AOBPreview originally published online on November 3, 2006
Annals of Botany 2007 99(1):131-139; doi:10.1093/aob/mcl231
Floral Anatomy of Paepalanthoideae (Eriocaulaceae, Poales) and their Nectariferous Structures
Departamento de Botânica, Instituto de Biociências, Universidade Estadual Paulista–UNESP, C.P. 199, Rio Claro, SP 13506-900, Brazil
* For correspondence. E-mail mm_rosa{at}hotmail.com
Received: 29 June 2006 Returned for revision: 9 August 2006 Accepted: 7 September 2006 Published electronically: 3 November 2006
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ABSTRACT |
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BACKGROUND AND AIMS: Eriocaulaceae (Poales) is currently divided in two subfamilies: Eriocauloideae, which comprises two genera and Paepalanthoideae, with nine genera. The floral anatomy of Actinocephalus polyanthus, Leiothrix fluitans, Paepalanthus chlorocephalus, P. flaccidus and Rondonanthus roraimae was studied here. The flowers of these species of Paepalanthoideae are unisexual, and form capitulum-type inflorescences. Staminate and pistillate flowers are randomly distributed in the capitulum and develop centripetally. This work aims to establish a floral nomenclature for the Eriocaulaceae to provide more information about the taxonomy and phylogeny of the family.
METHODS: Light microscopy, scanning electron microscopy and chemical tests were used to investigate the floral structures.
KEY RESULTS: Staminate and pistillate flowers are trimerous (except in P. flaccidus, which presents dimerous flowers), and the perianth of all species is differentiated into sepals and petals. Staminate flowers present an androecium with scale-like staminodes (not in R. roraimae) and fertile stamens, and nectariferous pistillodes. Pistillate flowers present scale-like staminodes (except for R. roraimae, which presents elongated and vascularized staminodes), and a gynoecium with a hollow style, ramified in stigmatic and nectariferous portions.
CONCLUSIONS: The scale-like staminodes present in the species of Paepalanthoideae indicate a probable reduction of the outer whorl of stamens present in species of Eriocauloideae. Among the Paepalanthoideae genera, Rondonanthus, which is probably basal, shows vascularized staminodes in their pistillate flowers. The occurrence of nectariferous pistillodes in staminate flowers and that of nectariferous portions of the style in pistillate flowers of Paepalanthoideae are emphasized as nectariferous structures in Eriocaulaceae.
Key words: Eriocaulaceae, Paepalanthoideae, nectariferous structures, staminodes, staminate flowers, pistillate flowers, floral anatomy, monocotyledons, Poales
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Eriocaulaceae is pantropically distributed but most of its species occur in the mountainous regions of South America, especially in Venezuela and in Brazil (Giulietti et al., 1995). In Brazil, the greatest concentration of species is found in the rocky outcrops (‘campos rupestres’) present at altitudes above 900 m, and closely associated with the Cadeia do Espinhaço that spans across the States of Minas Gerais and Bahia (Giulietti and Pirani, 1988).
This family is currently inserted in Poales (commelinids) sensu APG II (Angiosperm Phylogeny Group, 2003), and presents about 1200 species distributed in 11 genera, among which are Rondonanthus (Herzog, 1931) and Actinocephalus (Sano, 2004), that are still valid and included in the subfamily Paepalanthoideae after the classification proposed by Ruhland (1903). This author recognized two subfamilies and nine genera for Eriocaulaceae: Eriocauloideae, with Eriocaulon and Mesanthemum, which present petals with nectariferous glands, two staminal whorls and a gynoecium without appendages and with stigmas in the carinal position; and Paepalanthoideae, with Blastocaulon, Lachnocaulon, Leiothrix, Paepalanthus, Philodice, Syngonanthus and Tonina, which present petals without glands, one staminal whorl and a gynoecium with appendages in the carinal position and stigmas in the commissural position.
Most species of Eriocaulaceae present capituliform monoecious inflorescences, with staminate and pistillate flowers. Nevertheless, cases of dioecy are mentioned in the populations of some species and Rondonanthus flabelliformis presents monoclinous and staminate flowers on a same inflorescence (Giulietti and Hensold, 1990). Most Eriocaulaceae possess trimerous flowers, although dimerous flowers occur in some species of Eriocaulon, Leiothrix and Papepalanthus (Giulietti, 1997).
