally, these three taxa share certain significant character states: a circular pre-petal floral apex, helical (2/5 quincuncial) order of sepal initiation, and median abaxial initiation of the first sepal. Generic differences include suppression of certain floral organs in some, and elaborations in floral structure due to developmental timing in others. Missing floral organs are a feature of many other legume flowers (Tucker, 1988b
). No close systematic relationship within Detarieae is evident among these three genera; they belong to two different detarioid "groups" as designated by Léonard (1957)
. The aim of the work was to determine the developmental bases for similarities and differences among the three taxa.
The useful literature on floral structure and development in Detarieae includes Baillon (1872)
, Hutchinson (1964)
, and Thompson (l924)
for general floral descriptions. Hartog's (1888)
paper detailed the floral ontogeny of Brownea in considerable detail for its time, although differing in some significant ways from the present description. Floral morphology and pollen of Brownea were described by Klitgaard (1991)
, and some preliminary work on floral ontogeny was reported previously (Tucker, 1997
).
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Material of Tamarindus indica was processed from the spirit collection from the Royal Botanic Gardens, Kew, originally from Mwanza District, Tanganyika (R. Tanner 333; Kew 15508; Tucker 26935) and from National Botanic Gardens, Harare, Zimbabwe (B. Browning, I. Muronganwa, and S. Kativu 36, collections in 1987 and 1988; Tucker 28148, 28735, 28736). Other material of T. indica used for comparison was collected at Fairchild Tropical Garden, Miami, Florida (Tucker 25175); Waimea Arboretum, Oahu, Hawaii (Ann Bruneau 921; Tucker 32282), and Yucatan, Mexico (J. Ramírez-Domenech, 1987; Tucker 28062). All samples were transferred to glycerine—70% ethanol for storage.
Inflorescences and flower buds of all sizes of Brownea latifolia, Amherstia nobilis, and Tamarindus indica were transferred to and dissected in 95% ethanol. Bracts and larger floral organs were removed from each piece under a dissection microscope. After appropriate dissection, the pieces were further dehyrated through an ethanol-acetone series, critical point dried with CO2 in a Denton DCP-1 apparatus, and mounted on aluminum stubs with either colloidal graphite or carbon-conductive adhesive tabs (T. Pella Co., Redding, California, USA). They were coated with gold-palladium in an Edwards S-150 sputter-coater, and micrographs were taken with a Cambridge S-260 scanning electron microscope (SEM) at 25 kV in the Electron Microscope facility at Louisiana State University.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
25 species of small trees native to northern South America (Colombia and Venezuela in particular) and the West Indies. Brownea latifolia is a species with showy rose-red flowers in globose, terminal, few-flowered dense capitate racemes (Fig. 1a) that are cauliflorous on old wood. The flowers bloom nearly simultaneously in each inflorescence (Léonard, 1957
; Backer, 1963–1968
). Bracteoles form a short connate tube with two lobes, large and red in color; they enclose the calyx (Fig. 1a, e). The flowers have four petaloid imbricate sepals, five slightly unequal, imbricate clawed petals, 9–15 stamens, free or unequally connate (Fig. 1a, d, e; Baillon, 1872). The androecium in our material has 11 stamens with fused filaments forming an elongate tube (Fig. 1d). Hartog (1888)
said that B. coccinea usually has 11, B. grandiceps usually has nine, ten being a rare number in either species. The ovary is stipitate to the side of the hypanthium (Fig. 1c), with filiform style, capitate stigma, and numerous ovules. The hypanthium is turbinate-campanulate (Hutchinson, 1964
).
Brownea latifolia: Organogeny
The bracts and subtended floral buds of the inflorescence are initiated in acropetal order by the inflorescence apical meristem (Fig. 4). The phyllotaxy of the bracts is distichous at the base and helical distally. There are 20–30 flowers per raceme, and they are synchronous (Figs. 4, 11). This synchonicity, with all flower buds in an inflorescence being at the same stage, is unique among caesalpinioid flowers examined to date. It is achieved by floral apices remaining at a pre-bracteole stage until all flowers in the inflorescence have been initiated. At that time, all flowers undergo bracteole organogeny synchronously (Fig. 4). The flowers in an inflorescence continue organogeny together; one with all flowers undergoing sepal initiation is shown in Fig. 11.
|
Petals also arise helically, although so closely in time that finding all stages is difficult. A flower with the first two petal primordia is seen in Fig. 10 (at the 5- and l0-o'clock positions). Another with four petal primordia is seen in Fig. 12. The two largest are at arrowheads, showing a helical order continuous with that of the sepals. The vexillary petal appears later (at arrowhead, Fig. 13). Petal positions alternate with those of the sepals, but typically petals are not equidistant at initiation. As usual in a helical phyllotaxy, the largest petal primordia are not adjacent to each other (Fig. 12). Once all are initiated, the petals become quickly equalized in size and equidistant (Figs. 13–15).
