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2 Department of Biology (Ecology, Evolution, and Marine Biology), University of California, Santa Barbara, California 93106 USA; Department of Biology, Louisiana State University, Baton Rouge, Louisiana 70803 USA; and 4 Department of Biology, Saint Louis University, Saint Louis, Missouri 63103-2010 USA
Received for publication October 26, 1999. Accepted for publication February 15, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Adrastaea • androecium • centrifugal • Dilleniaceae • flower • Hibbertia • stamen fascicles • zygomorphy
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The temperate Mediterranean coast of southern Australia (south of the Tropic of Capricorn) and montane sites on the island of New Caledonia are centers of diversity for Hibbertia (Stebbins and Hoogland, 1976
). Stebbins and Hoogland (1976)
noted that the genus is remarkable for the striking interspecific diversity in floral symmetry (radial vs. dorsiventral or zygomorphic), in stamen number (3–200+ per flower), and carpel number (1–10 per flower). Wilson (1965)
showed that highly varied floral vasculature reflects differences in floral symmetry in the genus. Stamens are singly produced and free in some species, in fascicles or tufts in others, or forming a ring, more or less fused at base in yet others. The order of organ initiation may be entirely centripetal or may include centrifugal elements. The gynoecium shows variation in that styles are erect in some species, prostrate and projecting laterally in others. Carpels may be free or fused basally to some degree among different species (Dickison, 1968
). The species also vary greatly in habit, wood structure, leaf morphology and anatomy, inflorescence type, chromosome number, and karyology (Dickison, 1969, 1970a
; Stebbins and Hoogland, 1976
; Rury and Dickison, 1977
; Dickison, Rury, and Stebbins, 1978
; and Ehrendorfer, 1987
).
Our aim is to compare floral development among diverse representatives of the genus Hibbertia (Dilleniaceae) to elucidate the basis for the floral diversity that abounds in the genus. Adrastaea salicifolia also will be included, since this segregate genus differs primarily in the fusion of the outer five stamens. It had previously been considered a Hibbertia, monotypic in its own section Adrastaea (Stebbins and Hoogland, 1976
). The developmental bases will be sought for the following floral features that vary among taxa: symmetry (radial or zygomorphic); staminodia present or not; stamens in fascicles or not; stamen fusion; and carpel number. Although diversity also occurs in type of anther dehiscence (lateral slits or terminal pores), ovule number per carpel, and stigma type, consideration of these features will be deferred until a later paper. The variable floral features of species of Hibbertia and Adrastaea are associated with presumed contrasting pollinator behavior that has been investigated by Bernhardt (1984, 1986)
. Comparing floral development of Hibbertia species and of the satellite genus Adrastaea salicifolia (Syn.: Hibbertia salicifolia) allows us to add four overlapping pieces of information to the knowledge of Hibbertia sensu lato as a model system. First, an ontogenetic approach identifies the developmental bases for distinct floral features that vary among species, including symmetry, presence of staminodia, occurrence of staminal fascicles, ring meristems, stamen connation, and carpel number. Second, these developmental differences can then be related to functional aspects of floral morphology such as pollination biology (Bernhardt, 1984, 1986, 1996
; Keighery, 1991
). Third, floral development in Hibbertia and Adrastaea can be compared with that of other dilleniaceous genera. Finally, an assessment of comparative floral development in Hibbertia provides an opportunity to test the hierarchical-significance hypothesis of Tucker (1984, 1997)
, developed from work on legume flowers, in a markedly different plant family—the Dilleniaceae.
This project on Hibbertia was first planned in 1992, when a research proposal on comparative floral development of Hibbertia was submitted to the National Science Foundation by the senior author. It was not funded, nor was a sister proposal on pollination biology of Hibbertia by the second author. Due to recent interest in the project from another laboratory, the work on floral development has now been revived and updated for publication.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and accepted by Dickison (1968, 1969, 1970a, b)
and Stebbins and Hoogland (1976)
. The asterisks indicate those described and illustrated here.
Section Hibbertia
Hibbertia scandens* (
200 stamens and staminodia) and H. perfoliata* (60–80 stamens) were selected to show radial symmetry, free stamens, diversity in stamen number, and three to five carpels typical of this section. Hibbertia grossulariifolia* was studied with SEM to show increased number of carpels. Hibbertia dentata also was examined with SEM but is not illustrated or described since it resembles the other species in this section. All taxa in this section are radially symmetrical with free stamens.
Section Candollea
Hibbertia huegelii*, H. racemosa*, and H. saligna* were selected to show radial symmetry, a complete circle of fertile stamens in fascicles, and poricidal anthers typical of the section. Staminodia are lacking. Hibbertia racemosa has 10–12 stamens in three fascicles, H. fasciculata has 8–12 in three fascicles; H. saligna has 20–30 in three fascicles, and H. huegelii has 25–35 in five fascicles. Some additional stamens in each are initiated singly or united basally to stamen fascicle trunks. An SEM series was also obtained for H. cuneiformis, but is not illustrated.
Section Hemistemma
Hibbertia banksii* is representative of this section in showing zygomorphic floral symmetry, free fertile stamens (8–12 in number) in one or more basal clusters, with additional staminodia often present toward the outside (inside the petals), poricidal anthers, and two carpels. At least half the circle of stamens is absent or is replaced by staminodia.
Section Pleurandra
Hibbertia cistiflora, H. empetrifolia*, and H. hypericoides* are typical of this section in showing zygomorphic symmetry, an incomplete circle of fertile stamens, short filaments emerging from a solitary cluster of 2–12 fertile stamens, poricidal anthers, no staminodia, and carpels no more than two.
Other genera
Adrastaea salicifolia* has been segregated from Hibbertia, but is very close. The genera differ in that Adrastaea has two alternating whorls of stamens, and the filaments of the outer circle of stamens form a fused tube, while the stamens of Hibbertia are not fused to this extent. Adrastaea will be studied together with the species of Hibbertia, because of the possibility that developmental evidence may support reuniting it with Hibbertia.
Methods
The buds were dissected in 95% ethanol and then dehydrated through an ethyl alcohol series, critical point dried with CO2 in a Tousimus "Samdri-780" drier, and mounted on aluminum stubs with carbon conductive adhesive tabs (T. Pella Co., Redding, California, USA). They were coated with gold-palladium in a Denton "Desk-1" sputter coater. Scanning electron microscopy utilized a Cambridge S-260 in the Electron Microscope Facility at Louisiana State University, Baton Rouge, Louisiana, and a JEOL JSM-6300V in the Geology Department at University of California, Santa Barbara, California.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Organ numbers within individual androecia are species specific, ranging from three to 200, with a centrifugal order of initiation in most taxa with more than five stamens. Some androecia combine fertile stamens and staminodia (relatively unspecialized structures with filaments but nonfunctional anthers). Stamens are produced either singly or in discrete fascicles. Some fascicles are elongated structures resembling miniature candelabras, while others resemble an arched "hand" of bananas. In flowers of the satellite genus Adrastaea salicifolia, the filaments of an outer whorl of stamens unite to form a connate tube. Therefore, flowers of different Hibbertia species are either actinomorphic (radially symmetrical) or zygomorphic, depending mainly on variation in stamen arrangement (Stebbins and Hoogland, 1976
).