Data on the floral anatomy of Eriocaulaceae are restricted to Eriocaulon elichrysoides and Syngonanthus caulescens (Rosa and Scatena, 2003). These authors reported not only the occurrence of scale-like staminodes in the staminate flowers of Eriocaulaceae for the first time, but also the presence of nectar-producing structures in their staminate and pistillate flowers. The petal glands have been reported by several authors in the past (e.g. Cronquist, 1981) and the nectariferous appendages of the gynoecium have already been reported e.g. by Stützel (1998).
According to Linder and Rudall (2005), the presence of floral nectar is normally a good indicator of pollination by animals. In monocots, nectar is predominantly produced by septal nectaries (Smets et al., 2000; Rudall, 2002), structures rarely found among species of Poales. Although Bromeliaceae are characterized by the presence of flowers with septal nectaries (Böhme, 1988; Sajo et al., 2004), with regard to the other Poales, only Rapateaceae are reported to have ‘open septal nectaries’ in Spathanthus unilateralis (Venturelli and Bouman, 1988), and floral nectaries in Guacamaya, Kunhardtia and Schoenocephalium, which are pollinated by hummingbirds (Givnish et al., 1999, 2000).
According to the data available in the literature, the occurrence of gynoecium appendages in flowers of monocotyledons is only reported for Eriocaulaceae and Xyridaceae, families pointed out to be closely related in cladistic analyses of commelinids (Givnish et al., 1999; Chase et al., 2000; Bremer, 2002; Michelangeli et al., 2003).
In order to better understand the taxonomy and phylogeny of Eriocaulaceae (Poales), this work studied the floral anatomy of Actinocephalus polyanthus, Leiothrix fluitans, Paepalanthus chlorocephalus, P. flaccidus and Rondonanthus roraimae (Paepalanthoideae).
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MATERIALS AND METHODS |
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Capitula of Actinocephalus polyanthus (Bong.) Sano, Leiothrix fluitans (Mart.) Ruhland, Paepalanthus chlorocephalus Silveira and P. flaccidus (Bong.) Kunth at different stages of development were collected in rocky outcrops (‘campos rupestres’) of the Serra do Cipó, Minas Gerais, Brazil. The material was fixed in FAA 50 (Johansen, 1940), and stored in 70 % ethanol. The capitula of Rondonanthus roraimae (Oliv.) Herzog were obtained from herbarium materials collected in the table mountains (‘tepuis’) of Venezuela, boiled in water with a few drops of glycerin, and stored in 70 % ethanol.
For light microscopy (LM), material was dehydrated in a normal butyl alcohol series, embedded in historesin, and sectioned at 5–12 µm on a Reichert-Jung Model 2040 Microtome using glass knives. The sections were stained with periodic acid–Schiff's reagent (PAS reaction) and toluidine blue (Feder and O'Brien, 1968). Photomicrographs were taken using an Olympus BX 40 photomicroscope.
For scanning electron microscopy (SEM), flowers from the fixed capitula of A. polyanthus, L. fluitans, P. chlorocephalus and P. flaccidus were isolated, dehydrated in an ethanol series, critical-point dried using a MS 850 critical-point drier, coated with gold using a Desk II Denton Vacuum sputter coater, and examined using a Jeol JSM 5410 scanning electron microscope.
The chemical tests were performed to detect the presence of glucose and nectar in the floral structures. For the glucose test, the pistillodes of staminate flowers and apical portions of the style of pistillate flowers were isolated and placed separately in spot plates containing distilled water, which were later macerated with the help of a small metal stick. The extremities of small pieces of glucose enzymatic test strip (Lilly) were immersed in this maceration for 3 min.
For the nectar test, capitula of A. polyanthus, L. fluitans, P. chlorocephalus and P. flaccidus, whose involucral bracts had been removed, and staminate and pistillate flowers of R. roraimae were immersed in a 1:10 000 solution of neutral red for 20 min (Kearns and Inouye, 1993).