The carpel primordium next forms as a central mound (Fig. 14) and enlarges as a hemispherical mound until all organs complete initiation. It then becomes somewhat flattened adaxially (Fig. 24), and cleft formation begins adaxially at a height of 125 µm.
|
The first two antepetalous stamen primordia are initiated in abaxial positions (Figs. 19–21); in Fig. 22 a third member of this whorl has been initiated in a lateral site (arrow). The vexillary (median adaxial) stamen of the antepetalous whorl is the last to be initiated, represented by a pair in Fig. 23. The outer stamens remain small while the inner ones are initiated, so that the primordia are about equal in size in early stages. Initiation of primordia did not overlap between the outer and inner stamen whorls.
B. latifolia: Organ differentiation
Brownea is unique among caesalpinioid taxa examined to date in having synchronous floral development in the inflorescence, rather than successive development among its members. Although only two representative stages are shown (pre-bracteole in Fig. 4 and petal initiation in Fig. 11), development continues synchronously up to anthesis.
The paired bracteoles around each flower become massive, flat-topped, and fused early, with only a narrow slit between them over the floral summit (Fig. 7). They continue to enlarge and enclose the bud at all stages (Fig. 1a).
Although five sepals are initiated, the upper (adaxial) pair become laterally confluent (Fig. 14), so that the flower appears to have a four-parted imbricate calyx (Fig. 1b, e). The large, upper compound sepal is often associated with petal primordia that are not equidistant (Figs. 12–13). The sepals form a tube, which at anthesis is 20–25 mm long and encloses the proximal third of the flower (Fig. 1b, c).
Petal and stamen primordia grow as short cylinders at first and are tilted inward at midstage (Fig. 27). The vexillary petal is initiated late in many flowers and develops after the others (Fig. 20). The petal primordia begin to grow marginally and develop laminas (Figs. 25–26). Each becomes tapered at the base and flared distally (Figs. 1b, 27–28); at maturity the petals each have a frilly-margined ovate blade 20 mm long and a linear claw 15 mm long. The petals remain vertically oriented rather than reflexed; they are imbricately overlapping within the calyx tube (Fig. 1b). The petals are all essentially alike, so the flower appears radially symmetrical (Fig. 1b).
The outer (antesepalous) stamen primordia begin differentiation at a height of 145–200 µm (Fig. 27). The distal portion broadens to form the anther, and a cylindrical filament forms proximally. During development, the antesepalous (outer) stamens are uniformly larger than the inner (Fig. 27) and begin differentiation first. The stamen primordium (or primordia, if a pair forms) in the median antepetalous position is suppressed. Microsporangia become delimited adaxially in anthers of both whorls at about the same stage (Fig. 29). Stamens of both whorls have flaring filament bases (Fig. 29) during late developmental stages. In the open flower, the filaments become connate basally (Fig. 1d), due to intercalary growth below the levels of filament attachment to the receptacle. The filament tube is discontinuous adaxially, where the median antepetalous stamen is suppressed. The stamen anthers are long-exserted, tetrasporangiate, dorsifixed (Fig. 32), and have introrse longitudinal dehiscence. Size differences among stamens disappear in late bud stages (Figs. 1d, 32).
|
315 µm (Fig. 27), the margins have become appressed and confluent and the carpel is effectively sealed. The carpel grows straight and erect (Figs. 29–31). A hypanthium begins to form late in development (Figs. 29–31), so that the outer floral organs (sepals, petals, stamens) are attached to its rim. The gynoecium is attached to the adaxial side of the hypanthium (Fig. 1c) at anthesis. Vertical rows of trichomes (Fig. 32) are produced on the ovary. The style elongates and becomes revolute in late bud stage (Fig. 33), and unrolls at anthesis (Fig. 1c). In some flowers the carpel remains unusually small, and those flowers are probably functionally male (not shown).
