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Llllllllllllllllllllllllllllll PUFF /MFN 9702 llllllllllllllllllllllllllllll PUFF /MFN 9702 Malayan Nature Joumal200l, 55 (1 & 2): 133 ~ 146 The Significance of Gynoecium and Fruit and Seed Characters for the Classification of the Rubiaceae CHRISTIAN(PUFF1 Abstract: This paper attempts to give a survey of the highly diverse situation found in the gynoecium (especially ovary) of the Rubiaceae (multi-, pluri-, pauci- and uniovulate locules; reduction of ovules and septa in the course of development, etc.). The changes that can take place after fertilisation (i.e., during fruit and seed development) are discussed using selected examples. An overview of the many diverse types of fruits and seeds of the Rubiaceae is presented. In addition, the paper surveys the diaspores (dispersal units) found in the family and correlates them with the morphological-anatomical situation. Finally, selected discrepancies between "traditional" classification systems of the Rubiaceae and recent cladistic analyses are discussed. While DNA analyses and cladistic studies are undoubtedly needed and useful, it is apparent that detailed (comparative) morphological-anatomical studies of gynoecium, fruits and seeds can significantly contribute to the solution of"problem cases" and should not be neglected, Future cladistic :work should, therefore, more generously include such data. INTRODUCTION The Rubiaceae, with approximately 11 ,000 species and more than 630 genera (Mabberley 1987, Robbrecht 1988), is one of the five largest families of angiosperms. Although centred in the tropics and subtropics and essentially woody, the family also extends to temperate regions and exhibits a wide array of growth forms, with some tribes having herbaceous, and even annual members. Not surprisingly, floral, fruit and seed characters also show considerable diversity. One of the main aims of this paper is to give a survey of the female reproductive structures, concentrating on the ovary. Moreover, it will describe changes taking place after fertilisation, and also survey fruit and. seed characters, correlating them with ecological aspects (diaspores-dispersal units-and their mode of dispersal vs. morphological-anatomical fruit and seed structure). Finally, it will also discuss the significance of gynoecium, fruit and seed structure for the classification of the family. 1 Institute of Botany, University of Vienna, Rennweg 14, A-1 030 Vienna, Australia 133 - / THE CHARACTERS2 Gynoecium The basic type of Rubiaceae flower is five-merous, sympetalous and has an inferior ovary. With regard to the gynoecium, it is now quite safe to assume that, in spite of the five-merosity of the other floral parts, the basic situation is a bicarpellate gynoecium (this appears to be confirmed by cladistic analyses, e.g. Bremer et al. 1995, Bremer 1996b). The presence of two carpels, in fact, predominates in the family, occurring in tribes of all recognised subfamilies (Robbrecht 1988: Fig. 34). While numerous tribes are characterised by a strictly bicarpellate situation, others show increases in carpel numbers. Several tribes, such as Psychotrieae, show an increase from two to five. In others, the number may be even further increased (to over 10, in, for example, the Vanguiereae). The Urophylleae are perhaps the tribe with the highest range of variation in carpel number: (3-)4 to 8( -16) (Buchner 1995). Increase in carpel number is sometimes even recorded within genera, e.g., in the predominantly 4-5-carpellate genus Lasianthus (PSY.P.), carpel number may be increased to over 10 .. The genus Timonius (GUE.) represents a very exceptional and-in Rubiaceae -unique situation. Ovaries may contain up to 150 locules, each with a solitary ovule (and, subsequently, drupes with the same number of pyrenes!). This comes about-as in Punica (Punicaceae) or the Navel Orange-by a secondary increase in the number of carpels, caused by secondary formation of successive whorls (Martinello 1992). On the other hand, there are also reductions of the basic bicarpellate situation: Theligonum (THE.) is characterised by having a "1-locular ovary, with a s.ingle basal ovule" (Robbrecht 1988); recent, detailed investigations, however, show that the ovary is basically bilocular, but the incomplete septum is overarched by the only ovule (Rutishauser et al. 1998). While the wind-pollinated African and Madagascan Anthospermeae-Anthosperminae basically are bicarpellate, one of the two carpels is infertile, variously reduced and modified (and only 1 stigma present) in all but one species of the South-western Cape genus Carpacoce; similar reductions are also documented for two of the 39 species of Anthospermum (Puff 1986). ' . Ovary position. Although the overwhelming majority of Rubiaceae have inferior ovaries, some-notably Gaertnera and Pagamea (PSY.)