Voucher materials were deposited at the Herbarium of the Department of Botany, Universidade Estadual Paulista (HRCB): A. polyanthus (Scatena et al. 229; Scatena et al. 236; Scatena et al. 237); P. chlorocephalus (Coan et al. 4; Scatena et al. 238); L. fluitans (Rosa et al. 1; Rosa et al. 10); P. flaccidus (Scatena et al. 235; Scatena et al. 240). The duplicate of R. roraimae was deposited at the Herbarium of the Department of Botany, Universidade de São Paulo (SPF): R. roraimae (Huber and Alarcon 10526).
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RESULTS |
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The bisexual capitula of Actinocephalus polyanthus, Leiothrix fluitans (Fig. 1A), Paepalanthus chlorocephalus (Fig. 1B), P. flaccidus and Rondonanthus roraimae are surrounded by three to six series of sterile involucral bracts. The staminate and pistillate flowers of all species are randomly distributed in the capitulum, and develop in centripetal order. Flowers are trimerous in A. polyanthus, L. fluitans, P. chlorocephalus and R. roraimae, and dimerous in P. flaccidus.
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Staminate flowers
The staminate flowers of all species are pedicellate and present floral bracts (Fig. 1C, E and G). The calyx is gamosepalous (Fig. 1C and E). The corolla is gamopetalous in A. polyanthus, P. chlorocephalus and P. flaccidus (Fig. 1E), and dialypetalous in L. fluitans and R. roraimae (Fig. 1G).
All species present an isostemonous androecium, which consists of three scale-like staminodes and three fertile stamens in A. polyanthus, L. fluitans (Fig. 1D) and P. chlorocephalus; two scale-like staminodes and two fertile stamens in P. flaccidus (Fig. 1F); and three fertile stamens in R. roraimae (Fig. 1G). Filaments are adnate to the petal base (Fig. 2G, arrows), except in L. fluitans, where they are free, and in R. roraimae, where their inferior third is fused to the petal base.
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Since they are extremely tiny structures in the staminate flowers, the scale-like staminodes can only be observed using a light microscope. They are located in an alternate position to the functional stamens, as can be observed in L. fluitans (Fig. 2A, arrows), and only consists of an epidermis, whose two faces are very close together (Fig. 2A–C, arrow). The reduction of the vascular bundle almost reaches its basal region, as can be observed in P. chlorocephalus (Fig. 2C, arrowhead).
Since they produced positive results to the chemical tests carried out to detect the presence of glucose and nectar, the pistillodes of all species were called nectariferous pistillodes (Figs 1D, F and H, arrow, and 3A and B), following the terminology introduced by Rosa and Scatena (2003). Their size may differ (Fig. 1D, F and H), and their apical region is covered by an epidermis with papillose cells that secrete nectar. These cells are elongated in A. polyanthus (Fig. 3A, arrow), P. flaccidus and R. roraimae, and rounded in L. fluitans (Fig. 3B, arrow) and P. chlorocephalus.
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The sepals, petals and stamens of all species are vascularized by a single, extremely tiny collateral vascular bundle, consisting of one or two transport cells, as can be observed in P. chlorocephalus (Fig. 2G). This bundle is directly derived from the ramifications of the vascular cylinder of the floral axis (Fig. 2D, arrow) located in the basal region of the pedicel, as in A. polyanthus (Fig. 2F, arrow).
The nectariferous pistillodes of all species are vascularized by the dorsal bundle of the reduced carpels, but only in their basal and middle regions (Fig. 2D and E). These bundles are bigger than the vascular bundles of the other floral parts, as in P. chlorocephalus (Fig. 2G).
Figure 4A shows the schematic drawing of a staminate flower of L. fluitans, illustrating the branching pattern of the vascular bundles, starting from the base of the pedicel. Approximately two-thirds of the length of the sepals, petals and nectariferous pistillodes are vascularized, while all the length of the stamens filaments is vascularized. In A. polyanthus, P. chlorocephalus, P. flaccidus and R. roraimae, the floral parts present a vascular pattern similar to that of L. fluitans.