Amherstia nobilis: Organography (Figs. 34–77)
These small unarmed trees are native to Burma (Cowan and Polhill, 1981b
), often cultivated in the tropics, have huge showy pink to rose-scarlet perfect flowers 9–15 cm long in large, few-flowered, pendulous, terminal racemes. There are large (5 cm long) colorful persistent bracteoles that cover the bud (Fig. 2b). The elongate hypanthium has four petaloid, imbricate sepals inserted at the top of the tube (Fig. 2a); the adaxial or upper is broader than the others. The five free petals include three large petals adaxially, including an obcordate vexillum (standard); each has a yellow blotch distally. The two lower petals are minute (Fig. 2c). There are ten stamens, diadelphous, with nine forming a filament tube (five longer with larger anthers, four shorter with smaller anthers; Fig. 2c, d). The anthers are introrse and dorsifixed. The ovary is stipitate, the stipe adnate adaxially (Fig. 2d) to the elongate hypanthium that is lined with a disk. The style is filiform and revolute (Fig. 2a) or straight (Garcia, 1975
) with a capitellate stigma, and 1–6 ovules (Baillon, 1872
; Hutchinson, 1964
). The flower is resupinate on its pedicel.
|
Petals are initiated in unidirectional order. The first two or three are initiated simultaneously (Fig. 42): two on the abaxial side plus one lateral (Fig. 42). The two laterals are next to be initiated, either synchronously or successively (one in Fig. 42; two lateral petals in Fig. 43). The median adaxial petal is initiated last (at arrowhead, Fig. 44). All five petal primordia appear to form closely in time (Fig. 44) before any begin to enlarge. The petal primordia in some flowers are unequally spaced.
Before the outer or antesepalous stamens are initiated, the floral receptacle first expands laterally so that there are noticeable spaces in antesepalous sites between the petal primordia (at arrowheads; compare Figs. 44 and 45). The outer stamen primordia are initiated in bidirectional order starting with the two laterals (at arrowheads, Figs. 45–46), followed by the median abaxial (Fig. 47). The laterals are usually slightly larger than the median one, directly after their initiation (Fig. 48). The last two antesepalous (outer) stamen primordia are initiated on the adaxial side (Fig. 49, at arrowheads). Petals, carpel, and outer stamen primordia enlarge while antepetalous spaces form for the inner stamens (Figs. 48–49). There is no overlap in time of initiation among the whorls of organs.
|
The carpel primordium becomes evident as a low central mound concurrently with the first-initiated antesepalous (outer) stamens (Figs. 45–46). The carpel begins to flatten adaxially when it is 100 µm in height (Figs. 51–52), after which a cleft forms at 250 µm height (Fig. 53).
Amherstia: Organ differentiation
The two bracteoles enlarge and completely cover the flower (Fig. 41). They are massive, sparsely hairy, thick-walled, and have a slit between them. They enlarge together with the rest of the bud, enclosing it (Fig. 2b) until just prior to anthesis. At 43 mm in length, the bracteoles form a long narrow tapered tube covered by strigose trichomes (Figs. 58–60). At anthesis, the bracteoles are as large as the sepals and petals, and reflex similarly, adding to the showy display.
|
1 mm, there is a calyx tube and free sepal lobes that overlap imbricately (Figs. 59–60). The lobes elongate greatly by the time that the flower is 570 µm high above the bracteoles and the bud is 7.2 mm high (Fig. 61). The sepals enclose the flower as the bud grows inside the bracteoles. At anthesis the sepals reflex and form part of the showy perianth (Fig. 2a).
The petals grow as cylindrical primordia at first (Fig. 49), then heighten and broaden marginally (Fig. 52), with acute tips (Fig. 57) at a height of 300 µm. Aestivation is imbricate, with the two laterals overlapping the others, and is completed at a petal height of 800 µm (Figs. 63–64). The pattern of imbrication differs from the order of initiation, which was unidirectional. A tuft of trichomes terminates each petal by a height of 800 µm or earlier. All of the petals become broadly ovate. The two lateral petals have ciliate distal margins and are larger than the other petals at this stage (Fig. 64). The median vexillar (standard) petal is somewhat smaller than the laterals (Figs. 69–70,72) in late stages, but at anthesis all three are equally long (Fig. 2a). The two abaxial petal rudiments remain minute (Figs. 2c, 69, 72). At anthesis, the three large petals expand and spread, forming the showy perianth together with the bracteoles and sepals (Fig. 2a).
