Comparative Floral Structure and Systematics in Rhizophoraceae

Botanical Journal of the Linnean Society, 2011, 166, 331–416. With 197 ﬁgures

Comparative ﬂoral structure and systematics in Rhizophoraceae, Erythroxylaceae and the potentially related Ctenolophonaceae, Linaceae, Irvingiaceae and

Caryocaraceae (Malpighiales) Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021

MERRAN L. MATTHEWS* and PETER K. ENDRESS FLS

Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, CH-8008 Zurich, Switzerland

Received 28 January 2011; revised 3 May 2011; accepted for publication 27 May 2011

Within the rosid order Malpighiales, Rhizophoraceae and Erythroxylaceae (1) are strongly supported as sisters in molecular phylogenetic studies and possibly form a clade with either Ctenolophonaceae (2) or with Linaceae, Irvingiaceae and Caryocaraceae (less well supported) (3). In order to assess the validity of these relationships from a floral structural point of view, these families are comparatively studied for the first time in terms of their floral morphology, anatomy and histology. Overall floral structure reflects the molecular results quite well and Rhizo- phoraceae and Erythroxylaceae are well supported as closely related. Ctenolophonaceae share some unusual floral features (potential synapomorphies) with Rhizophoraceae and Erythroxylaceae. In contrast, Linaceae, Irvingiaceae and Caryocaraceae are not clearly supported as a clade, or as closely related to Rhizophoraceae and Erythroxy- laceae, as their shared features are probably mainly symplesiomorphies at the level of Malpighiales or a (still undefined) larger subclade of Malpighales, rather than synapomorphies. Rhizophoraceae and Erythroxylaceae share (among other features) conduplicate petals enwrapping stamens in bud, antepetalous stamens longer than antesepalous ones, a nectariferous androecial tube with attachment of the two stamen whorls at different positions: one whorl on the rim, the other below the rim of the tube, the ovary shortly and abruptly dorsally bulged and the presence of a layer of idioblasts (laticifers?) in the sepals and ovaries. Ctenolophonaceae share with Rhizophoraceae and/or Erythroxylaceae (among other features) sepals with less than three vascular traces, a short androgynophore, an ovary septum thin and severed or completely disintegrating during development, leading to a developmentally secondarily unilocular ovary, a zigzag-shaped micropyle and seeds with an aril. Special features occurring in families of all three groupings studied here are, for example, synsepaly, petals not retarded and thus forming protective organs in floral bud, petals postgenitally fused or hooked together in bud, androecial tube and petals fusing above floral base, androecial corona, apocarpous unifacial styles, nucellus thin and long, early disintegrating (before embryo sac is mature), and nectaries on the androecial tube. Some of these features may be synapomorphies for the entire group, if it forms a supported clade in future molecular studies, or for subgroups thereof. Others may be plesiomorphies, as they also occur in other Malpighiales or also in Celastrales or Oxalidales (COM clade). The occurrence of these features within the COM clade is also discussed. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416.

ADDITIONAL KEYWORDS: androecium – Celastrales – COM clade – core eudicots – ﬂoral anatomy – ﬂoral morphology – gynoecium – malvids – Oxalidales – perianth – rosids.

INTRODUCTION large clade based on molecular phylogenetic studies, containing newly found orders and orders with The present study is part of a series of comparative largely new family compositions (e.g. Chase et al., ﬂoral structural studies on suprafamilial clades of 1993; Soltis, Gitzendanner & Soltis, 2007; Zhu et al., rosids. Among angiosperms, rosids are an especially 2007; APG III, 2009; Wang et al., 2009; Christenhusz et al., 2010; Qiu et al., 2010). Most of these newly *Corresponding author. E-mail: [email protected] recognized clades still need to be characterized