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Pistillate flowers
The pistillate flowers of all species are pedicellate and present floral bracts (Fig. 1I, L and N). The calyx is dialysepalous in A. polyanthus (Fig. 1I), L. fluitans and R. roraimae (Fig. 1 N) and gamosepalous in P. chlorocephalus and P. flaccidus (Fig. 1L). The corolla is dialypetalous (Figs 1K and P and 5D, asterisks).
The base of the gynoecium of A. polyanthus, L. fluitans, P. chlorocephalus and P. flaccidus present scale-like staminodes opposite to the ovary septa (Figs 1J and M and 3C–E, arrow) and adnate to the petal base (Fig. 1K). These staminodes can be observed using a stereomicroscope. In R. roraimae, they are linear and elongated (Fig. 1P).
The scale-like staminodes form from periclinal divisions of the protoderm and, in most of their extension, consist of epidermis whose faces are very close together but which leave small spaces filled with phenolic compounds, as in A. polyanthus (Fig. 2H), P. chlorocephalus (Fig. 5A, arrow) and L. fluitans (Fig. 5D, arrow). The vascular bundle almost reaches the basal region of the scale-like staminodes, as can be observed in P. chlorocephalus (Fig. 5A, arrowhead). In R. roraimae, the linear and elongated staminodes consist of three or four layers of parenchymatic cells and are vascularized (Fig. 5E, arrow).
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The ovary of all species is sessile (Figs 1J, M and O and 3C–E) and syncarpous. It is tricarpellate (Fig. 5D and F), trilocular, with one ovule per locule (Fig. 5F), except for P. flaccidus which presents a bicarpellate, bilocular ovary, with one ovule per locule.
The style of the species studied is hollow (Fig. 5H) and ramified, which results in stigmatic portions alternating with nectariferous portions. Only the nectariferous portions (Figs 1J, M and O and 3C–E) responded positively to the chemical tests performed to detect the presence of glucose and nectar.
The stigmatic portions are formed from the union of the margins of two adjacent carpels. In L. fluitans and A. polyanthus (Figs 1J, 3C and 5G, arrowheads), the simple stigmas result from the complete fusion of the margins of the adjacent carpels. In P. flaccidus (Figs 1M and 3E), R. roraimae (Fig. 1O) and P. chlorocephalus (Figs 2D and 5H, arrowheads), the bifid stigmas result from the partial fusion of the margins of the adjacent carpels. The stigmatic portions of the style are located on the ovary septa (=commissurally) while the nectariferous portions are located on the ovary locules (=in carinal position) (Figs 1J, M and O and 3C–E).
In the initial stages of flower development, the nectariferous and stigmatic portions of the style are part of the same primary structure, as can be observed in P. chlorocephalus (Fig. 5B). In young flowers, the nectariferous portions are longer than the stigmatic portions of the style (Fig. 3E), whereas in adult flowers, the stigmatic portions are longer than the nectariferous portions (Figs 1J, M and O and 3C and D).
The epidermis that covers the nectariferous portions on the apical region of the style consists of papillose cells that secrete nectar. These cells present an elongated form in A. polyanthus (Fig. 3C), P. flaccidus (Fig. 3E) and R. roraimae, and a rounded form in L. fluitans and P. chlorocephalus (Fig. 3D).
The vascularization of the floral parts of all species is reduced and it is derived from the ramifications of the vascular cylinder of the floral axis, located in the basal region of the pedicel (Fig. 5C, arrow). Sepals and petals are vascularized by a single collateral vascular bundle which is composed of one to two transport cells, as in P. chlorocephalus (Fig. 5F).
The base of the gynoecium (Fig. 5F) presents the last ramification of the vascular cylinder of the floral axis, giving rise to the dorsal (arrows) and ventral (arrowheads) bundles of the carpels. The dorsal bundles of the carpels of all species vascularize the ovary walls and the style, whereas the ventral ones vascularize the placentas and ovules. In the region of the style (Fig. 5G and H), the dorsal bundles of the carpels only vascularize the nectariferous portions (arrows), since the stigmatic portions are devoid of vascularization (arrowheads).
