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. 2006 Sep;98(3):619–630. doi: 10.1093/aob/mcl138

The Floral Scales in Hellmuthia (Cyperaceae, Cyperoideae) and Paramapania (Cyperaceae, Mapanioideae): An Ontogenetic Study

A VRIJDAGHS 1,*, P GOETGHEBEUR 2, E SMETS 3, A M MUASYA 4
PMCID: PMC2803571  PMID: 16807256

Abstract

• Background and Aims In 1976 the monotypic genus Hellmuthia was placed in the Hypolytreae s.l., but was subsequently ascribed to the Mapanioideae, tribe Chrysitricheae, mainly because of the presence in Hellmuthia of two lateral, mapanioid-like floral scales with ciliated keels, the anatomy of the nutlet, the embryo and the inflorescence. Recently, based on cladistic analyses and supported by pollen ontogenetic evidence, Hellmuthia was transferred to a Cyperaceae, tribe Cypereae, clade mainly consisting of Ficinia and Isolepis. In this study, the floral ontogeny in Hellmuthia was investigated and compared with the floral ontogeny in Paramapania, with special attention for the floral scales.

• Methods Freshly collected inflorescences of Hellmuthia membranacea and Paramapania parvibractea were investigated using scanning electron and light microscopy.

• Key Results In the conical ‘spikelet’ in Hellmuthia, proximal bracts occur, each axillating an axis with empty glume-like structures, or a reduced spikelet. Hence, it is a reduced partial inflorescence. In Hellmuthia, the stamen primordia originate before the primordia of the perianth–gynoecium appear. Moreover, a third adaxially positioned ‘floral scale’ was observed for the first time. The position and relative time of appearance of the floral scales in Hellmuthia are typical for perianth parts in Cyperoideae. The basal position of Hellmuthia within a clade of species with usually perianthless flowers, allows the presence of rudiments of a perianth in Hellmuthia to be interpreted as a primitive state. Development of the lateral ‘scales’ in Paramapania follows a different pattern. Therefore, it was decided that the lateral ‘scales’ in Paramapania are different from the lateral perianth parts in Hellmuthia. The pollen grains in Hellmuthia are cyperoid, with one polar and five lateral apertures, of which the membrane is covered with sexinous bodies. The pollen surface is granulate and perforate with microspines.

• Conclusions The floral ontogeny in Hellmuthia occurs according to the general cyperoid pattern. The lateral scales in Hellmuthia are perianth parts, and they are not homologous to the lateral ‘scales’ in Paramapania.

Keywords: Floral scales, Paramapania, floral ontogeny, Cyperaceae, Hellmuthia, SEM, homology

INTRODUCTION

According to the molecular phylogenetic studies of Simpson et al. (2006; see Table 1), the Cyperaceae can be subdivided into two subfamilies, the Mapanioideae and the Cyperoideae (Table 1). Morphologically, the Mapanioideae are characterized by a particular ‘flower’, also called ‘spicoids’. The term ‘spicoid’ refers to a synanthial interpretation of the inflorescence unit, opposite to the use of the term ‘flower’. A typical ‘spicoid’ (e.g. Kukkonen, 1984) or ‘flower’ (e.g. Goetghebeur, 1998) is subtended by a large glume-like bract, which envelops most of the reproductive unit. The ‘flower’ consists of a very short and contracted central axis, several spirally placed scales subtending a stamen (or not), and a terminal pistil. The two proximal scales are keeled, opposite to each other and larger than the other scales, each subtending or opposite to a stamen (or not) (Kukkonen, 1984; Goetghebeur, 1986). In the Cyperoideae, a flower is trimerously built, tetracyclic with two whorls of each three perianth parts, one whorl of three stamens, and a trimerous gynoecium. In many genera, there is a tendency to reduce the number of floral parts or modify them (Vrijdaghs et al., 2004, 2005a, b).

Table 1.