The stamen primordia grow as undifferentiated cylinders (Fig. 50) to a height of 220 µm, when they become acute-tipped and begin to display heteromorphy. Three of the outer stamens (the abaxial median and two adjacent laterals) become much larger than the other two of their whorl (Figs. 55–56). At a height of 290 µm, the outer stamen primordia become broadly sagittate, appressed distally against the carpel, and tapered basally (Fig. 62). As anther formation begins, median and lateral furrows become visible at a stamen height of 250 µm (Fig. 68). A tuft of trichomes tops each anther (Figs. 68–70, 72). The anthers become tetrasporangiate (Fig. 71) and elongate greatly (0.3 mm long in Fig. 74). The developing filaments are dorsifixed from the first (Figs. 68–69) and relatively thick and sinuous close to the time of anthesis (Fig. 74). The filament tube (Figs. 74–75) develops late by zonal growth below the level of filament attachment and elevates all nine stamens on a tube (Fig. 2d).
|
40 µm high in Fig. 54. Formation of anther and filament begins at a height of 300 µm (Fig. 65). Next, the median and lateral furrows (Figs. 68–69) form, delimiting the microsporangia. The antepetalous stamens have smaller anthers and shorter filaments (Figs. 65–66) than the outer stamen whorl. At anthesis the antepetalous stamens are attached to the filament sheath (Figs. 2c, 74–75), alternating with the longer antesepalous stamens, which are the only fertile ones (Endress, 1994
). Occasionally a stamen is represented by a rudiment lacking an anther (Fig. 71).
When the carpel primordium is 260–315 µm high, the cleft is seen to end above a short basal pedestal (Fig. 54). The carpel heightens but the margins remain unfused while ovules begin initiation (Figs. 65–66) at a height of 760 µm. The margins become appressed at the base of the cleft by a carpel height of 346 µm, and appression is complete in Fig. 67. The carpel tip recurves adaxially at a height of 1.3–1.5 mm (Fig. 68). At 3 mm carpel height, the ovary becomes covered by strigose trichomes that continue up the style (Fig. 71). The latter becomes revolute more than 360° in bud (Figs. 2a, 73, 75–77). The stigma is narrow, capitate, and papillate (Figs. 73, 77).
The hypanthium starts by formation of a depression around the carpel base (Fig. 67). Stipe formation results by elongation of the basal pedestal noted earlier and is first evident at a carpel height of 1.2 mm (Figs. 67, 73). In the open flower the stipe is attached to the adaxial side of the hypanthial rim (Fig. 2d).
Tamarindus indica (Figs. 78–124): Organography
Tamarinds are small unarmed trees, widely cultivated but probably native to tropical Africa (Léonard, 1952
; Cowan and Polhill, 1981b
). They bear axillary or terminal racemes of deep yellow to pale gold flowers, each 1.5 cm long with red markings on the petals. The flowers (Fig. 3a) have similarly colored caducous bracts and bracteoles, the latter ovate-oblong and valvate. The hypanthium is narrowly turbinate (Fig. 3b, c), the calyx tube four-parted, the sepal lobes imbricate and membranous, the adaxial sepal lobe of which is broad and double. The corolla has five free petals, of which the upper, more adaxial three are equally long (11–13 mm) and the lower are minute (1–2 mm long; Fig. 3a, d). The median adaxial petal is overlapped by the laterals. The nine stamens include three (-five) large functional stamens, with filaments connate to half their length and dorsifixed introrse anthers (Fig. 3a–d) dehiscing longitudinally, and six minute staminodia (Fig. 3d) lining the rim of the hypanthium. There is a stipitate ovary, the stipe adnate adaxially to the elongate hypanthium (Fig. 3c), which is lined with a disk. The style is elongated, the stigma truncate, narrow, and subcapitate; ovules are 8–10 or more (Baillon, 1872
; Léonard, 1952
; Hutchinson, 1964
). Rarely, a flower is tetramerous (not shown) rather than pentamerous.
|
3–10 flowers each. Long, straight trichomes cover the axis and the abaxial sides of the bracts. Each floral apex first produces a pair of opposite bracteoles in lateral positions (Figs. 80–81). One may be developed slightly before the other. The remaining floral meristem expands in the sagittal plane (Fig. 81), at right angles to the plane bisecting the bracteoles. The first sepal forms abaxially and medianly (Fig. 82), the second adaxially and nonmedianly (Fig. 83), and the third laterally (Fig. 84). The fourth sepal is also lateral, and the fifth is adaxial and nonmedian (Fig. 85). All five are positioned along a 2/5 quincuncial helix that may be either clockwise (Fig. 87) or counterclockwise (Fig. 85). In early stages, the sepal primordia maintain their relative sizes correlated with their order of initiation (Fig. 85). The second and fifth (adjacent adaxially) usually become laterally confluent (Fig. 87), so that in later stages only four sepals or sepal bases are apparent. Most flowers have four sepal lobes, but there are five lobes in some flowers (not shown).