The nectariferous portions of the style of all species are vascularized by vascular bundles that present a higher number of xylem and phloem cells than the vascular bundles of the other floral parts, as can be observed in A. polyanthus (Fig. 5G) and P. chlorocephalus (Fig. 5H).
Figure 4B shows the schematic drawing of a pistillate flower of L. fluitans that illustrates the branching pattern of the vascular bundles from the vascular cylinder at the pedicel base. The sepals, petals and nectariferous appendages are vascularized until approximately two-thirds of their length. Actinocephalus polyanthus, P. chlorocephalus, P. flaccidus and R. roraimae present a vascular pattern similar to that illustrated for L. fluitans. Only in R. roraimae are the staminodes vascularized for all their length.
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DISCUSSION |
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The presence of scale-like staminodes in the staminate flowers of Actinocephalus polyanthus, Leiothrix fluitans, Paepalanthus chlorocephalus and P. flaccidus, and their absence in Rondonanthus roraimae, as well as the fact that linear and elongated vascularized staminodes are only present in the pistillate flowers of the latter may have an important taxonomic meaning, with phylogenetic implications for the Eriocaulaceae.
Since they are extremely tiny structures, the occurrence of scale-like staminodes in the staminate flowers of Eriocaulaceae has only been reported for Syngonanthus caulescens (Rosa and Scatena, 2003). According to Hensold and Giulietti (1991), the presence of linear and elongated staminodes in the pistillate flowers of Rondonanthus is a character that distinguishes them from those of the other genera of the family.
Hensold and Giulietti (1991) considered Rondonanthus to be a basal genus of Paepalanthoideae, since it presents characters of both this subfamily and Eriocauloideae. Stützel (1998) agreed with this and considered Rondonanthus to be located close to the phylogenetic basis of Eriocaulaceae.
The phylogenetic studies carried out on the family (Giulietti et al., 1995, 2000) presented Rondonanthus in an intermediate rather than basal position. However, some incongruities in these phylogenies make it difficult to draw conclusions about the taxonomic and evolutionary hypotheses proposed for the family.
Assuming that an androecium with two staminal whorls can be considered a basal character for the monocotyledons (Dahlgren et al., 1985; Goldberg, 1989; Ronse De Craene and Smets, 1995; Walker-Larsen and Harder, 2000; Ronse De Craene et al., 2003), it is suggested that the isostemonous androecium found in the species studied here represents a derived character in Eriocaulaceae, due to the reduction of the antesepalous whorl of stamens of a probable ancestor with a diplostemonous androecium. In addition, the antepetalous staminodes found in the pistillate flowers are homologous to the antepetalous stamens of the staminate flowers.
The present results show that the vascular bundles that almost reach the basal region of the scale-like staminodes and those of the fertile stamens diverge from the vascular cylinder of the floral axis at different heights, evidencing that the stamens and staminodes have their origin in different whorls. The scale-like staminodes found in the androecium of A. polyanthus, L. fluitans, P. chlorocephalus and P. flaccidus thus correspond to the reduction of the outer whorl of stamens that would be found in a probable ancestor with a diplostemonous androecium.
Among the monocots, clades with whorled staminodes tend to be derived, as asserted by Walker-Larsen and Harder (2000). According to these authors, during the reduction of the androecium, the staminodes that do not acquire new floral functions are soon lost. Following this reasoning, it is suggested that, in Eriocaulaceae, the presence of an androecium constituted by both an outer whorl of scale-like staminodes and an inner whorl of fertile stamens is probably a derived character in the family. This character is observed for most species of Paepalanthoideae, except for staminate flowers of R. roraimae, which do not present staminodes and whose androecium only consists of fertile stamens. According to Unwin (2004), characters that are considered more derived within the family occur in Paepalanthoideae and included, for example, the reduction in stamen number.
The presence of vascularization in the linear and elongated staminodes of the pistillate flowers of R. roraimae may be an evidence that, in Paepalanthoideae, these structures represent a transition between the inner whorl of stamens found in both the monoclinous flowers of Rondonanthus flabelliformis (Hensold and Giulietti, 1991) and the staminate flowers of all Eriocaulaceae, and the whorl of scale-like staminodes devoid of vascularization found in the pistillate flowers of A. polyanthus, L. fluitans, P. chlorocephalus and P. flaccidus.