Suprageneric classification of Cyperaceae

Goetghebeur (1998) Simpson et al. (2006)
Subfamily Mapanioideae Subfamily Mapanioideae
    1. Hypolytreae     1. Hypolytreae
    2. Chrysitricheae (+ Hellmuthia)     2. Chrysitricheae
Subfamily Cyperoideae Subfamily Cyperoideae
    1. Cypereae     1. Cypereae (+ Hellmuthia)
    2. Fuireneae     2. Fuireneae
    3. Eleocharideae     3. Eleocharideae
    4. Abildgaardieae     4. Abildgaardieae
    5. Scirpeae     5. Scirpeae
    6. Dulichieae     6. Dulichieae
    7. Schoeneae     7. Schoeneae
Subfamily Sclerioideae     8. Cryptangieae
    1. Cryptangieae     9. Trilepideae
    2. Trilepideae     10. Sclerieae
    3. Sclerieae     11. Bisboeckelereae
    4. Bisboeckelereae     12. Cariceae
Subfamily Caricoideae
    1. Cariceae
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The taxon, initally described as Scirpus membranaceus by Thunberg (1794), has been treated as a member of a number of several distinct genera depending on the interpretation of the floral characters. The species was transferred to Isolepis (Nees von Esenbeck, 1835), Ficinia (Kunth, 1837), and independently, the same plant was placed by Steudel (1855) in a new genus named after his son, Hellmuthia: ‘genus in nomine filii Hellmuth Steudel dixi’. The genus Hellmuthia consisted of one species H. restoides, because of its ressembance with the Restionaceae (Steudel, 1855).

In 1898, Clarke used the name Scirpus membranaceus Thunb. for the current Hellmuthia membranacea, arguing that it belongs to Scirpus: ‘I regard the squamellae here present as analogous to the broad scale-like hypogynous setae sometimes developed in Scirpus littoralis Schrad … the species seems to me a Eu-Scirpus, near S. littoralis Schrad., rather than an Isolepis.’ (see Fig. 8A, after Clarke, 1909). Schönland (1922) mentioned that the lateral scales (Clarke's squamellae) were often called ‘prophylls’, though not fully approving this view: ‘...the view is gaining ground that all lateral cyperaceous flowers are without prophylls, whereas these are a constant feature in Graminaceae. Structures which most botanists would consider as prophylls,…,are also occasionally found in Scirpus membranaceus Thunb. and Ficinia ixioides Nees.’ (Schönland, 1922, p. 12).

In 1976, Haines and Lye changed Scirpus membranaceus into Hellmuthia membranacea, belonging to the monotypic genus Hellmuthia, and they transferred Hellmuthia to the Hypolytreae s.l., tribe Mapaniineae. The spikelet and flower in Hellmuthia was described as a cone with a wide prophyll at its base and numerous imbricate membranous scales, each subtending a single, bisexual flower. Distinction was made between ‘lower’ and ‘upper flowers’, the lower ones having a membranous ‘perianth’. Haines and Lye (1976) did not describe a perianth, but a drawing of a flower and a floral diagram showed two lateral scales enclosing the two lateral-adaxial stamens (Haines and Lye, 1976, fig. 1G and I, p. 62). In the captions of the figure, the ‘flower’ is called spikelet, though in the description the term ‘flower’ is used. Goetghebeur (1998) used unambiguously the term ‘flower’, and ‘floral scales’, and he classified Hellmuthia within his subfamily Mapanioideae, tribe Chrysitricheae (Table 1), mentioning that the taxonomic position of the genus is controversial. About the lateral scales, Haines and Lye (1976, p. 66) wrote: ‘... They bear no resemblance to the true perianth members found in other species of Scirpus s. lat. They can, however, be matched precisely, particularly as regards the ciliation of the keels, in the inflorescences of the Mapanieae.’ According to Haines and Lye (1976), as well as Goetghebeur (1986), only the more distally positioned flowers without lateral scales form fruits. The lateral scales with ciliated keels within the flower, as well as the anatomy of the fruit, were for Haines and Lye (1976) decisive arguments to revalidate the genus Hellmuthia and classify it in the Mapanioideae. Hellmuthia was used by Holttum (1948) and Schultze-Motel (1959) as an argument in favour of their synanthial hypothesis. More recently, however, based on a combined morphological and molecular analysis, Muasya et al. (2000) suggested Hellmuthia to be phylogenetically closer to Ficinia, Isolepis and Scirpoides. Eventually, Hellmuthia has been classified in the Cyperoideae tribe Cypereae, in the Ficinia–Isolepis clade (Simpson et al., 2003, 2006; Muasya et al., 2006). Table 1 summarizes the suprageneric phylogenetic hypotheses of Goetghebeur (1998) and Simpson et al. (in press), which are used in this study. The global floral ontogenetic pattern in Hellmuthia was examined, comparing it with the ontogenetic pattern in the reproductive unit of Paramapania, and with the recently published (Richards et al., 2006) floral ontogenetic data in Exocarya (Mapanioideae), with special attention for the two lateral ‘floral scales’. In addition, some pollen morphological data in Hellmuthia are presented.