The five petals, alternating in position with the sepals, form in unidirectional order. The first one or two form abaxially and successively on either side of the first sepal (Figs. 86–87). The second pair form laterally and successively (only one present in Fig. 87), and the last petal (often delayed or sometimes absent) is median and adaxial (Fig. 88). The latter petal is broader and more blunt in shape than others at initiation. The four lateral petals have an initial size advantage over the adaxial one (Figs. 91–92).
The flower enlarges in diameter so that there are large but unequal spaces between the petal primordia (Figs. 88–89); the larger spaces are toward the abaxial side. At the same time as petal initiation, the carpel primordium becomes visible as a central mound (Figs. 87–88).
Although only three stamens are functional, nine are initiated (Fig. 3d). Stamens arise in unidirectional order in both whorls. The first three stamen primordia of the outer, antesepalous whorl appear simultaneously in abaxial and lateral positions (Fig. 89). The last two antesepalous stamens are initiated in adaxial positions, either simultaneously or in succession (one in Fig. 90, two in Fig. 91). Spaces form for the next set of stamen primordia internal to the abaxial petal primordia (Fig. 91).
Stamen primordia of the inner or antepetalous whorl are initiated alternately to the antesepalous ones in unidirectional order, starting with a pair on the abaxial side. Initiation is not shown, but where all four antepetalous stamen primordia (Fig. 92) are present, members of the abaxial pair are the larger. The four or five members of this whorl appear very closely in succession. There is no overlap of initiation among the different organ whorls.
Tamarindus: Organ differentiation
The bracteoles are thick with a dense marginal tomentum (Figs. 95, 99). They enclose the developing flower bud during its entire development. The four sepals (one of these a fusion product of two) arch inward to cover and enclose the rest of the flower (Figs. 94–95). In Fig. 95, five sepal lobes are evident, although the adaxial two are fused at their bases. The sepal primordia differ in size, reflecting their quincuncial helical order of initiation. In bud, the sepals are thick and have a dense marginal tomentum. The two outer sepals are larger and enclose the flower in late bud. In the open flower, the four sepal lobes are reflexed and appear similar to the petals (Fig. 3a).
|
90 µm, and become tilted inward (Fig. 97). When the petals are 400 µm high, their tips become acute (Fig. 103). The median adaxial and two adjacent lateral petals become much larger than the two abaxial ones (Fig. 105). The laterals and the median adaxial petal develop terminal tufts of trichomes (Figs. 105–106) at 500 µm high. The two abaxial petals remain rudimentary flaps (Figs. 105 and 119, at arrowheads), and even these have terminal trichome tufts (Fig. 119). At anthesis, the three large petals have frilled margins (Fig. 3a) and are tomentose on the adaxial side at the base (Figs. 114–115).
|
|
270 mm high. The lateral (actually introrse) grooves are visible at a height of 300 µm (arrowheads, Fig. 108). The microsporangia of the three larger stamens become clearly evident at a height of 430 µm (Fig. 111). The filaments at first are basifixed (Fig. 105) and then through differential growth of the anther base become dorsifixed (Fig. 110). The introrse lines of lateral dehiscence eventually are continuous across the summit of the anther (Fig. 111). The filaments are connate basally in a sheath formed by zonal growth below their level of attachment to the receptacle (Figs. 3b, 120). Mature anthers are seen in adaxial and abaxial views (Figs. 121–122). Their filaments are sinuously folded in large buds, but become straight or slightly curved at anthesis (Fig. 3a). The two more adaxial antesepalous (outer) stamen primordia remain rudiments (Figs. 100–102) from the stage of carpel-cleft formation. They are easily confused with the similar-sized antepetalous stamen rudiments (Figs. 107–110). In large buds (Fig. 113) the antesepalous stamen rudiments have terminal tufts of hairs, like the large stamens.