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 331 332 M. L. MATTHEWS and P. K. ENDRESS structurally and biologically in order to gain inte- ceae) belonging instead to Cucurbitales (Schwarzbach grated knowledge of their properties and their evolu- & Ricklefs, 2000; Zhang et al., 2006). Anisophylleaceae tionary biology. However, this is a long-term goal as were sometimes also placed in other rosid orders such studies are time-consuming. First attempts have (Cronquist, 1981; Tobe & Raven, 1987a; Dahlgren, already been made focusing on the entire rosid clade 1988; Juncosa & Tomlinson, 1988a, b; discussion on (Endress & Friis, 2006; Endress & Matthews, 2006b; floral structure, Tobe & Raven, 1988a; Matthews et al., Schönenberger & von Balthazar, 2006; Endress, 2001). 2010a) and on specific orders or clusters of families The position of Rhizophoraceae with other families (Matthews et al., 2001; Matthews & Endress, 2002, now constituting Malpighiales (Erythroxylaceae not 2004, 2005a, b, 2006, 2008; Bachelier & Endress, included) was first identified in the molecular study 2008, 2009). Malpighiales, with 35 families listed in by Conti, Litt & Sytsma (1996) [Rhizophoraceae + Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 APG III (2009), are the largest and most recalcitrant Drypetes Vahl sister to Humiriaceae + (Euphorbia clade of rosids in terms of phylogenetic resolution L. + Malpighiaceae)]. Earlier, Rhizophoraceae were (Davis, Xi & Wurdack, 2008a; Korotkova et al., 2009; commonly placed in or close to Myrtales or with Wurdack & Davis, 2009; Soltis et al., 2011). families that are now in Myrtales (Endlicher, 1836– It has been assumed that the difficulties in phylo- 1840, 1841; Bentham & Hooker, 1862–1867; Baillon, genetic resolution, especially in Malpighiales, are the 1876; Schimper, 1893; Dahlgren, 1983; Takhtajan, result of an explosive radiation in the mid-Cretaceous 1987) or with Cornales (Thorne, 1983). However, (Davis et al., 2005; Magallón & Castillo, 2009; Wang already Hallier (1921: 95) regarded Rhizophoraceae et al., 2009). The most surprising recent phylogenetic as related to Linaceae. According to Cronquist (1981) discovery is that the giant-flowered Rafflesiaceae are they were difficult to place, with Myrtales, Cornales members of Malpighiales and that they are closely or Rosales, or as a separate order, Rhizophorales (in related to Euphorbiaceae (Davis et al., 2007; Davis, Rosidae). Dahlgren (1988) assumed relationships of 2008; Davis, Endress & Baum, 2008b). Thus, floral Rhizophoraceae primarily with Elaeocarpaceae (now gigantism is a striking example of drastic evolution- in Oxalidales) and with Celastraceae (Celastrales), ary changes in the diversification of Malpighiales. but also discussed potential relationships with Eryth- The present study focuses on six families: Rhizopho- roxylaceae and some other groups, and Keating & raceae, Erythroxylaceae, Ctenolophonaceae, Linaceae, Randrianasolo (1988) found similarities with Hugonia Irvingiaceae and Caryocaraceae. These families have L. (Linaceae), among other groups. In contrast to been placed in very different orders in premolecular Rhizophoraceae, Erythroxylaceae were placed close to classifications. Some are known for single familiar other families of the current Malpighiales, such as genera, such as flax and linseed (Linum L., Linaceae), Malpighiaceae (de Jussieu, 1789; Endlicher, 1836– coca (Erythroxylum P.Browne, Erythroxylaceae) or 1840, 1841 and Linaceae (Bentham & Hooker, 1862– mangroves (Rhizophora L. and some other genera of 1867; Baillon, 1873, 1874; Gundersen, 1950; Rhizophoraceae). Of the six families, only the sister Oltmann, 1968) or Linales–Rosidae (Cronquist, 1981). relationship of Rhizophoraceae and Erythroxylaceae is With regard to the other four families considered currently most robustly supported. It was first found here, Caryocaraceae + [Linaceae + Irvingiaceae] are (with moderate support) in an rbcL study by Setoguchi, sister to Rhizophoraceae + Erythroxylaceae in the Kosuge & Tobe (1999) and a study with atpB and rbcL angiosperm analysis by Soltis et al. (2007) with narrow by Savolainen et al. (2000a), but Schwarzbach & Rick- sampling within Malpighiales, but without strong lefs (2000) found strong support for this sister clade support (Fig. 1A), whereas Ctenolophonaceae appear based on plastid DNA and nuclear DNA analyses, and as sister to Rhizophoraceae + Erythroxylaceae in the this relationship was clearly confirmed by further large 13-loci analysis of Malpighiales by Wurdack & studies (Tokuoka & Tobe, 2006; Korotkova et al., 2009; Davis (2009) (Fig. 1B), also without strong support, Wurdack & Davis, 2009; Soltis et al., 2011). That Ery- and similarly in the recent 17-loci, 640-taxon throxylaceae are related to Rhizophoraceae was first angiosperm-wide analysis of Soltis et al. (2011). The assumed based on the shared special type of sieve-tube relationship between Caryocaraceae, Linaceae, and plastids (Behnke, 1982, 1988). Curiously, when the Irvingiaceae also lacks strong support (Soltis et al., genus Peglera Bolus (now in Nectaropetalum Engl. in 2007), and their positions are scattered in Malpighi- Erythroxylaceae) was first described by Bolus (1907), it ales in Wurdack & Davis (2009) and Soltis et al. (2011). was thought to be closely related to Rhizophoraceae Linaceae and some related families were earlier (Macarisieae A. Schimp). At the same time as the predominantly seen as related to Geraniaceae or relationship between Rhizophoraceae and Erythroxy- Geraniales (Endlicher, 1836–1840, 1841; Baillon, laceae was established by molecular studies, Rhizo- 1874; Takhtajan, 1959, 1987; Dahlgren, 1983; Thorne, phoraceae were found to be non-monophyletic, with 1983, 1992), which also contained some other families Anisophylleaceae (formerly included in Rhizophora- of the current Malpighiales. Hutchinson (1959) placed