Fig. 1.

Fig. 1.

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Floral ontogeny in Hellmuthia membranacea. (A) Apical view of the rachilla apex and flower primordia in successive stages of development (1–6). The glumes of stages 4 and 6 are fused. (B) Lateral view of the rachilla apex with two flower primordia with fused glumes (marked). (C) Glume primordium with the floral primordium appearing in its axil. (D) Early flower primordium. (E) Two floral primordia at successive stages of development. The oldest flower primordium (right-hand side) expands laterally. (F) Flower primordium with two lateral stamen primordia and developing flower apex (arrowed). (G, H) The flower apex differentiates into a ovary primordium surrounding a central ovule. In (G), the abaxial stamen primordium is appearing (arrowed). (I) Two lateral and one abaxial stigma primordia originate on the top of the ovary wall. (J) Lateral-abaxial view of a developing flower. The abaxial and opposite lateral stamen have been removed. Anther and filament become visible. The ovary wall encloses the central ovule, and the stigma primordia are growing out. *, rachilla apex. Abbreviations: a, anther; f, filament; F, flower primordium; G, glume (primordium); o, ovule (primordium); ov, ovary (primordium); s, stamen (primordium); sg, stigma.

MATERIALS AND METHODS

Partial inflorescences of Hellmuthia membranacea were collected in South Africa by A. M. Muasya (voucher 2792, KUL) and Byetebier (voucher 2645, STELL), in June–July 2005 and fixed in FAA (70 % ethanol, acetic acid, 40 % formaldehyde; 90 : 5 : 5). Partial inflorescences of Paramapania parvibractea (Clarke) Uittien were collected by Reynders and Sabulao (voucher 32, UG) on Samar Island, Philippines in January 2006. Floral buds were dissected in 70 % ethanol under a Wild M3 stereo microscope (Leica Microsystems AG, Wetzlar, Germany) equipped with a cold-light source (Schott KL1500; Schott-Fostec LLC, Auburn, NY, USA).

The material was washed twice with 70 % ethanol for 5 min and then placed in a mixture (1 : 1) of 70 % ethanol and DMM (dimethoxymethane) for 5 min. Subsequently, the material was transferred to 100 % DMM for 20 min, before it was critical point dried using liquid CO2 with a CPD 030 critical point dryer (BAL-TEC AG, Balzers, Liechtenstein). The dried samples were mounted on aluminium stubs using Leit-C and coated with gold with a SPI-Module™ Sputter Coater (SPI Supplies, West-Chester, PA, USA). Scanning electron microscope (SEM) images were obtained with a JEOL JSM-6360 (JEOL Ltd, Tokyo) at the Laboratory of Plant Systematics (K.U.Leuven).

For light microscopic (LM) observations, semi-mature spikelets of Hellmuthia membranacea were dehydrated through a t-butyl alcohol series to be embedded in paraffin. Transverse and longitudinal serial sections (Microm HM360) were cut at 12 µm and stained with saffranin in 70 % ethanol and anilin blue in an automatic staining machine Varistain 24-3 (Shandon, Runcorn, UK) and were mounted with Eukitt. LM images were observed with a Leitz Dialux 20 microscope (Germany) and digital photographs were made with an Olympus DP50 camera (Germany).