If it is assumed that Rondonanthus is probably closer to the phylogenetic base of Eriocaulaceae (Hensold and Giulietti, 1991; Stützel, 1998), the scale-like staminodes of the pistillate flowers of A. polyanthus, L. fluitans, P. chlorocephalus and P. flaccidus must be structures derived from an ancestor with floral characters similar to those of R. roraimae.
The presence of nectariferous pistillodes in the staminate flowers of the species studied corroborates the reports by Hare (1950) for Eriocaulon septangulare and by Rosa and Scatena (2003) for E. elichrysoides and S. caulescens as for the production of nectar by the pistillodes.
A. Oriani and V. L. Scatena (UNESP, Rio Claro, Brazil, unpubl. res.) made field observations and checked that the nectariferous pistillodes of the staminate flowers of Syngonanthus elegans produce nectar. In addition, they also observed the presence of insects of the orders Diptera, Coleoptera, Hemiptera and Hymenoptera visiting flowers of S. elegans and extracting the nectar from these structures. The results obtained here thus suggest entomophily as the main pollination syndrome of A. polyanthus, L. fluitans, P. chlorocephalus, P. flaccidus and R. roraimae, and corroborate Ramos et al. (2005), who reported insects of the orders Diptera, Coleoptera and Hymenoptera as the main pollinators of Syngonanthus mucugensis and S. curralensis.
As for the gynoecium of the pistillate flowers of Eriocaulaceae, the presence of a style that divides into nectariferous and stigmatic portions, in probably all Paepalanthoideae, made taxonomists use a different term (e.g. ‘stigmas’; ‘internal and sterile carpelar circle’; ‘staminodes’; ‘nectaries’) to denominate the nectariferous structures, and ‘appendages’ has been the most widely used (Koernicke, 1863; Ruhland, 1903; Giulietti, 1997; Parra, 1998; Stützel, 1998; Sano, 2004).
After confirming the presence of nectar in the gynoecium appendages of S. caulescens, Rosa and Scatena (2003) adopted the terminology ‘nectariferous appendages’ and showed that they are homologous structures to the simple stigmas of E. elichrysoides, and that both are located on the ovary locules and vascularized by the dorsal bundles of the carpels.
The present work shows that the style of the species studied is hollow, and interprets it as a structure ramified in portions with a stigmatic function, interspersed with nectariferous portions. The presence of a hollow style in Eriocaulaceae is a common characteristic among the monocots that present a syncarpous ovary (Rudall et al., 2002).
It is emphasized that the nectariferous portions of the style of A. polyanthus, L. fluitans, P. chlorocephalus, P. flaccidus and R. roraimae (Paepalanthoideae) represent nectariferous structures that have their origin in the morphofunctional modification of the stigmas. This modification is related to the attraction of pollinator agents, which, according to Rosa and Scatena (2003), in the pistillate flowers of E. elichrysoides (Eriocauloideae), is performed by the glands of the petals that also produce nectar, but which are lacking in all taxa of Paepalanthoideae.
According to Givnish et al. (1999), within the commelinids only some Eriocaulaceae developed petal nectaries to substitute the septal nectaries that were lost during evolution. The data obtained in the present work make it possible to hypothesize that the nectariferous pistillodes (in the staminate flowers) and nectariferous portions of the style (in the pistillate flowers) form an alternative substitution for septal nectaries.
The vascular pattern found in the staminate and pistillate flowers of the species studied is constant in the family, and is similar to that presented by Rosa and Scatena (2003) for E. elichrysoides and S. caulescens, in which a single vascular cylinder occurs at the base of the pedicel. The presence of a single, extremely tiny vascular bundle in most floral parts is associated with the reduced size of the flowers of Eriocaulaceae. The prominent vascularization observed in the nectariferous pistillodes of the staminate flowers and in the nectariferous portions of the style of the pistillate flowers of A. polyanthus, L. fluitans, P. chlorocephalus, P. flaccidus and R. roraimae is associated with the production of nectar performed by these structures.