The gynoecium consists of one to ten carpels per flower, with some ovaries showing minor connation (Dickison, 1968
). Carpel number often is correlated with the presentation and symmetry of the androecium. Styles are held erect in some species, or project laterally in others (Bernhardt, 1996
). Upon reviewing the genus, Stebbins wrote (1974, p. 184) "there is probably no other genus of angiosperms that exhibits such a high degree of variation in those floral characteristics that are regarded as "fundamental" and are usually associated with the separation of genera or of even higher categories."
Androecium and gynoecium characters are so stable within species of Hibbertia that they have been given priority as taxonomic characters for almost 140 yr. Bentham and Mueller (1863)
organized the Australian species into four sections. While sectional names and characters have changed, to date they continue to be treated as natural subunits, identified on the bases of stamen/staminodium numbers, androecium symmetry, and, to a lesser extent, carpel number (see Stebbins and Hoogland, 1976
). The majority of keys to species begin with couplets comparing the relative positions of stamens around the ovaries (Bentham and Mueller, 1863
; Stanley and Ross, 1983
; Wheeler, 1987
; Harden and Everett, 1990
).
Phenology
The majority of species of Hibbertia in temperate-Mediterranean regions of Australia flower from mid-winter to mid-summer (July to January in Australia). Individual plants in subtropical populations of H. scandens (Fig. 1a) may flower twice a year with peaks in September and March (T. Hawkeswood, personal observations). Each Hibbertia flower arises terminally on a vegetative branch (often on a short side branch without elongated internodes) or in a leaf axil. In contrast to cymose species of New Caledonia, the majority of Australian species bear solitary flowers, with each bud subtended by a vegetative leaf. Flower buds open in acropetal or subacropetal order along the stem. Flower presentation may be erect, horizontal, or nodding, depending on species habit (Bernhardt, 1984, l986
; Harden and Everett, 1990
).
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). In the majority of species, flower-bearing shoots collected for herbarium vouchers drop their petals within an hour of cutting. Retention of petals on cut branches appears limited to a few species bearing thick, leathery leaves (e.g., H. dentata, H. scandens).
In Adrastaea salicifolia (Fig. 5a), ovaries are covered by the stamens, and erect styles protrude from the center of two whorls of stamens in recently opened flowers. In most Hibbertia species, stamens arch inward at anthesis so that the ovaries are largely obscured by the stamens, particularly where the stamen number is high. Therefore, stigma exposure in radially symmetrical flowers depends on stamen number per flower and on the angle of stylar position. Adrastaea salicifolia and a few species of Hibbertia (e.g., H. dentata) bear longitudinally dehiscent anthers. Most Hibbertia species have anthers that are porose or poricidal (sensu Buchmann, 1983
) with the dehiscence of sutures restricted to two expanding subapical slits.
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. Scent production is centered in anther sac interiors, in pollenkitt, and on stigmas, based on neutral red tests (Bernhardt, 1984, 1986
) on H. dentata, H. diffusa, H. fasciculata, H. saligna, H. scandens, and H. stricta. The flowers lack nectar glands or secretion (Bernhardt, unpublished data); pollen is the primary edible reward.
Organography of selected species
Each flower of the examined Australian species of Hibbertia arises terminally on a vegetative branch (often on a short branch without elongated internodes); the branch or stem may bear flowers in each leaf axil. Technically flowers are solitary (because each is subtended by a vegetative leaf), although a stem may bear several flowers. Inflorescences are found in some New Caledonian species and a few Australian species (Stebbins and Hoogland, 1976
; Veillon, 1990
), but no developmental series of these were available for this study. The petals of Hibbertia species are obovate and yellow to yellow-orange, with anthers slightly darker.
Hibbertia scandens (Willd.) Gilg (Figs. 1a–c, 6–20, 22)
Hibbertia scandens is a scrambling vine 2–5 m tall from Queensland, Northwest Territory, and New South Wales. Flowers are yellow to gold, solitary and terminal on otherwise vegetative branches. They are sessile or short-stalked. Floral symmetry is radial, and calyx, corolla, and gynoecium are pentamerous (Fig. 1a, c). Sepals are 8–12 cm long, silky-hairy abaxially; petals are 2–3 cm long and membranous; stamens are numerous (150–200) with occasional staminodia (2–6 per flower), and carpels are 3–8 and glabrous (Elliot and Jones, 1990
).
Organogeny of Hibbertia scandens
The five sepals are initiated successively in a 2/5 quincuncial spiral (Fig. 6), the outer sepals largest and partially enclosing the rest during initiation (Fig. 7) and in bud (Fig. 1b). The five petals are initiated nearly simultaneously and alternate to the sepals (Fig. 8) around a flat floral apex. Because petal primordial size diminishes inward along a 2/5 spiral (Figs. 9–11), their initiation may be successive, although no petal stages were seen with less than all five petals present. The ontogenetic spiral is continuous and in the same direction from sepals through petals (Figs. 1c, 9).
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Five carpels are initiated in a circle (at arrowheads, Fig. 15) inside the original whorl of stamens, concurrently with the centrifugally initiated stamens. The carpel primordia heighten, develop adaxial clefts (Fig. 17), and become tapered terminally (Fig. 18). At anthesis the stamen anthers are lanceolate, basifixed, tetrasporangiate, and poricidal (Fig. 22). The stigmas at anthesis (Fig. 22) are narrow and truncate.
Hibbertia grossulariifolia (Salisb.) Salisb. (Fig. 21)
Hibbertia grossulariifolia is a prostrate shrub from Western Australia. The flowers are 15 mm in diameter with radial symmetry, solitary on peduncles 20–30 mm long. The five sepals are 5–6 mm long, ovate and acuminate; the five petals are 5–8 mm long, light yellow, obovate and shallowly indented. Stamens are 100, and staminodia are also present. There are 8–15 hairy free carpels (Elliot and Jones, 1990
). Organogenetic stages of this species were not available to us, but Payer (1857)
described and illustrated some stages in its development. Five stamens are initiated on mounds that alternate with the petals. Additional stamens form centrifugally on each of the five mounds until 100 have been initiated, when the original five groups can no longer be distinguished. Five carpel primordia are initiated concurrently with, and alternate to, the first five stamen primordia and above them on the floral apex. A second whorl of approximately five carpels then is initiated acropetally from the first carpel whorl. A large flower bud with numerous stamens and eight carpels is shown in Fig. 21 (perianth removed).
Hibbertia perfoliata Endl. (Figs. 23–37)
Hibbertia perfoliata is a weakly ascending (to 0.5 m) or prostrate shrub from Western Australia. The flowers are solitary and axillary, 15–28 mm in diameter, on peduncles 10–65 mm long. The ovate sepals are 7–10 mm long, glabrous, acuminate, and reflexed, and the five petals are 7–15 mm long. The flower resembles that of H. scandens except that the total stamen number is less than half that of H. scandens. The 60–80 free stamens have anthers that are elliptic, oblong, or obovate, and dehisce by longitudinal slits. There are numerous staminodia outside the stamens. The three to five carpels are glabrous (Marchant et al., 1987
).