The four antepetalous (inner) stamen primordia remain as rudiments. They are still small pegs (Figs. 107–109) while the three large antesepalous stamens are forming microsporangia. The antepetalous stamen primordia enlarge very little beyond this primordial stage, appearing as short, digitate structures on the rim of the stamen sheath (Figs. 115, 119), alternating with the large antesepalous stamens and the two rudiments of that whorl. After zonal growth raises the three large fertile stamens upward on a filament tube (Fig. 3b), the inner (antepetalous) stamens remain as short flaps lacking anthers (Fig. 3c). The rudiments may be attached on the filament of a large stamen (Fig. 119), or directly on the filament tube (Figs. 115, 118). The filament tube or sheath forms via zonal growth below all stamen bases when the antesepalous stamens are 270 µm high and are starting to form anthers (Figs. 107, 109). The petals remain distinct from the filament tube.
The carpel primordium at first grows as a dome, then flattens adaxially (Fig. 93). A cleft first begins to form adaxially (Fig. 98) when the carpel primordium is 125 µm high. At a carpel height of 330 µm the cleft is still open, and ovule primordia are visible, being initiated within the open locule (Fig. 104). The margins become conduplicate, appressed along the cleft, and fuse from the base upward (see partial fusion at 500 µm height, Fig. 110). The cleft does not extend to the base of the carpel, which has a cylindrical pedestal at its base (Figs. 110, 112). This basal pedestal later elongates to form the short stipe (Fig. 3c). One flower seen (not shown) had an ovary of relatively smaller size than most, suggesting possible sexual dimorphism.
The hypanthium is first visible as a depression around the carpel base in Fig. 100 and persists in later stages (Figs. 107, 109–110). The carpel base is carried up the adaxial side of the hypanthium just before anthesis (Figs. 3c, 124). Trichomes develop rather sparsely over the surface of the ovary (Fig. 112), as well as on the abaxial side of the style (Figs. 116–117). In large buds, the stigma recurves (Figs. 122–123); the full-length line of carpel-margin fusion is evident on the style. At anthesis, the stigma is narrow, papillate, and distal to the cleft terminus (Fig. 123).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). All have paired persistent showy bracteoles at anthesis. Floral symmetry is dorsiventral (zygomorphic) in all except Brownea, which displays radial symmetry at anthesis.
|
). First, the floral apex is circular and relatively large compared to the bracteoles, directly after their initiation. Second, five sepals are produced; third, they are initiated in helical succession. This assemblage of character states contrasts with an assemblage seen in several other Detarieae in the Brachystegia group including Aphanocalyx, Monopetalanthus, and Brachystegia (Tucker, 2000
). In these latter taxa, the post-bracteole floral apex is narrow transversely and elongate in the sagittal plane. The bracteoles are relatively large directly after their initiation and occupy a large proportion of the apical circumference at that time. The number of sepals and petals is reduced to one or none. The floral apex becomes circular at stamen initiation, much later than in the Amherstia/Brownea/Tamarindus group. These differences are heterochronous in the sense that floral apex expansion occurs earlier in the Amherstia/Brownea/Tamarindus group, later in the Aphanocalyx group. Bracteole enlargement occurs late in the Amherstia/Brownea/Tamarindus group and early in the Aphanocalyx group. The distinctions transcend heterochrony, however, in that marked perianth reduction in number results from, or is correlated with, the reduced apical size at the critical time for perianth initiation in the Aphanocalyx group. Interestingly, bracteoles can be large and showy at anthesis in either group; in the Amherstia group, bracteole enlargement occurs later in development than in the Aphanocalyx group.
Sepals are initiated helically in Brownea, Amherstia, and Tamarindus. Petals are initiated helically in Brownea, unidirectionally in Amherstia and Tamarindus. Stamens are initiated unidirectionally in each whorl in all except Amherstia, in which those of the outer whorl are bidirectional starting in lateral positions. The carpel initiates concurrently with the petals in Brownea and with the outer stamens in the other two taxa. No overlap of organ initiation occurs between whorls in any of the taxa.
Shared post-initiation features include five sepals but a tetramerous calyx resulting from the two adaxial sepals becoming fused. Petal suppression affects two petals in Amherstia and Tamarindus, none in Brownea. The inner stamen whorl is initiated but suppressed in Tamarindus; some stamens are suppressed after their initiation in all taxa. All taxa have a hypanthium, and all except Tamarindus have the gynoecium attached adaxially to the hypanthial rim.