RESULTS

The conical ‘spikelet’ in Hellmuthia is indeterminate, with spirally placed glumes, each subtending a bisexual flower (Fig. 1A). Proximally, bracts axillating lateral axes with empty glume-like structures, or rudimentary spikelets with glumes axillating floral primordia (Fig. 4E), occur. At early stages, glumes subtending neighbouring flowers may be fused (Fig. 1B). In the axil of the glume, a floral primordium originates (Fig. 1C, D), which expands laterally, forming two stamen primordia (Fig. 1E–G). Meanwhile, a floral apex becomes apparent as a bulge. Next, the floral apex differentiates into an annular ovary primordium surrounding a central ovule primordium (Fig. 1H). Simultaneously, the abaxial stamen primordium originates (Fig. 1H). The ovary primordium rises, and on the top of it two lateral and one abaxial stigma primordium are formed (Fig. 1I). Subsequently, the ovary wall envelops the central ovule, and the stigma primordia grow out (Figs 1 J and 2A, B). Simultaneously, each stamen primordium develops into a filament and a basifixed and introrse anther (Figs 1 J, 2A–E and 5A). In proximal flowers, opposite the lateral stamens, a scale-like structure is formed (Fig. 2C–G), which appears only after the formation of the stamens (Fig. 2C). At later stages, the scale-like structures obtain ciliated margins and keels, each one enveloping a filament (Fig. 2F, G). Meanwhile, a short single style and three papillose stigma branches are formed (Figs 2H and 3C, D, G, H). At semi-maturity, the relatively short style shows spiny protuberances, consisting of four cells, one more elongated cell, two spherical cells, and an antrorsely protruding spine (Fig. 3I). In the stamens, first the anthers elongate. Antrorse spine-like cells protrude from the distal part of the anther and a spiny apiculus has been formed (Figs 2H and 4B). Next, the filaments elongate and become flattened (Fig. 3E–G), continuing in a broad connective (Figs 3E and 4A). The base of each pollen sac is prolonged proximally (Fig. 4A), and on the top of each anther a spiny apiculus is formed (Figs 2D and 4B). In the proximal half of the spikelet, in between the larger glumes, small, membranous glumes are present (Fig. 3A), subtending (or not) each a reduced flower (Figs 3B and 4C). The margin of such a small glume is partially ciliated (Figs 3A, B and 4C). The large glumes are very wide (Figs 3C, D and 4D) with lateral wings that at later stages fold back (Figs 3C and 4D).At maturity, the lateral wings might separate from the main body of the glume (Fig. 3G). The margins of the wings and the apex of the mature glume are ciliated (Fig. 4D). In many proximally situated, (semi-)mature flowers, the ovary appears to protrude out of the conical ‘rachilla’, having a curved shape (Figs 2F–H and 5D).Lateral scales do not occur in more distally situated flowers (Fig. 5A, B), whereas in the proximal part of the spikelet flowers with lateral scales are present (Fig. 5C, D).In a more basal transverse section of flowers with lateral scales, a third, adaxial scale can also be present (Fig. 5E, F). Hellmuthia pollen grains have six apertures, five equatorial, and a polar one (Fig. 6A–D). Critical point-dried (partially collapsed) pollen grains are bullet-shaped with an average length of 37 µm and diameter of 20 µm (Fig. 6C). The surface is granulate with microspines, and perforate (Fig. 6E). Each aperture membrane is covered with sexinous bodies (Fig. 5D, G) showing the same ornamentation and microspines as the sexine. The tapetum wall is covered with irregularly shaped aggregated (or free) orbicules with connecting threads (Fig. 6F). The orbicules tend to have the same ornamentation as the sexinous bodies (Fig. 6E–G).

Fig. 2.

Fig. 2.