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Stamen initiation is preceded by an increase in apical diameter (compare Figs. 27 and 28). The first stamen primordia are initiated successively, beginning with a few high on the apical flanks (at arrowheads, Fig. 27). More stamens are initiated until there is a ring or whorl of 12 (Fig. 28) around the floral apex. These stamen primordia at first show little regular alignment with respect to the petal primordia. Subsequent stamen primordia are initiated in gaps among the primordia of the original ring (compare numbers of primordia in the innermost ring in Figs. 30 and 33), and centrifugally (Figs. 29 at arrowheads, 30), outside the first ring. In Fig. 31, it becomes evident that there are five antesepalous "triplets" or clusters of stamen primordia; one triplet is bracketed. Each triplet consists of a cluster of organs initiated in a predictable sequence: a single one high on the apical flank, then a pair centrifugally, one on either side of the first. Each triplet is here augmented by another single primordium on the same radius as the first, then another pair centrifugally. Additional primordia continue to be initiated centrifugally (Figs. 31–34), which obscure the original five triplets. In this species, there are no common primordial mounds preceding triplet initiation. Eventually there are 65 stamens present, four to five deep radially (Fig. 37). Anthers are differentiating in Fig. 37, with the innermost stamens becoming differentiated first, the others in their order of initiation. The "triplet" aspect will be more prominent and persistent in the next species, H. huegelii.
The floral meristem of Hibbertia perfoliata inside the original ring of stamen primordia is flat to very low convex (Figs. 28, 29). The five carpel primordia are initiated simultaneously on the apex (Figs. 30–32, at arrowheads), utilizing most of the remaining apical meristem and leaving a small residuum at center. The carpel primordia are at first small distinct mounds (Figs. 32–34). They heighten and show an incipient cleft (Figs. 35, 36) at 70 µm in height. No older stages of carpels were available for study.
Hibbertia huegelii (Endl.) F. Mueller (Figs. 2a, b, 38–52)
Hibbertia huegelii is a low shrub, sometimes semiprostrate to 0.5 m high, of Western Australia (Marchant et al., 1987
). Flowers are terminal on axillary branches, solitary or paired. Each flower (Fig. 2a) is 20–35 mm in diameter, subtended by leaves and brown scarious bracts. The five sepals are ovate to elliptic, 10–17 mm long, the inner wider than the outer, with acuminate ciliate tips. The petals are obovate, indented, and 15–20 mm long. The 25–35 stamens are arranged in five fascicles of four to eight stamens each (Fig. 2a, b). The stamens in each fascicle are connate (Marchant et al., 1987
), with occasionally one free. Anthers dehisce by longitudinal slits. The five carpels are glabrous.
Organogeny of Hibbertia huegelii
The five sepals are initiated successively in a 2/5 spiral (Figs. 38, 39). Next, five petals are initiated simultaneously or in very close succession (Figs. 39, 40). In Fig. 40, two of the petal primordia are slightly larger (at 2 o'clock and 7 o'clock), indicating a 2/5 spiral order of initiation. The petals are equidistant. They enlarge, broaden, and overlap, the outer two being larger than the rest during development (Fig. 51).
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Just before carpel initiation, the floral apex flattens and is pentagonal (Fig. 46). The five carpels are initiated simultaneously (Figs. 47, 48) on the edges of the flat apex, alternate to the five stamen fascicles. The carpels remain free and are shorter than the surrounding stamens during development. The carpel clefts form adaxially (Fig. 51).
Hibbertia racemosa (Endl.) Gilg (Figs. 53, 54)
Hibbertia racemosa is a small erect shrub (to 0.4 m high) of Western Australia, with flowers on slender peduncles 1–3 cm long, in leaf axils. Flowers are radially symmetrical and have sepals 0.5–0.6 cm long, with the outer ones narrower than the inner; petals 0.5–0.7 cm long, obovate; stamens 10–12, joined in three bundles of three or four; one or two stamens free; infrequent staminodia; and three glabrous carpels (Elliot and Jones, 1990
). Hibbertia racemosa resembles H. saligna (Fig. 3a) in having stamen fascicles and relatively few stamens.
Organogeny in Hibbertia racemosa
Developmentally, Hibbertia racemosa differs from H. huegelii in that only three stamen primordia are initiated in the first whorl. Developing around these three are three common primordia that initiate most of the stamen primordia, although there are five common primordia in all. The three most productive common primordia are antesepalous, with a truncate outer periphery. Each of these three common primordia produces four or five stamens (Figs. 53, 54), the innermost first (at arrowheads), followed by a pair, one on either side of the first. The fourth stamen primordium of each common primordium is on the same radius as the first and centrifugal to it; a fifth may be added (Fig. 54, at arrow). Each of the two less active common primordia initiates one to three stamens (arrows, Fig. 53). The flower becomes asymmetrical at initiation of the first three stamen primordia and the three carpel primordia, which together form an asymmetrical pattern (Fig. 53). Although nearly zygomorphic, positions of the two weaker common primordia disrupt that configuration so that the flower is asymmetric. In no way is this a transition between actinomorphic and zygomorphic flowers.
Only three carpels are initiated in H. racemosa, a number correlated with the three most prolific stamen fascicles, even though there were five common primordia. The three carpels are not symmetrically arranged (Fig. 53) when seen at a young stage.
Hibbertia saligna R. Br. ex DC. (Figs. 3a, b, 55)
Hibbertia saligna is a small shrub to 2 m high and l.5 m wide, native to New South Wales. The radially symmetrical flowers (Fig. 3a, b) are 30–40 mm in diameter, sessile above a cluster of bracts. The five sepals are 12–16 mm long, thick, and imbricate, trending from outer acute to inner blunt-tipped. The five membranous obovate, imbricate petals are 15–20 mm long, bright yellow, obovate and with only a shallow notch (Fig. 3a). There are 20–30 stamens evenly distributed in three clusters around the three glabrous carpels at center (Fig. 3a, b; Elliot and Jones, 1990
). Rarely, staminodia may be present in the fascicles that are only weakly developed.
Organogeny of Hibbertia saligna
Initiation of organs in Hibbertia saligna is similar to that of H. huegelii, including radial symmetry and stamen-fascicle formation, except that the first whorl of stamens includes three rather than five members. Carpel number also is fewer: three, vs. five in H. huegelii. Two of the five stamen fascicles in H. saligna are only weakly developed, as in H. racemosa. Three stamens are initiated symmetrically in the first whorl (Fig. 55) compared to five in H. huegelii, and three asymmetrically in H. racemosa. The three early stamen primordia are equidistant and in antesepalous sites (at arrowheads, Fig. 55). Each serves as a locus for centrifugal initiation of three additional stamens: a pair below and to either side of the first (Fig. 55), and then a single primordium directly below the first stamen. The flower of H. saligna in Fig. 55 is radially symmetrical, although the number of stamens per common primordium differs somewhat. The 12 stamens in these three fascicles are augmented in some flowers by two to four additional single stamens that are not in fascicles. Hibbertia saligna demonstrates a modification toward reduction in stamen number by limitation of the number and development of fascicles.
Hibbertia fasciculata R. Br. ex DC. (not illustrated)
Although only large buds and open flowers were available to us, Hibbertia fasciculata is a species of interest because it varies from three stamens per flower in New South Wales populations to seven to nine stamens in Victoria populations. In the former material, three stamens alternate with the three carpels in a radially symmetrical flower. However, the base of each stamen is attached to a broad flat platform, similar to that supporting two or more stamens from a common primordium in species such as H. huegelii. This feature will be discussed later.