Previous and current work on Detarieae
The related literature on floral structure and development begins with a short and not very accurate series of drawings of Amherstia floral buds at different stages (Griffith, 1847). Baillon's (1872) meticulous descriptions of floral structure of many legumes included Amherstia, Tamarindus, and several other Amherstieae. Both these taxa figure in an interesting theory by Thompson (1924)
of a trend toward "sterility" in Amherstieae, which he arranged so that there appears to be a progressive loss of organs during evolution among various taxa of the tribe. Thompson erred in his assessment of order of initiation, because he depended on serial cross sections of buds.
Occasional bicarpellate flowers have been reported in Amherstia nobilis (Garcia, 1975
; van Heel, 1983, 1993
). The extra carpel is small and rudimentary according to van Heel; the two carpels are positioned opposite, with their dorsal sutures facing one another. Some preliminary observations on Amherstia nobilis (Tucker, 1997
) illustrated the late developmental timing of expression of floral specializations. The pollination biology and nectaries of Amherstia nobilis were described by Endress (1994
, pp. 273–275). Its floral structure suggests pollination by butterflies, although birds and Xylocopa bees also may pollinate it. Birds are thought to pollinate flowers of Brownea species (Arroyo, 1981
).
Concerted efforts are currently being made by many individuals to assemble relevant evidence from various fields to test phylogenetic relationships among Amherstieae/Detarieae. Among the approaches are comparative developmental floral anatomy (Tucker, 1999
, 2000
), fruit and vegetative morphology and fossil evidence (Herendeen, 1999
), wood (Gasson, 1999
), pollen (Banks, 1999
; Klitgaard and Banks, 1999
), molecular evidence (Gervais and Bruneau, 1999
), pollination biology (Lewis and Simpson, 1999
), and treatments of selected genera (Breteler, 1995
; Breteler and Wieringa, 1999
; Kruger, Tiedt, and Wessels, 1999
; and Mackinder, 1999
).
Fusion of organs
Fusion between organs is responsible for some instances of "loss." Some or all sepals are commonly missing throughout tribe Amherstieae, including all the taxa studied here. A trend toward a tetramerous calyx (rather than pentamerous) is evident in the Amherstia group (Amherstia, Humboldtia, Hymenostegia, Tamarindus), Cynometra, Brownea, Crudia, Detarium, Hymenostegia, and in parts of the Berlinia and Macrolobium groups. In taxa with a tetramerous calyx, the four-parted calyx is initiated as five sepals, the upper two of which become laterally confluent during development. In Tamarindus, there is an intermediate condition between the four- and five-sepal states. The two adaxial sepals fuse just above the level of the calyx cup, but the tips of these sepals are free.
Stamen bases are "fused" in a stamen sheath connecting the filaments in all three taxa studied here. The process involved is intercalary growth of the receptacle below the bases of the separate stamen filaments, rather than any actual fusion among organs.
The distinction between missing organs and suppressed organs has been discussed previously (Tucker, 1987, 1988b, 1990
). Basically, missing organs are of four types: "lost" organs are not represented by primordia during organ initiation, while "suppressed" ones are initiated and then fail to develop fully. The third type is transformation of organs, with concomitant loss of one set, and the fourth is reduction in number resulting from fusion among some members, as in the frequent fusion between the two adaxial sepals, seen in Amherstia, Brownea, and Tamarindus. Examples of totally missing organs in legumes have been shown in Caesalpinieae (Gleditsia, inner stamens; Tucker, 1991
), Cassieae (Ceratonia, petals; Tucker 1992b
; Labichea, one petal and eight stamens; Tucker, 1998; Dialium, four petals and eight stamens; Tucker, 1998), and in papilionoid tribe Swartzieae (Swartzia, four petals; Tucker, 1988b
, and unpublished data; and Ateleia, four petals; Tucker, 1990
).
Tamarindus shows organ suppression after initiation, in the inner whorl of four (rarely five) stamens, a whorl that is usually present in the majority of legumes (Tucker, 1987
). Both Amherstia and Tamarindus show organ suppression after initiation: one sepal, two petals, and two outer stamens as a rule. The number of suppressed organs can vary among flowers, because suppression may differ in degree.