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Floral ontogeny in Hellmuthia membranacea. (A) Adaxial view of a developing (distally positioned) flower, with the anthers appearing, the ovary wall enveloping the central ovule, and the stigma primordia starting to grow out. (B) Adaxial view of a successive developmental stage of a (distally positioned in the spikelet) flower. (C) Lateral-abaxial view of a developing (proximally positioned in the ‘spikelet’) flower. Connective crests appear on the tops of the anthers. At the base of the lateral stamen, a primordium of a lateral perianth part originates (arrowed). (D) Abaxial-lateral view of a developing flower with a lateral stamen. Opposite it, a scale-shaped perianth part is developing (arrowed). (E) Detail of a lateral perianth part. (F) Adaxial view of a developing flower. The anthers rise high above the still underdeveloped gynoecium. The lateral perianth parts (‘scales’) show their typical morphology with ciliated keels. (G) Adaxial view of a developing flower with well-developed lateral perianth parts. At the adaxial base of the gynoecium, a rudiment of an adaxial perianth part is visible (arrowed). (H) Semi-mature gynoecium and stamen. The stigma branches are becoming papillose. Antrorse spine-like cells protrude at the distal part of the anther. Abbreviations: a, anther; ap, apiculus; f, filament; o, ovule (primordium); ov, ovary; pp, perianth part; sg, stigma; st, style.

Fig. 3.

Fig. 3.

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Floral ontogeny in Hellmuthia membranacea. (A) Adaxial view of a nearly mature flower and a small glume (Gs) with ciliated margin (arrowed). (B) Small glume with a reduced flower (arrowed). (C) Adaxial view of a semi-mature flower and its subtending glume, with two lateral wings (Gw) and ciliated distal margins and keel (arrowed). (D) Adaxial view of a nearly mature flower. A ribbon-shaped single style with three ribbon-shaped, papillose stigmatic branches are formed. Anthers and filament are elongating. The ovary wall shows a typical texture. (E) Abaxial view of a semi-mature flower. (F) Detail of a mature ovary and style (with spiny antrorse epidermal protuberances) from the adaxial side. The filaments are elongated. At the base of the ovary, there is a rudimentary hypogynous stalk. (G) Mature flower, adaxial side. The wings of the glume tend to tear off (arrowed). (H) Detail of the stigmas. (I) Detail of the spiny epidermal protuberances of the style (arrowed). Abbreviations: a, anther; f, filament; G, glume; Gs, small glume; Gw, wing of a glume; ov, ovary; sg, stigma; st, style.

Fig. 4.

Fig. 4.

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Floral ontogeny in Hellmuthia membranacea. (A) Detail of the base of an anther in a developing stamen. The base of each pollen sac is prolonged proximally (arrowed). A broad connective can be observed in between the pollen sacs. The filament is wide and ribbon-shaped. (B) Detail of the connective crest (apiculus) on the top of a developing anther. (C) Small glume (Gs) with ciliated margin, subtending a reduced flower (arrowed). (D) Flower subtending glume with ciliated distal parts of the margins and glume apex, and wings that fold back (arrowed). (E) ‘Spikelet’ with developing early floral primordia (arrowed), removed from its subtending glume-like bract in the proximal part of a conical ‘spikelet’. Abbreviations: Ap, piculus; co, connective; f, filament; Gs, small glume; ps, pollen sac.

Fig. 5.

Fig. 5.

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Images of transverse LM sections through the ‘spikelet’ of Hellmuthia membranacea. (A) Section through a flower at the more distal part of a ‘spikelet’. (B) Section through the distal part of a ‘spikelet’. In ‘1’ and ‘2’ a transverse section through the basal part of the floral primordium shows three stamen primordia around the floral axis. Floral primordium ‘2’ is older and the section through it is higher. The tranverse section through flower ‘3’ is made at the transition between the just formed filament and anther. In the centre of the flower the ovary wall surrounding the central ovule primordium is visible. The glumes (G1–G3) are imbricate. Glume ‘G1’ encloses a developing flower primordium as well as an undifferentiated primordial zone (arrowed). (C) Section at the height of the style of a developing flower and through the central part of the rachilla, with numerous, circulary positioned vessels (v). Opposite each lateral stamen there is a flat and plied perianth part (arrowed). (D) Section through the central part of the ovary of a developing flower, and through the filaments (f) of the lateral stamens and the anther of the abaxial stamen (a). The perianth part (pp) at the left-hand side is fused with a tissue (primordial adaxial perianth part) in between the adaxial side of the ovary and rachilla (arrowed). (E) Section through a developing flower, with two free lateral perianth parts and an adaxial perianth part fused with the more basal central ovary wall (arrowed). (F) Section at the height of the transition between style and stigma branches through a developing flower. Two lateral and a free adaxial perianth part are visible (arrowed). Abbreviations: a, anther; g, gynoecium; f, filament; G, glume; pp, perianth part; v, vessel.