The results obtained in this work show that the scale-like staminodes, which might be interpreted as rudiments of an outer whorl of stamens (as occurs in Eriocauloideae), are lacking only in R. roraimae. Furthermore, they have shown that the nectariferous pistillodes and the nectariferous portions of the style are, in fact, nectariferous structures in Eriocaulaceae.
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ACKNOWLEDGEMENTS |
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We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 301404/2004-6), and the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 05/02141-4) for their financial support. We also thank the two anonymous referees for improvements to the manuscript, and Paulo T. Sano for identifying the material.
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LITERATURE CITED |
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Angiosperm Phylogeny Group. (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141:399–436.[CrossRef]
Böhme S. (1988) Bromelienstudien. III. Vergleichende Untersuchungen zu Bau, Lage und systematischer Verwertbarkeit der Septalnektarien von Bromeliaceen. Tropische und Subtropische Pflanzenwelt 62:1–154.
Bremer K. (2002) Gondwanan evolution of the grass alliance of families (Poales). Evolution 56:1374–1387.[CrossRef][ISI][Medline]
Chase MW, Soltis DE, Soltis PS, Rudall PJ, Fay MF, Hahn WH. (2000) Higher-level systematics of the monocotyledons: an assessment of current knowledge and a new classification. In Wilson KL and Morrison DA (Eds.). Monocotyledons: systematics and evolution(CSIRO, Melbourne) pp. 1–16.
Cronquist A. (1981) An integrated system of classification of flowering plants(Columbia University Press, New York, NY).
Dahlgren RMT, Clifford HT, Yeo PF. (1985) The families of the monocotyledons: structure, evolution and taxonomy(Springer-Verlag, Berlin).
Feder N and O'Brien TP. (1968) Plant microtechnique: some principles and new methods. American Journal of Botany 55:123–142.[CrossRef][ISI]
Giulietti AM. (1997) Análise crítica da evolução da morfologia e da sistemática das Eriocaulaceae(Universidade Estadual de Feira de Santana, Brazil) Titular degree Thesis.
Giulietti AM and Hensold N. (1990) Padrões de distribuição geográfica dos gêneros de Eriocaulaceae. Acta Botanica Brasilica 4:133–158.
Giulietti AM and Pirani JR. (1988) Patterns of geographic distribution of some plant species from the Espinhaço Range, Minas Gerais and Bahia, Brazil. In Vanzolini PE and Heyer WR (Eds.). Proceedings of a Workshop of Neotropical Distribution Patterns(Academia Brasileira de Ciências, Rio de Janeiro) pp. 39–69.
Giulietti AM, Amaral MCE, Bittrich V. (1995) Phylogenetic analysis of inter- and infrageneric relationships of Leiothrix Ruhland (Eriocaulaceae). Kew Bulletin 50:55–71.
Giulietti AM, Scatena VL, Sano PT, Parra LR, Queiroz LP, Harley RM. (2000) Multidisciplinary studies on Neotropical Eriocaulaceae. In Wilson KL and Morrison DA (Eds.). Monocotyledons: systematics and evolution(CSIRO, Melbourne) pp. 580–589.
Givnish TJ, Evans TM, Pires JC, Sytsma KJ. (1999) Polyphyly and convergent morphological evolution in Commelinales and Commelinidae: evidence from rbcL sequence data. Molecular Phylogenetics and Evolution 12:360–385.[CrossRef][ISI][Medline]
Givnish TJ, Evans TM, Zjhra ML, Patterson TB, Berry PE, Sytsma KJ. (2000) Molecular evolution, adaptive radiation, and geographic diversification in the amphiatlantic family Rapateaceae: evidence from ndhF sequences and morphology. Evolution 54:1915–1937.[CrossRef][ISI][Medline]
Goldberg A. (1989) Classification, evolution, and phylogeny of the families of monocotyledons. Smithsonian Contributions to Botany 71:1–74.
Hare LC. (1950) The structure and development of Eriocaulon septangulare With. Journal of the Linnean Society of Botany 53:422–448.