Synchronous vs. sequential inflorescence
All taxa studied here have helically arranged inflorescences that develop acropetally during initiation. Mature inflorescences are paniculate, with ultimate racemes, in all except Brownea latifolia, which has cauliflorous capitate heads. Sequential order of flower initiation prevails except in Brownea, in which all flowers of an inflorescence develop synchronously. This latter order of development is extremely rare among legumes, except in Mimosoideae where it is the prevalent state (Tucker, 1987
; Ramírez-Domenech and Tucker, 1988
; Ramírez-Domenech, 1989
). The synchronous state is probably a specialization that has evolved at least twice among legumes.
Timing of appearance of zygomorphy
Zygomorphy can be defined either by appearance at anthesis (the usual method) or in developmental terms. Floral symmetry at anthesis is dorsiventral (zygomorphic) in all except Brownea, having radial symmetry at anthesis. Based on floral ontogeny, zygomorphy is expressed by a shift from helical or whorled order of initiation to unidirectional order. The calyx has helical order in Brownea, Amherstia, and Tamarindus, as in many caesalpinioid taxa (Tucker, 1987, 1988a, 1996
; Tucker and Kantz, 1997
). The shift to unidirectional occurs at petal initiation in Amherstia and Tamarindus, but not until stamen initiation in Brownea, which reverts to radial at anthesis.
The three genera share an assemblage of early-stage developmental character states considered significant (Tucker, 2000
). First, the floral apex is circular and relatively large compared to the bracteoles, directly after their initiation. Second, five sepals are produced; third, they are initiated in consecutive, helical order. This assemblage of character states contrasts with an assemblage seen in several other Detarieae including Aphanocalyx, Monopetalanthus, and Brachystegia (Tucker, 2000
). In these taxa, the post-bracteole floral apex is narrow transversely and elongate in the sagittal plane. The bracteoles enlarge directly after their initiation and occupy a large proportion of the apical circumference at this time. The number of sepals and petals is strongly reduced to one or none. The floral apex then becomes circular at stamen initiation.
These differences are heterochronous in that floral apex expansion occurs earlier in the Amherstia/Brownea/Tamarindus group, later in the Aphanocalyx group. Bracteole enlargement, on the contrary, occurs late in the Amherstia/Brownea/Tamarindus group and early in the Aphanocalyx group. Marked perianth reduction results from, or is correlated with, the reduced apical size at the critical time for perianth initiation in the Aphanocalyx group. Interestingly, bracteoles can be large and showy at anthesis in either group; in the Amherstia group, it occurs later in development than in the Aphanocalyx group.
The carpel initiates concurrently with the petals in Brownea and with the outer stamens in the other taxa. No overlap of organ initiation occurs between whorls in any of the taxa. The description of organogeny in Brownea by Hartog (1888)
differed from the current one in his assertion that primordia of the petal whorl and outer stamen whorl each initiated simultaneously. He speculated that this simultaneous initiation was connected in some way with the nearly radial symmetry at anthesis. Hartog's work depended upon observations of living buds with a dissecting ("simple") microscope and dissecting needles, so it is not surprising that his findings about organogeny were less accurate than those possible now with a scanning electron microscope.
Shared post-initiation features include five sepals but a tetramerous calyx resulting from the two adaxial sepals becoming fused. Petal suppression affects two petals in Amherstia and Tamarindus, none in Brownea. The inner stamen whorl is missing in Tamarindus, and some stamens are suppressed after their initiation in all taxa. All taxa have a hypanthium, and all except Tamarindus have the gynoecium attached adaxially to the hypanthial rim.
The search continues, so far unsuccessfully, for apomorphic characters that would define subfamily Caesalpinioideae. Inwardly tilted stamen primordia is a character that occurs in some taxa (but not all) in all four caesalpinioid tribes: species of Gleditsia and Caesalpinia (Caesalpinieae; Tucker, 1991
, Tucker, Stein, and Derstine, 1985
), Bauhinia spp. (Cercideae; Tucker, 1988a
), Saraca (Detarieae; Tucker, 1989
), Cassiineae (Cassieae; Tucker, 1992a
), and also in some papilionoid Sophoreae (Myroxylon and Castanospermum ; Tucker, 1993
). The search for shared specializations may be futile, as Caesalpinioideae appears to be the stem grade out of which several clades have arisen (Tucker and Douglas, 1994
; Bruneau, 1999
).
Shared states in the three detarioid taxa studied here include helical order of sepal initiation, fusion of two adaxial sepals, imbricate sepals, a filament sheath, a basal pedestal below the cleft of the carpel, a stipe, and a coiled style during late development.