Hibbertia banksii Benth. (Figs. 56–67)
Hibbertia banksii is a small shrub to 2 m high from Queensland, having one-sided terminal leafy branches of flowers, and brown tomentose flower buds. The flowers have zygomorphic symmetry, five sepals 0.6–0.8 cm long, rusty-hairy abaxially; five yellow petals 1.3–1.8 cm long, obovate, notched, margins often crinkled; and 20–30 stamens plus 12–20 staminodia, clustered on one side of the two hairy carpels (Elliot and Jones, 1990
).
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The floral apex becomes more convex after petal initiation (Fig. 58). A ridge forms across the middle between the abaxial and adaxial sides, and three to five stamen primordia are initiated in a row on this ridge. The center primordium forms first, then the others in outward succession toward either side (Fig. 59), with up to seven stamen primordia in the first row in Fig. 62. The outermost in the row are antesepalous. Up to three additional rows of stamen primordia are initiated (Figs. 60–62) in centrifugal order toward the adaxial side. The center primordia are initiated first in each row, the end primordia last in each row. The total stamen number is 23–30 (Figs. 64, 65), plus 12–20 staminodia initiated last, along the periphery on the adaxial side (at arrowheads, Figs. 65, 67). The stamens become lanceolate, with a notch at the tip (Fig. 67). All sporangia dehisce by longitudinal slits toward the center of the flower (Fig. 66).
Before carpel initiation, the remaining floral apex on the abaxial side is flat and sloping below the stamen primordia (Fig. 60), and rather angular from pressure of overlying organs. The two carpel primordia are initiated, facing each other, on the abaxial side of the floral apex (at arrowheads, Fig. 61). The styles form early (Figs. 62, 63), becoming reflexed and folded distally. Clefts become visible (Fig. 64) after the styles become vertically oriented. The carpels are connate at their bases (Fig. 64). A row of trichomes forms along the adaxial side of the carpel and along the earliest formed stamens (Fig. 64). Later, the trichomes are elongate and abundant, obscuring the outlines of the two ovaries (Fig. 66); the trichomes also cover the base on the adaxial side of the flower (Fig. 67). The two pistils have densely hairy ovaries, slender styles, and narrowly punctiform stigmas (Figs. 66, 67).
Hibbertia hypericoides (DC.) Benth. (Figs. 68–70)
Hibbertia hypericoides is a small spreading shrub to 1 m high from Western Australia, with flowers solitary in leaf axils (Elliot and Jones, 1990
). Flowers are deep golden yellow and zygomorphic. The five sepals are 0.5–0.6 cm long and densely covered with stellate hairs; the five petals are 0.7–1.2 cm long, cuneate, and deeply notched. The ten to 15 fertile stamens are in a single fascicle (Figs. 68, 69) on one side of the flower. Staminodia are 15 in number, spathulate, and positioned around the bases of the two trichome-covered carpels (Figs. 69, 70). Organogenesis in this species is very similar to that of H. banksii, so is not shown. An exceptional feature of H. hypericoides is the unusual morphology of its staminodia (Figs. 69, 70).
Hibbertia empetrifolia (DC.) Hoogl. (Figs. 4a, b, 71–83)
Hibbertia empetrifolia is either a small shrub to 2 m tall and to 3 m wide, or a scrambling vine with wiry stems, native to Victoria, Tasmania, and New South Wales (Elliot and Jones, 1990
). The flowers (Fig. 4a, b) are 10 mm in diameter on peduncles 5–15 mm long. The five sepals are 3–4 mm long, in an imbricate whorl; petals are 4–5 mm long, bright yellow, and notched (Fig. 4a, b). There are four to 12 stamens in a fascicle on one side of the two carpels (Fig. 4a, b) and no staminodia.
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Prior to stamen initiation, the floral apex becomes increasingly convex, with an incipient ridge between adaxial and abaxial sides (Fig. 75). Stamen initiation begins with three stamen primordia in a row across the middle of the floral apex (Fig. 76). Additional stamen primordia are initiated: two or three adaxially (Figs. 77, 78) and two laterally (Fig. 78) on either end of the original row of three. Depending on the number formed after the first three, the total stamen number is 5–8 in a single fascicle. The stamen anthers are tetrasporangiate, basifixed, with filaments attached to a common broad base as a single fascicle (Figs. 79, 80). The anthers dehisce by lateral slits (Figs. 81, 82).
The two carpel primordia are initiated on the abaxial side of the floral apex (at arrowheads, Figs. 76, 77). The carpels become arcuate in polar view, and their clefts face each other (Fig. 78). The two carpels are basally connate (Fig. 81), and each has a fused adaxial suture extending its full length (Figs. 81–83). The ovaries become covered by stiff trichomes, the styles are twisted, and the stigmas are punctiform (Figs. 82, 83).
Adrastaea salicifolia DC. (Figs. 5a–e, 84–96)
Adrastaea salicifolia is monotypic; it resembles a Hibbertia closely in its five-merous calyx and corolla, each with imbricate aestivation (Fig. 5a–e). The androecium differs from any Hibbertia, however, in that the outer whorl of five stamens is antepetalous and the inner whorl of five is antesepalous (Fig. 5a, c–e). There are two free carpels (Harden and Everett, 1990
).
Organogeny of Adrastaea salicifolia
The floral apex is low convex before sepal initiation. Five sepals are initiated successively in a 2/5 helix (Fig. 84). Initiations are high on the flanks, so that the remaining apex is nearly flat; the peduncle is formed at this time. Five petal primordia are initiated nearly simultaneously (Fig. 85) but in a 2/5 helix, judging from slight differences in petal sizes (Figs. 85, 88). Sepals, petals, and stamens are on the same phyllotactic spiral (Fig. 88). After petal initiation, the floral apex is a low-convex mound (Figs. 86, 87). Five stamens are initiated (at arrowheads, Figs. 86, 87) in antesepalous sites. These first five stamen primordia are indicated by asterisks in Figs. 88–91 during completion of organogeny. The two carpels are initiated next (at arrowheads, Fig. 88) around the floral apex. One is on the same radius as the earliest initiated petal, while the other is opposite a sepal. The floral apex then expands as a narrow ring meristem (at arrowheads, Fig. 89) between the petals and stamens. An outer whorl of five antepetalous stamen primordia is next initiated on the ring meristem (Figs. 90, 91), centrifugally from the first whorl of stamens. The facts that the stamens of the outer whorl form last and are antepetalous (and the flower obdiplostemonous) are highly unusual and provide support for generic segregation of the taxon. Centrifugal order of initiation prevails in the androecium and contributes to the obdiplostemonous condition. The outer five stamen primordia (A, Figs. 92–95) are laminal, emarginate at their tips, and confluent basally (Figs. 92, 93, at arrowheads). Occasionally, one or two extra stamen primordia are initiated outside the outer five (at arrows, Fig. 94).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Sections Hibbertia and Candollea are included in the first group with radial symmetry. The two sections are distinguished by presence of staminodia in Hibbertia and by presence of stamen fascicles in Candollea. Innovations in the radially symmetrical group provide various means of achieving polystameny: by meristem rings and increased floral-apical size among members of section Hibbertia, by common primordia in section Candollea, and by a late-forming meristem ring without apical size increase in Adrastaea. Staminodial development is activated at a later stage when floral organs differentiate; some of the last-initiated stamen primordia around the periphery may fail to develop anthers. The distinction between presence and absence of staminodia is hence a mere superficial distinction that does not affect later stages of development. The group of taxa with zygomorphic symmetry includes species in sections Hemistemma and Pleurandra. The flower is actinomorphic during sepal initiation, then becomes zygomorphic with unidirectional petal initiation. Stamen primordia are initiated as a linear row across the summit of the floral apex, which may be augmented by additional rows on either side. Two carpel primordia are initiated laterally on one side. This order of organ initiation, with stamens terminal on the floral apex and carpels lateral, is highly unusual, and has not previously been reported for any angiosperm. The two sections are distinguished by presence of staminodia in Hemistemma, vs. their absence in Pleurandra. This distinction in presence/absence of staminodia is of minor significance, depending on events during organ differentiation.