Hensold N and Giulietti AM. (1991) Revision and redefinition of the genus Rondonanthus Herzog (Eriocaulaceae). Annals of the Missouri Botanical Garden 78:441–459.[CrossRef]
Herzog T. (1931) Neue und weniger bekannte Eriocaulaceae aus Nord-Brasilien und dem angrenzenden Venezuela. Feddes Repertorium Specierum Novarum Regni Vegetabilis 29:202–213.
Johansen DA. (1940) Plant microtechnique(McGraw-Hill Book Company, New York, NY).
Kearns CA and Inouye DW. (1993) Techniques for pollination biologists(University Press of Colorado, Niwot, CO).
Koernicke F. (1863) Eriocaulaceae. Flora Brasiliensis (Typographia regiaIn von Martius CFP and Eichler AW (Eds.). , Monachii)274–507.
Linder HP and Rudall PJ. (2005) Evolutionary history of Poales. Annual Review of Ecology, Evolution, and Systematics 36:107–124.[CrossRef][ISI]
Michelangeli FA, Davis JI, Stevenson DW. (2003) Phylogenetic relationships among Poaceae and related families as inferred from morphology, inversions in the plastid genome, and sequence data from the mitochondrial and plastid genomes. American Journal of Botany 90:93–106.
Parra LR. (1998) Flora da Serra do Cipó, Minas Gerais: Syngonanthus Ruhland (Eriocaulaceae). Boletim de Botânica da Universidade de São Paulo 17:219–254.
Ramos COC, Borba EL, Funch LS. (2005) Pollination in Brazilian Syngonanthus (Eriocaulaceae) species: evidence for entomophily instead of anemophily. Annals of Botany 96:387–397.
Ronse De Craene LP and Smets EF. (1995) The androecium of monocotyledons. In Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ (Eds.). Monocotyledons: systematics and evolution(Royal Botanic Gardens, Kew, London) pp. 243–254.
Ronse De Craene LP, Soltis PS, Soltis DE. (2003) Evolution of floral structures in basal angiosperms. International Journal of Plant Sciences 164:S329–S363.[CrossRef]
Rosa MM and Scatena VL. (2003) Floral anatomy of Eriocaulon elichrysoides and Syngonanthus caulescens. Flora 198:188–199.
Rudall PJ. (2002) Homologies of inferior ovaries and septal nectaries in monocotyledons. International Journal of Plant Sciences 163:261–276.[CrossRef]
Rudall PJ, Bateman RM, Fay MF, Eastman A. (2002) Floral anatomy and systematics of Alliaceae with particular reference to Gilliesia, a presumed insect mimic with strongly zygomorphic flowers. American Journal of Botany 89:1867–1883.
Ruhland W. (1903) Eriocaulaceae. In Engler A (Ed.). Das Pflanzenreich(Wilhelm Engelmann, Leipzig) pp. 1–294.
Sajo MG, Rudall PJ, Prychid CJ. (2004) Floral anatomy of Bromeliaceae, with particular reference to the evolution of epigyny and septal nectaries in commelinid monocots. Plant Systematics and Evolution 247:215–231.[CrossRef]
Sano PT. (2004) Actinocephalus (Körn.) Sano (Paepalanthus sect. Actinocephalus), a new genus of Eriocaulaceae, and other taxonomic and nomenclatural changes involving Paepalanthus Mart. Taxon 53:99–107.
Smets EF, Ronse De Craene LP, Caris P, Rudall PJ. (2000) Floral nectaries in monocotyledons: distribution and evolution. In Wilson KL and Morrison DA (Eds.). Monocotyledons: systematics and evolution(CSIRO, Melbourne) pp. 230–240.
Stützel T. (1998) Eriocaulaceae. In Kubitzki K (Ed.). Flowering plants: the families and genera of vascular plants(Springer-Verlag, Berlin) pp. 197–207.
Unwin MM. (2004) Molecular systematics of the Eriocaulaceae Martinov(Miami University, Ohio) PhD Thesis.
Venturelli M and Bouman F. (1988) Development of ovule and seed in Rapateaceae. Botanical Journal of the Linnean Society 97:267–294.
Walker-Larsen J and Harder LD. (2000) The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention. American Journal of Botany 87:1367–1384.
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