Fig. 6.

Fig. 6.

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SEM images of critical point-dried pollen grains in Hellmuthia membranacea. (A) View of a group of pollen grains, seen from the polar side, each with a polar aperture (pa). (B) Lateral view of a pollen grain, with three lateral (la) and the polar apertures visible. (C) Lateral view of a pollen grain with two lateral apertures and the zone of the previous adhesion (arrowed) with the three deteriorated pollen grains. (D) Polar view of a pollen grain. (E) Detail of the the granulate, perforate pollen surface with microspines. (F) Tapetum covered with orbicules. (G) Detail of an aperture with sexinous bodies with microspines on its membrane. Abbreviations: pa, polar aperture; la, lateral (equatorial) aperture.

In Paramapania parvibractea, the two lateral scales originate and develop before other parts of the reproduction unit become visible (Fig. 7A). The scales elongate, enveloping the rest of the floral unit (Fig. 7B, C), and obtain the typical margins with spiny outgrows. At maturity, the lateral scales envelop the filaments of the stamens, and protect the inner part of the floral unit which consists of three inner scales and the gynoecium (Fig. 7D). Only the style and three short stigma branches protrude above the inner scales (Fig. 7D). The lateral scales are fixed at the floral apex neatly below the point of attachment of the filaments (Fig. 7E). The nutlet is terete, and projected on a plane, it shows an obovate shape. The surface is smooth to slightly wrinkled. The style base is persistent with the fruit (Fig. 7F).

Fig. 7.

Fig. 7.

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Floral ontogenetic stages in Paramapania parvibractea. (A) Apical view of a reproductive unit hidden by two lateral scales at an early developmental stage. (B) Adaxial view of a subtending glume-like bract with developing lateral scales, which, at this stage, envelop the entire reproductive unit. (C) Successive developmental stage. The distal part of the margins of the lateral scales becomes ciliated. (D) Mature flower with the two massive lateral scales, abaxial view. (E) Mature flower, the lateral scales have been removed. The lateral scales are attached below the point of attachment of the filaments (arrowed). (F) Beaked nutlet. Abbreviations: f, filament; GB, glume-like bract; isc, inner scale; lsc, lateral scale; sg, stigma; st, style.

DISCUSSION

The conical ‘spikelet’ in Hellmuthia is considered to be a reduced partial inflorescence, because of the presence of proximal bracts subtending reduced spikelets. These spikelets are sterile, or glumes subtending floral primordia (Fig. 4E) do occur. The floral ontogeny in Hellmuthia (Figs 1–5) follows the general floral ontogenetic pattern as it was observed in all Cyperoideae studied (Vrijdaghs et al., 2004, 2005a–c). There are, however, some particular features in its floral development and morphology, such as (a) fused glumes (Fig. 1A, B) at early developmental stages, (b) the membranous and partially ciliated small glumes subtending reduced flowers (Figs 3A, B and 4C), and (c) the extremely wide glumes with folding, ciliated wings at (semi-)mature stage (Figs 3C, D, G and 4D). These glume features might originate from initially fused glumes of which one part develops into a usual wide, winged glume subtending a well-developing flower, and the other part into a small membranous glume subtending a underdeveloped flower.