Despite the marked morphological differences in symmetry, Stebbins and Hoogland (1976)
upheld the unity of the genus Hibbertia, based on presumed intermediates in floral structure between the two types of symmetry. Baillon (1871)
also reported what he considered intermediates in symmetry in Hibbertia. In one example (Stebbins and Hoogland, 1976
), Hibbertia hermannifolia DC. has two carpels with stigmas both curved downward and stamens somewhat unequally placed around the carpels. The bending of the styles (radiating outward in actinomorphic flowers, or parallel in zygomorphic ones) is a late event in floral development, occurring as the flower bud opens. Late developmental events such as this stylar inflexion tend to be potentially more labile than early organogenetic events (Tucker, 1984, 1997
). One of the "intermediates" noted by Baillon is H. angustifolia (R. Br. ex DC.) Benth., in which there are two carpels at center and six fascicles: two of fertile stamens, both on one side but separated by a fascicle of staminodia. Two other staminodial fascicles stand on the side opposite the fertile clusters of stamens. It would be desirable to examine organogenesis of stamens in these putatively intermediate species.
We found examples that might be thought to show intermediate symmetry in H. saligna, which has three antesepalous fascicles of stamens and two single stamens in the other two antesepalous positions. Thus the flower has zygomorphic symmetry, but only in a subtle sense not easily recognized at anthesis when the stamens become rather evenly distributed around the periphery. Zygomorphic symmetry in this species results from a different developmental mechanism (failure of common primordia to proliferate equally) from that in the Hemistemma/Pleurandra group (stamen initiation in apical rows, followed by lateral carpel initiation). Zygomorphy has arisen at least twice in evolution of the genus, based on our small sample. The two zygomorphic states are alternate states and not homologous since they arise by quite different mechanisms. An example of asymmetry was found in H. racemosa, which shows reduced activity in two of the five common stamen primordia.
Centrifugal order of initiation
Species of Hibbertia having only three or five stamens per flower show acropetal order of initiation for all organs. But the great majority of species of Hibbertia (including those studied here) with more than five stamens per flower show centrifugal order of stamen initiation. Payer (1857)
remarked on centrifugal order of stamen initiation in several families, but the character has received little other attention. Corner (1946)
reported centrifugal stamen order in 14 dicotyledonous families, with particular attention to Wormia and Tetracera in Dilleniaceae and Bixa in Bixaceae. Sattler (1972)
described widespread examples among plant families of centrifugal order of initiation of particular floral organs, but indicated that no flower has entirely centrifugal order. In flowers of Lythrum, three types of organs are initiated centrifugally (Cheung and Sattler, 1967
; Sattler, 1972
). Stamens are the organs that most commonly are initiated centrifugally, often in flowers having numerous stamens. Examples of centrifugal order are reported in Pereskia (Cactaceae—Leins and Schwitalla, 1986
), Capparis (Capparidaceae—Leins and Metzenauer, 1979
; Erbar and Leins, 1997
), Hypericum (Hypericaceae—Leins, 1964a, b, 1979
), Lagerstroemia and Punica (Lythraceae; Punicaceae—Mayr, 1969
), Lythrum (Lythraceae—Cheung and Sattler, 1967
), Paeonia (Paeoniaceae—Schöffel, 1932
; Hiepko, l965; Leins and Erbar, 1994
), Thea, Stewartia (Theales—Erbar, 1986
), and in Hydrocharis and Limnocharis (monocotyledonous families Hydrocharitaceae and Limnocharitaceae—Kaul, 1967, 1968
).
Fascicled stamens vs. free stamens
In sections Pleurandra and Candollea of Hibbertia, stamens are produced in clusters called fascicles. The filaments are fused basally, with three to ten anthers on one fascicle. Wilson (1965)
investigated many species of Hibbertia having fascicles, and Sporne (1958)
found that each fascicle is generally supplied by a shared vascular trace. Tucker (1972)
explored the strong correlation between fascicled stamens, common stamen traces, and centrifugal initiation among angiosperm taxa. Several other plant families have one or more taxa with fascicled stamens: Actinidiaceae (Brown, 1935
; Wilson, 1937, 1965, 1974
; Aizoaceae (Payer, 1857
; Kawano, 1965
); Bombacaceae (Wilson, 1937
); Clusiaceae (Leins and Erbar, 1991
); Flacourtiaceae; subfamily Morobonoideae of Guttiferae (Kawano, 1965
); Hydrangeaceae (Hufford, 1998
); Hypericaceae (Corner, 1946
; Hirmer, 1918
; Sporne, 1958
); Loasaceae (Hufford, 1990
); Malvaceae (Wilson, 1937
; van Heel, 1966, 1984
); Paeoniaceae (Schöffel, 1932
; Hiepko, 1965
; Leins and Erbar, 1991, 1994
); Sterculiaceae (Payer, 1857)
; Theaceae (Erbar, 1986
; Tsou, 1998
), and Tiliaceae (Payer, 1857)
.
Developmentally, each stamen fascicle develops from a single common primordium. In Hibbertia (and other families: e.g., Hufford [1990, 1998]
—Loasaceae and Hydrangeaceae) the first stamen primordium is median and on the innermost side of the common primordium. Subsequent organs form centrifugally beginning with a pair, one on either side of the first. This set of three stamens from the common primordium is termed a "triplet" by Hufford (1998)
. Stamen organogeny may cease after the first triplet on the common primordium, or it may continue by adding pairs and single primordia alternately outward.
The stamen-forming common primordia in Hibbertia species are antesepalous, standing in the sites of individual stamens in many other dicot flowers. For this reason, the stamen fascicle has been interpreted occasionally as equivalent to a single highly branched stamen that has been telescoped at its base (Wilson, l937
). Stebbins and Hoogland (1976)
suggested that the fascicle (rather than individual stamens) in Hibbertia is "the fundamental unit of the androecium." However, developmental evidence shows that the stamens of each fascicle are initiated individually and become "fused" basally by intercalary elongation below the filament bases.
Ring meristem
Stamen proliferation by activity of a ring meristem ("Ringwall" in some European literature), interpolated between whorls of petals and carpels, is an innovation recognized in some species of Hibbertia (H. scandens), Adrastaea salicifolia, and other genera of Dilleniaceae that have been studied developmentally (Corner, 1946
; Endress, 1997
). Such ring meristems have evolved in many other plant families, for example, Bixaceae (Bixa—Corner, 1946
; Ronse Decraene, 1989
), Cactaceae (Leins and Schwitalla, 1986
), Capparidaceae (Capparis—Leins and Metzenauer, 1979
), Cochlospermaceae (Cochlospermum—Corner, 1946
; Keating, 1972
; Ronse Decraene, 1989
), Hypericaceae (Hypericum—Leins, 1964a, b
), Lecythidaceae (Couroupita—Leins, 1972
), Lythraceae (Lagerstroemia—Mayr, 1969
), Malvaceae (Payer, 1857
; Sattler, 1973
), Punicaceae (Punica—Mayr, 1969
; Leins, 1988
), and Theaceae (Stewartia—Erbar, 1986, 1988
; Camellioideae—Tsou, 1998
). A more extensive compilation is given by Ronse Decraene and Smets (1992)
. Most taxa with a ring meristem are polystemonous, but a few legumes having a ring meristem produce only ten stamens (Tucker, 1990, 2000
).