-are cited as having (semi-) superior ovaries. In a detailed investigation of the paleotropical Gaertnera, Igersheim et al. (1994), however, prove that the ovary only becomes secondarily superior in the course of floral development. They suggest that its neotropical counterpart, Pagamea, exhibits the same situation and speculate that "half-inferior" ovaries such as those of some Hedyotideae taxa (cf. Jovet 1941) are basically inferior and represent 2 The abbreviations for tribes and subtribes used throughout the text follow Robbrecht (1988). The inclusion of the Hedyotideae, and of genera of the Knoxieae, in the Spermacoceae (Bremer 1996a) is not followed here. 134 only a variation of the general situation. Fused ovaries. In a number of Rubiaceae, adjacent ovaries ·of one and the same flower are united by tissue fusion from the pre-anthesis stage onwards. In the simplest case, it is two fused ovaries (Mitchella, MIT.), in other cases it is several to many (e.g. Morinda, MOR., or Rennellia, PRI.). Ovary fusion is not tribe-specific; in the Naucleeae, for example, there are taxa with both fused and free ovaries, although the basic inflorescence type is the sa~e in all of them (Ridsdale 1978). As the presence or absence of ovary fusion determines which kind of dispersal unit will develop (infructescences, if ovaries are fused; see below), it is a feature to be looked at closely. True, false, complete and incomplete septa. The normal or "typical" situation is that septa completely separate locules, whereby the septum marks the border between two adjacent carpels. In some (basioally bicarpellate) taxa, however, the septum never is fully continuous (it is "incomplete" in that it leaves a gap between two locules). An example is Faramea (COU.), where in early floral stages the septum is only visible at the base of the ovary. In Theligonum, too, the septum is incomplete (see also reduction of carpels, above). False septa of certain Rubiaceae are outgrowths of the carpel wall which extend through the locule towards the centre of the ovary. They either are restricted in their growth (never actually reaching the centre; "incomplete"), or they actually completely subdivide a locule because they come in touch with the centre. In Strumpfia (INC.SED.), for example, cross sections of ovaries (from top to bottom), first sho~ a seemingly 4-locular ovary, then the true septum and two false septa retracting from the centre, and finally a bicarpellate ovary, without any trace of false septa at all (Igersheim 1993). Both, the African Pauridiantheae and the Asiatic Urophylleae are characterised by ovaries with false septa. In both, the false septa are usually only continuous in the apical part of the ovaries but (largely) disappear further below (Bangoura 1993, Buchner 1995). Due to the presence of false septa, the ovary structure of, for example, Praravinia (URO.; with up to 16 carpels) may become highly complicated. Also the presence of large placentas, extending all the way to the carpel walls, may mimic the presence of false septa. In Morinda, with bicarpellate ovaries and two ovules per locules, the placentas are so massive and extensive that they divide each locule into two halves (thus giving the impression that the ovaries are 4-locular and only contain one ovule per locule) (Igersheim and Robbrecht 1993). Placentation. The ~ubiaceae are basically characterised by an axile placenta. There are, however, transitions from axile to parietal, and truly parietal placentas (especially in the Gardenieae; Robbre~ht and Puff 1986). Moreover, some tal(a (e.g. those with incomplete "true" septa, see above), show a placentation that at least approaches basal placentation. - The insertion and shape of the placentas are highly variable. They may be attached to the entire septum or, in the other extreme, to only a very small portion 135 of it. Their shape ranges from small to very large, they may be variously divided, ± sessile or stalked (see Robbrecht 1988 for details). Noteworthy are proliferating placentas (particularly prominent in genera of the Gardenieae). Placentas start growing around the ovules, eventually immersing ­ them. This process starts at (or even before) an thesis and continues during fruit development (finally, the seeds are totally immersed in a fleshy pulp) (e.g. Euclinia; Halle 1967, Fig. 37). Ovules. Presumably the basic situation in the Rubiaceae is a large placenta bearing numerous ovules. The latter are mostly anatropous (or hemi-anatropous), but a trend to camp:Ylotropous ovules is noticeable (recorded for various taxa of diverse alliances but apparently particularly common in PAV.; de Block 1995). Various tribes are characterised by consistently pluriovulate placentas, but for several others reduction series are documented. In Tricalysia (GAR.D.), for example, the ovaries are multi- to two- and, in a few species, even consistently uniovulate (Robbrecht 1979, 1987). On the other hand, a large number of tribes is almost exclusively defined by having uniovulate locules. In this group, two very clear-cut categories can be distinguished: (a) ovule (and placenta) inserted near or at the base of the septum, and the micropyle of the erect ovule points down- and outward (away from the septum)(e.g. Paederia, PAE., Svoma 1991); (b) ovule (and placenta) inserted near or at the top of the septum, and the micropyle of the pendulous ovule points up- and inward (towards the septum) (e.g.
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