Most controversy on Hellmuthia was related to the presence of two lateral floral scales, which occur only in the proximal flowers (Figs 2F, G and 5C–F). Haines and Lye (1976) mentioned that the lateral scales might join adaxially below. The present observations show the existence of a third adaxial scale (Fig. 5F), which is basally connate with the two lateral scales (Fig. 5D, E). Scale-like perianth parts also occur in Fuirena, a genus in which a wide diversity of scale morphology and several reduction trends in the number of perianth parts can be observed (Muasya, 1998; Vrijdaghs et al., 2004; Muasya et al., 2006). In Fuirena, however, laminar perianth parts always belong to the inner whorl of the perianth. The lateral scale-like structures observed in Hellmuthia are positioned exactly where an outher perianth part could be expected (Fig. 2C, E), at the base of the filaments. In some flowers, situated in the proximal zone of the conical ‘spikelet’, a third, adaxial (and inner) perianth part occurs (Fig. 5F). Schönland (1922, p. 44) described a similar adaxial structure in Ficinia ixoides Nees: ‘Its most extraordinary character is the association with each flower of an adaxial, linear, obtuse, (often obtusely red) scale’. The adaxial scale-like structure, in H. membranacea (as well as in F. ixoides as illustrated by Schönland; Fig. 8B) has the position of an adaxial, inner perianth part (Fig. 5F). Basal fusion of perianth parts is not uncommon (Vrijdaghs et al., 2004, 2005a). The position and the relative time of appearance of the scale-like structures in Hellmuthia, after the formation and differentiation of the staminal primordia into filament and anther, which is later than in most other Cyperoideae observed by us (Vrijdaghs et al., 2006), supports the conclusion that they are homologous to perianth parts. Clarke (1897–98) had already suggested that the lateral scales are perianth members, a suggestion that is supported by the present results. The abaxial outer perianth part, as well as the two abaxial inner ones, are suppressed, which might be explained by the dorsoventral compression of the flowers due to the conical form of the ‘spikelet’ axis. The early development of the lateral scales resembles the ontogeny of the inner perianth parts in Fuirena.

Fig. 8.

Fig. 8.

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Reproductions of diagrams. (A) Drawing of a flower (adaxial view) of Hellmuthia membranacea, reproduced from Clarke (1909), plate XLVII,12. The lateral perianth parts are arrowed. (B) Drawing of a flower of Ficinia ixoides, reproduced from Schönland (1922), plate 44). The adaxial perianth part is arrowed. (C) Floral diagram of Mapania, reproduced from Goebel (1888), plate XIV, 14. The lateral ‘scales’ are arrowed.

The detailed floral ontogenetic results in Exocarya published by Richards et al. (2006), show a similar developmental sequence for the lateral scales as in Paramapania. Figures 14–21 of this publication show that the lateral scales in Exocarya are actually the very first ‘floral’ primordia to appear, followed by the lateral stamen primordia. The point of attachment of the lateral scales in Paramapania, neatly below the point of attachment of the filaments, suggests that the lateral scales do not belong to the reproductive unit. The developing lateral scales seem to envelop and protect the ‘floral apex’, without being part of it. The abaxial and adaxial scales in Exocarya, as shown by Richards et al. (2006), originate apparently at the same positions and relative time as perianth parts in a cyperoid flower. In Paramapania, the lateral scales also originate and develop before the appearance of any other structure on the ‘floral apex’. The two lateral scale primordia develop fast, enveloping the ‘floral apex’ (floral primordium?), on which the first (lateral) stamen primordia appear only when the lateral scales have already been well developed. This is a different floral ontogenetic sequence from the general scirpoid floral ontogenetic pattern observed by Vrijdaghs et al. 2006. Therefore, the lateral scales in Paramapania are not considered to be homologous with the lateral perianth parts in Hellmuthia.