Homology among floral organs
Burger (1996)
recently challenged the convention that stamens are homologous to other floral organs. One basis was the supposed cylindrical shape of stamen primordia during early stages, compared to a "laminar" shape in petal primordia. But during development (before microsporangia become evident), primordia of stamens often appear broad tangentially. Examples can be seen in Cassia and Chamaecrista (Tucker, 1996a, b
), Ceratonia (Tucker, 1992
), and Gleditsia (Tucker, 1991
), among many examples available. In the current work, the stamen primordia of the outermost whorl in Adrastaea salicifolia are broadly laminar (see Figs. 92–95). Another misconception by Burger about floral development is that the cylindrical stamen filament is derived directly from the cylindrical stamen primordium. However, in most taxa, the anther is the first part of the stamen to form from the primordium, as a sessile structure. The filament is formed late in development, in many cases appearing very short until a late stage.
The strongest evidence for homology of stamens with other floral organs is ontogenetic, namely that perianth members and stamens all are initiated alike in most flowers, as lateral appendages on the flanks of the floral apical meristem. Histological details of initiation are basically alike. Small differences in depth of the initiatory periclinal cell divisions have been reported (reviewed in Esau, 1965
), but the similarities of appendage ontogeny overwhelm these small differences. The appendages are also very similar in early developmental stages (Esau, 1965
). In Gleditsia triacanthos, for example, sepals, petals, and stamens lie on the same ontogenetic helix, and organ identity is often quite difficult to distinguish in the early stages (Tucker, 1991
). Laminar form of petals is not evident in early stages, so that petal and stamen primordia are difficult to distinguish except by position.
Floral vasculature as it relates to centrifugality
Literature on this subject is reviewed here because of the fact that previous work on vasculature showed the need for ontogenetic study to explain some of the anomalies. Stebbins and Hoogland (1976)
pointed out the need for developmental studies in Hibbertia, because of the high level of androecial diversity. Anatomical structure of stamens (Dickison, 1970b
) and carpels (Dickison, 1968
) has been examined for the family. Carpel anatomy is rather uniform among species (Dickison, 1968
). Wilson (1965, 1974)
demonstrated in detail the remarkable range of stamen structure and vasculature at anthesis among 58 species representing the major sections of Hibbertia and other genera of the family. Ozenda (1949)
and Sastri (1958)
also reported on the floral vascular system of several dilleniaceous taxa. Sporne (1958)
illustrated the unusual stamen trunk bundles in diverse families, including Hibbertia scandens in Dilleniaceae. He asserted that occurrence of these highly branched vascular trunk bundles is correlated with centrifugal direction of initiation. The numerous stamen traces are basally connected to a few trunk bundles, because in a centrifugal system there is no remaining undifferentiated procambial tissue in the receptacle, within which additional stamen traces could differentiate downward from the newly initiated primordia. Tucker (1972)
explored this hypothesis of correlation between fasciated stamen clusters and internal trunk bundles from a developmental point of view.
Previous work on floral structure and ontogeny of Hibbertia
Baillon (1871)
described the floral morphology of the major taxa. Floral development has been reported for two species of Hibbertia, H. scandens (Sattler, 1973
), and H. grossulariifolia (Payer, 1857)
. Hibbertia scandens has a pentamerous calyx and corolla, 150–200 stamens produced centrifugally, and five carpels. Order of initiation is helical in the calyx and helical to simultaneous in the corolla. The first five stamens arise alternately to the petals, after which additional stamen primordia arise outside the first five in a centrifugal direction. The five carpels are initiated last, in helical succession at the center of the androecium. Sattler was uncertain whether common primordia were present preceding initiation of stamens (they were not found in the present study) and about the exact order of stamen initiation among the numerous stamens after the first five, except for their centrifugal direction.
The description of floral ontogeny in H. grossulariifolia (Payer, 1857)
differs from that just described, in that Payer reported simultaneous petal initiation, then five common primordia on which several stamen primordia are initiated in basipetal (centrifugal) order, and two whorls of five carpels each. Structure and function of the common primordia described by Payer resemble those in H. huegelii and H. racemosa, examined here.
Evolutionary trends in Australian species of Hibbertia
The major trends are from radial symmetry to zygomorphy, toward either increase or decrease in stamen number and carpel number, and toward basal fusion among stamen filaments. Two additional trends in the New Caledonian species, toward heteranthery and aggregation of solitary flowers into inflorescences, were not studied because of a lack of material. One may ask whether the observed evolutionary trends in Hibbertia confirm the hierarchical-significance hypothesis that one of us (Tucker, 1984, 1997
) has proposed? This hypothesis proposes that early events in a developmental cascade tend to be stable and canalized, while late events are more prone to evolutionary lability. The stable, early-expressed character states often characterize suprageneric levels of hierarchy (here sections), while the late-expressed character states typically distinguish lower levels of hierarchy such as species. Any change in early events has a profound effect on development of subsequently produced organs, while a change in late events has relatively little effect on other organs. Many examples in legumes support the hypothesis (Tucker, 1997
), and it is important to test it in other plant families with differing floral structure as well.
In Hibbertia the shift from radial to zygomorphic floral symmetry is determined early, directly after sepal initiation, which is uniform throughout the genus. Subsequent developmental pathways of stamen and carpel organogenesis differ markedly in the two groups. In radially symmetrical flowers, petals are initiated helically and stamen primordia are initiated in a circle all round the floral apex, followed by initiation of a circle of carpel primordia acropetally and by additional stamen primordia basipetally. In zygomorphic species, petals are initiated unidirectionally, and the first stamen primordia are initiated in a linear row across the summit of the floral apex, followed by additional stamens to one side centrifugally and initiation of two carpel primordia on the opposite side. The fact that symmetry is determined early in Hibbertia suggests that it is a stable feature in each group, not likely to be labile or to show transitions. The division between radially symmetrical and zygomorphic taxa is a sharp one in which it is difficult to imagine a flower combining these two markedly different pathways. A putative transition, down-turned styles (typical of the zygomorphic taxa) in the otherwise radially symmetrical flower of H. hermannifolia, was thought to be transitional by Stebbins and Hoogland (1976)
. This species certainly merits developmental study if and when material can be obtained. However, the inclination of the styles is a feature that is expressed late in development as the flower bud opens and may result from differing genetic controls from those that govern floral symmetry.
Evolutionary changes in stamen number in the genus Hibbertia have mostly tended toward increase, via at least four developmental shifts: increase in number within a "whorl," addition of more primordia basipetally (centrifugally), or by the innovations of either a ring meristem or common primordia. By "whorl" we mean here a circle of stamen primordia initiated at approximately the same level on the flanks of the floral apex. The stamen positions later become somewhat reoriented, so that whorls are not evident at anthesis. The flowers with few stamens result where there is a single "whorl" with relatively few primordia, or where common primordia are present but show limited proliferation.
High stamen numbers may result first where the stamen number increases over time within each "whorl" or by additional initiations centrifugally (as in H. perfoliata and H. scandens), enabled by marked increase in apical meristem surface during stamen initiation. Additional stamen primordia are four to five rows deep radially in H. perfoliata and up to seven rows deep in H. scandens. The difference developmentally is the amount of available meristematic surface for new initiations (which is probably a function of meristem duration over time), and also whether the initiatory activity is evenly distributed. In the ring meristem in H. scandens, initiations occur uniformly around the periphery, while in H. perfoliata, initiatory activity is concentrated in five areas, the common primordia. The ring meristem in Adrastaea salicifolia has a very limited duration, producing only five stamen primordia. All of these modes of stamen-number increase occur early (during organogeny) and hence tend to be stable as patterns of development.
Stamen number increases in many species of Hibbertia by the innovation of common primordia. Five meristematic mounds form on the flanks of the floral apex, alternately with petals. On each mound (or common primordium) a succession of stamen primordia is formed. The total number depends on whether three or five common primordia are active, and the duration of primordial initiation activity in each. This innovation can produce a 20–35-staminate flower in H. huegelii or a 100-stamen flower in H. grossulariifolia (latter based on Payer, 1857)
.
The two differing populations of H. fasciculata may be an example of stamen-number evolution in progress. The Victoria populations have seven to nine stamens in three fascicles per flower. The New South Wales populations have three-staminate flowers in which each stamen has a broad base resembling that derived from a common primordium. Further developmental studies are planned for this species. Common primordia are the most versatile innovation in evolution of the Hibbertia androecium.
While the mode of stamen-number increase is stable among Hibbertia species, the actual number may be labile. The genus abounds in species that differ in number of stamens, and number can increase simply by extending the time of meristematic activity of the floral apex. As centrifugally initiated stamen primordia are the last organs to initiate, increasing their number does not affect subsequent organogeny.
Carpel number also has undergone evolution in Hibbertia, although the range (1–10) is narrower than for stamens and is closely related to floral symmetry and stable evolutionarily. Radially symmetrical flowers have three, five, or rarely up to ten carpels, depending on the species, while zygomorphic taxa generally have two. (In New Caledonia, all Hibbertia species have radially symmetrical flowers, and two carpels per flower.) The carpels are initiated simultaneously in each flower. In H. grossulariifolia with up to ten carpels, they appear to initiate in two whorls in acropetal succession (based on Payer, 1857; no developmental material was available to us).
The innovation of fusion among stamens is most evident in Adrastaea salicifolia, a segregate genus sometimes placed in Hibbertia. The outer five stamens, which result from a ring meristem, remain basally connate during their enlargement. The filaments also are connate in stamen fascicles resulting from common primordia. Fusion thus is another character that results from events early in ontogeny, and one that is stable and resistant to change. No fusion occurs among stamens that are initiated directly on the floral apex.
Key characteristics of Hibbertia flowers that are first expressed late in ontogeny and that are relatively labile include staminodial occurrence and the type of anther dehiscence. Staminodia (defined here as sterile organs in stamen positions) are said to occur commonly in sections Hibbertia (with radial flowers) and Hemistemma (with zygomorphic flowers). However, one of us (P. B.) with considerable field experience observing Hibbertia flowers reports often finding occasional staminodia even in species reported to lack them (e.g., H. racemosa, H. saligna). Developmentally, staminodia are usually in the last-initiated stamen sites; for example, a few may be found around the periphery of the androecium in H. scandens. Staminodia may be initiated after the majority of stamen primordia in the flower have undergone microsporogenesis and gametogenesis. Staminodial presence, although it has been used as a sectional distinction in Hibbertia, is probably more variable and labile than has been realized, and has questionable significance evolutionarily.
Another relatively labile key character is the type of stamen anther dehiscence, which can be either lateral (a full-length slit) or porose/poricidal (a subterminal pore or slit). Our SEM (scanning electron microscopy) examinations of anther dehiscence in Hibbertia (Tucker, unpublished data) show a lateral suture line in anthers of all species; none have the bordered pores seen in some other plant families (e.g., the legume Chamaecrista nictitans in Tucker, 1996a, 1997
). Dehiscence may occur uniformly throughout the length of the suture, or it may begin distally and proceed proximally until the entire slit is open. In poricidal anthers the initially distal dehiscence does not progress far down the anther. We found a developmental continuum over time in some species (H. dentata), beginning as poricidal and becoming full-length lateral dehiscence. The dehiscence process is obviously a late event in flower development, occurring usually as the flower opens or shortly thereafter. The anatomical particulars of the anther dehiscence process in Hibbertia have not been studied, but should prove worth investigating. The lack of sharp distinctions between the types of anther dehiscence suggests that the character may be too unstable to characterize sections.
Summarizing, floral symmetry, number and position of sepals and petals, mode of stamen and carpel initiation, position of organs, and centrifugal stamen organogeny are significant features in evolution in the genus Hibbertia. They are determined early in ontogeny and tend to be stable. But stamen number is highly variable among species in the genus, resulting from several alternative developmental pathways. Centrifugal order of stamen initiation, and the developmental innovations of the ring meristem and common primordia have contributed to high levels of speciation.
Evolutionary relationships among sections of Hibbertia
In Baillon's day (1871)
, the genus Hibbertia included taxa with flowers having indefinite numbers of stamens and free carpels, while Candollea included taxa with definite numbers of stamens, often in fascicles. The two are currently combined under Hibbertia sensu lato. Strong dissimilarities such as those in floral symmetry have generally not been considered sufficient to separate the genus; supposed "intermediates" between actinomorphic and zygomorphic symmetry (Baillon, 1871
; Stebbins and Hoogland, 1976
) have been used as evidence to maintain the genus. Our developmental evidence supports a separation of two entities that differ in floral symmetry, because the zygomorphic species of sections Hemistemma and Pleurandra have markedly different floral organogeny from those with radially organized flowers. The latter group includes species with free stamens (section Hibbertia) and those with stamen fascicles (section Candollea). Recently, Horn and Manos (1999)
have reported two major clades in the genus, based on molecular evidence that is correlated strongly with floral symmetry.
Does Adrastaea deserve generic status?
Adrastaea salicifolia has some unique developmental features: a ring meristem that produces only five stamens, the obdiplostemonous arrangement of the outer stamens, and strongly reflexed anthers of the outer stamens. But it shares most other aspects of the floral developmental pathway with radially symmetrical Australian Hibbertias: solitary floral position, pentamerous alternating whorls in calyx and corolla, helical order of initiation of the sepals and petals, the whorled arrangement of the first stamens and the carpels, and centrifugal order among additional stamens. Androecium development differs widely in Hibbertia and could easily include the features found in Adrastaea. The developmental pathway of the radially symmetrical species of Hibbertia is much more similar to that of Adrastaea than it is to zygomorphic species of Hibbertia. On developmental evidence, Adrastaea appears undeserving of separate generic status.
Pollination in Hibbertia
Variation in the diversity of pollen vectors and their activity depends primarily on four interrelated morphological characters: (1) whether anther dehiscence is longitudinal or poricidal; (2) whether the androecium forms at least one complete whorl of fertile stamens; (3) whether there are 40 stamens or more per flower; and (4) whether the gynoecium contains fewer than three carpels and the styles are straight and erect or curved and laterally extended at anthesis. The androecium is at least as important in controlling pollinator activity (Bernhardt, 1996
) as the perianth, which receives much more notice from pollination investigators. In Hibbertia, androecial characters control pollinator activity (Bernhardt, 1996
), just as perianth characters control the movement of pollinators in flowers with zygomorphic or tubular corollas.