The presence of antrorse, spiny cells on the style (Fig. 3F, H, I) and anthers (Fig. 2H) is peculiar. Since the style is deciduous (Haines and Lye, 1976, fig. 3A, p. 64; Goetghebeur, 1998), these hook-shaped epidermal protuberances directed distally cannot play a role in the distribution of the fruit. They might protect the plant inflorescence against herbivores. Pollen grains in Hellmuthia are medium sized compared with other Cyperoideae (Fig. 6A–D). They have a typical cyperoid morphology, mostly described as triangular to pear-shaped (e.g. Haines and Lye, 1983) or cuneiform (e.g. Goetghebeur, 1998; Wichelen et al., 1999) with six apertures. Many authors mention four apertures for pollen grains within the Cyperoideae and monoporate pollen within the Hypolytreae tribe (e.g. the Carex-like type and the Mapania type pollen in Haines and Lye, 1983). Pollen grains, however, differ in number of apertures as well as morphologically within the Cyperoideae and within the Mapanioideae sensu Simpson (2006) (e.g. Erdtman, 1966; Koyama, 1969; Fernandez, 1987; Bruhl, 1995). The authors' observations (unpublished) confirm that, within Cyperoideae, the number of apertures varies. In Haines and Lye (1983, p. 20), an SEM photograph of pollen in Fuirena is shown, with four equatorial and one polar aperture out of probably six apertures. The pollen surface in Hellmuthia is similar to a ‘Carex-type’ pollen surface. Simpson et al. (2003) showed that pollen grains in Hellmuthia are pseudomonads, like most pollen grains in Cyperoideae. Opposite the polar aperture (Fig. 6A) is the zone (Fig. 6B, C) where the three deteriorated cells of the former tetrad are present (Simpson, 2003). Following Simpson et al. (2003), the present observations confirm that the pollen morphology in Hellmuthia is cyperoid (Wichelen et al., 1999) and hence the conclusion is corroborated that Hellmuthia is better placed away from Mapanioideae, Chrysitriceae.

Muasya et al. (1998, 2000) suggested that Hellmuthia should not be maintained in the Chrysitricheae sensu Goetghebeur (1998) and that it should be placed closer to Ficinia, Isolepis and Scirpoides. The mature nutlet of Hellmuthia membranacea, as illustrated with a SEM image by Haines and Lye (1976, p. 64, fig. 3A), has a hypogynous stalk and its morphology resembles the typical Isolepis-type nutlet (Muasya and Simpson, 2002; Vrijdaghs et al., 2005c). Eventually, as a result of a cladistic analysis based on plastid DNA sequences, and pollen developmental evidence, Hellmuthia membranacea was placed in a Cypereae clade, sister to Ficinia gracilis (Muasya et al., 2006; Simpson et al., 2006). Cypereae have always been defined based on, among others, perianthless flowers (e.g. Goetghebeur, 1998). There are, however, indications that flowers with perianth parts do occur within the Cypereae (Muasya et al., 2006). The basal position of Hellmuthia in the Ficinia–Isolepis complex suggests that the tendency in this clade to reduce the number of perianth parts to zero has not yet been fully established. As has already been illustrated in Fuirena (Vrijdaghs et al., 2004), the absence or presence of perianth parts can no longer be used as a decisive character for the delimitation of genera or tribes.

It is concluded that (a) the ‘spikelet’ in Hellmuthia is actually a reduced partial inflorescence, (b) the third, adaxial ‘floral scale’ and the two lateral ones in some proximal flowers in ‘spikelets’ in Hellmuthia are perianth members, (c) the overall floral ontogeny in Hellmuthia occurs according to the cyperoid general floral ontogenetic model, (d) the lateral ‘floral scales’ in Hellmuthia are not homologous to the lateral ‘floral scales’ in Paramapania, (e) the present morphological results support the transfer, based on molecular data, of Hellmuthia to a Cypereae clade.

Acknowledgments

We thank Marc Reynders (Research Group Spermatophytes, University of Gent) for kindly providing Paramapania material and DENR-PAWB region 8, Tacloban city, Philippines for providing collection permits, Benny Byetebier (Stellenbosch University) for collecting Hellmuthia material, Anja Vandeperre for her most professional help with the LM preparations and drawings, and palynologists Dr Stefan Vinckier and Dr Suzy Huysmans (Laboratory of Plant Systematics, K.U.Leuven). This work was supported financially by research grants of the K.U.Leuven (0T/05/35) and the Fund for Scientific Research-Flanders (FWO-Vlaanderen, Belgium, G.0268·04). A. Muthama Muasya was a visiting postdoctoral fellow of the Fund for Scientific Research-Flanders (FWO-Vlaanderen, Belgium) and of the Research Fund of the K.U.Leuven.

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