Hibbertia species are pollinated primarily by female pollen-collecting bees (Apidae s. l., Colletidae, and Halictidae) and pollen-eating flies in the family Syrphidae (Bernhardt, 1996
, unpublished data). Bees are far more significant pollinators of Hibbertia species than beetles (Keighery, 1975
; Armstrong, 1979
). While the same bee taxon pollinates several Hibbertia species, androecium morphology predetermines different sites for pollen deposition on the bee's body. Different bees also forage differently, based on variation in mouthparts, vestiture, and physical size. Accordingly, four pollinator syndromes have been detected by the second author among species of Hibbertia; all are represented among the species studied here.
Pollination of the larger-flowered radially symmetrical species of Hibbertia such as H. scandens, with up to 200 stamens that conceal the ovaries, poricidal anther dehiscence, and erect, ascending styles, is effected by thoracic vibration by large bees 7–22 mm long (Halictidae and large-bodied anthophorine bees in the Apidae). The bees circle the center of the flower, clasping groups of stamens at different points and vibrating them to release the pollen (Buchmann, 1983
; Bernhardt, 1996
; Endress, 1997
).
In the H. fasciculata pollination syndrome (Bernhardt, 1986
), flowers have radial symmetry, a single whorl of 8–12 stamens that conceal the three ovaries with bent styles outside the anther tuft, and poricidal anthers. Bees 7 mm long or larger (Anthophoridae, Colletidae, and Halictidae) clasp the whole tuft of fertile anthers, apply thoracic vibration, and spin around the androecium, collecting pollen while the stigmas contact the underside of the pollen-storing abdomen. This syndrome is represented by H. huegelii, H. racemosa, H. saligna, and H. cuneiformis among species in our study.
Species of Hibbertia with longitudinally dehiscent anthers, radial symmetry, two or more whorls of over 100 stamens that conceal the three ovaries, and erect styles (e.g., H. dentata; see Bernhardt, 1996
) are pollinated primarily by small-bodied bees (4–7 mm) and by large syrphids. The insects crawl over the protruding stigmas as they forage directly on the exposed, extruded pollen. This pollination syndrome prevails in H. dentata and H. grossulariifolia among the species studied here.
In zygomorphic flowers of Hibbertia in sections Hemistemma and Pleurandra (e.g., H. stricta—Bernhardt, 1984
), stamens are aggregated on one side of the flower, and the styles of the two carpels curve upward with stigmas parallel on either side of the bundle of stamens. Hibbertia banksii, H. empetrifolia, and H. hypericoides in our study represent this syndrome. Bees 7–22 mm long hang longitudinally or inverted from the flower while clutching the anthers and apply thoracic vibration to extract the pollen. The stigmas of the two upcurving styles contact the bee's abdomen.
With the exception of Trigona and introduced Apis (both in Apidae sensu stricto) bearing true corbiculae, and some colletids (Hylaeus) that collect pollen by swallowing and regurgitating grains, all native Australian bees carry deposits of pollen on scopal hairs on their hind legs and at the base of the abdomen. Pollen grains are packed in scopae without using nectar as a pollen mortar. The way in which a bee's hindlegs or hairy abdomen transfer loosely collected pollen from a porose anther to a stigma depends ultimately on stamen number in the flower, androecial architecture, and the angle of the styles. The significance of organographic distinctions among Hibbertia species remains enigmatic until they are interpreted in the light of function at anthesis. We are still only beginning to understand floral function in Hibbertia. Insect behavior in species of Hibbertia will be explored in more detail in a second paper.
Developmental comparison with other Dilleniaceae
Systematic treatments of Dilleniaceae include those by Gilg and Werdermann (1925)
, Hutchinson (1964)
, and Hoogland (1952
, for Dillenia). The family Dilleniaceae was viewed as relatively primitive, a southern-hemisphere equivalent to Magnoliidae (Cronquist, 1981
) on the basis of many of the same characteristics as Magnoliidae: scalariform vessels; perfect, hypogynous actinomerous flowers; numerous stamens; essentially apocarpous gynoecium with conduplicate carpels not completely sealed; ovules bitegmic and crassinucellar. However, taxa of Dilleniaceae differ from Magnoliidae in the centrifugal direction of organ initiation in the androecium. The significance of this organogenetic distinction between Dilleniaceae and Magnoliidae and Rosiidae has been judged highly significant by Sattler (1972)
, Tucker (1972)
, and Cronquist (1981)
. Taxa of Dilleniaceae also differ chemically; they have ellagic acid, proanthocyanins, and raphide crystals (none of which are found in Magnoliidae), and they lack alkaloids and ethereal oils that are present in Magnoliidae (Kubitski, 1968
; Cronquist, 1981
; Gurni and Kubitski, 1981
).
Dilleniaceae currently are considered to have little relationship to Magnoliidae and, instead, are allied to Rosidae, based on a large-scale cladistic analysis by Chase et al. (1993)
. It is the sister group in this analysis to an assemblage of Caryophyllidae. No detailed cladistic analysis within Dilleniaceae has been done, although Horn and Manos (1999)
are working on a much-needed molecular analysis.
Radial floral symmetry occurs in all genera in the family; zygomorphy occurs only in Hibbertia pro parte. Some species of Dillenia have as many as 700 stamens per flower; the flowers are much larger than even the largest in Hibbertia. Heteranthery is found in some species of Dillenia (with short feeder stamens and long pollination stamens as well as staminodia), and in some New Caledonian species of Hibbertia (with both lanceolate and falcate anthers). Organogeny is similar between Dillenia species described by Endress (1997)
and Hibbertia scandens, with its 200 stamens per flower, helical acropetal initiation of five sepals and five petals, then a ring of eight stamen primordia, and lastly a ring of seven or eight carpel primordia. After the first stamen whorl, other stamens are initiated in a centrifugal direction on a ring meristem. The outermost stamen primordia become staminodia, as in Hibbertia banksii. Poricidal anthers and punctiform stigmas in Dillenia also resemble those of species of Hibbertia. Dillenia differs from most species of Hibbertia in heteranthery, in more numerous carpels and styles (usually eight vs. two to five in most species of Hibbertia), and in its syncarpous ovary. Hibbertia is essentially apocarpous, although Dickison (1968)
mentioned some basal coalescence of ovaries. Styles in Dillenia are broad and flat and are disposed in a flat rosette over the top of the reflexed anthers of the androecium (Endress, 1997
); neither of these characters are found in Hibbertia. While Hibbertia has staminodia as well as fertile stamens, all the latter are alike in any one Australian species, unlike the heteranthery among functional stamens in Dillenia (Endress, 1997
).
Centrifugal order of stamen initiation and frequent occurrence of staminodia toward the outside of the androecium as the last-initiated primordia appear to be common developmental features among taxa of Dilleniaceae that have been studied (Endress, 1997
). A ring meristem producing stamens occurs in all genera but is not universal in Hibbertia, in which other mechanisms for stamen-number increase also have arisen during evolution. Summarizing, Hibbertia includes most of the character states responsible for familial diversity among other dilleniaceous genera that have been investigated developmentally.
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FOOTNOTES |
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3 Author for reprint requests.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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