Ctenolophon was at ﬁrst tentatively placed in Ola- caceae (Oliver, 1873), but then positioned in Linaceae Rhizophoreae 1.0 Gynotrocheae by Pierre (1893) and Winkler (1931) and in Hugoni- phoraceae 1.0 Rhizo- aceae (Linales) by Cronquist (1981). The family Erythroxylaceae 0.66 Ctenolophonaceae was erected by Exell & Mendonça 1.0 Linaceae Rhizophoraceae s.l. (1951) and positioned in Geraniales (with Linaceae 0.59 Irvingiaceae 1.0 0.69 and other malpighialean families) by Takhtajan Caryocaraceae (1959) and in Linales (with Erythroxylaceae and other Malpighiales four other families) (Takhtajan, 1987). Huber (1991) A found resemblances in the seeds of Ctenolophon and Rhizophoraceae. Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 Although there is currently no strong support for Rhizophoreae a sister relationship between the Rhizophoraceae– 100/1.0 Gynotrocheae 100/1.0 Erythroxylaceae clade and Ctenolophonaceae or phoraceae Macarisieae Rhizo- 100/1.0 100/1.0 Paradrypetes Linaceae–Irvingiaceae–Caryocaraceae (Soltis et al., Erythroxylaceae 2007, 2011; Wurdack & Davis, 2009), the molecular

84/1.0 100/1.0 Rhizophoraceae s.l. Ctenolophonaceae studies that yielded these groups as potential rela- 100/1.0 tives are to date the most extensive ones including other Malpighiales the entire order Malpighiales. Therefore, we include B representatives of all six families in this study. Cur- rently, our knowledge of the detailed floral struc- Figure 1. Cladograms of Rhizophoraceae s.l. (Rhizopho- raceae and Erythroxylaceae) with potentially related fami- ture of some of these families is poor and, although lies. A, Caryocaraceae + (Linaceae + Irvingiaceae) sister to there are numerous short publications on floral mor- Rhizophoraceae s.l. (simplified after Soltis et al., 2007; phological and anatomical aspects, they often focus on Fig. 8, 3-gene analysis, with Bayesian posterior probability single species and mostly concentrate on vascular values). B, Ctenolophonaceae sister to Rhizophoraceae s.l. patterns. Comparative studies are lacking for most (simplified after Wurdack & Davis, 2009, Fig. 3, 13-gene families (except for Rhizophoraceae; Juncosa, 1988) analysis, with maximum likelihood bootstrap/Bayesian and suprafamilial comparisons are not available. The posterior probability values). present paper intends to remedy this situation and to further broaden our understanding of the multiple them in his Malpighiales (the order then much families that constitute Malpighiales. smaller than today and also including a few extra- neous families). Irvingia Hook.f. was positioned in Simaroubaceae MATERIAL AND METHODS (Sapindales) for a long period of time (still by Noot- eboom, 1967 and Cronquist, 1981), or as its own TAXA EXAMINED AND MICROSCOPY family Irvingiaceae close to Anacardiaceae (Pierre, The open flowers and floral buds of all six families 1892) or to Simaroubaceae (van Tieghem, 1905), and (Table 1), fixed in formalin–acetic acid–alcohol (FAA), in Rutales (Takhtajan, 1987, 1997), although Hallier 70% ethanol or ‘Copenhagen Mix’ (see Table 1 for (1921) placed Irvingieae Engl. in his Erythroxyleae herbarium material) were used for light microscopy Kunth of Linaceae, Forman (1965) close to Linaceae (LM) and scanning electron microscopy (SEM). Her- and Eckert (1966) suggested to remove it from Sima- barium material was rehydrated and softened using roubaceae because of its different floral development sodium bis (2-ethylhexyl) sulphosuccinate (Fluka) at c. (also Oltmann, 1971, for pollen; van Welzen & Baas, 20°C. For serial microtome sections, specimens were 1984, for leaf anatomy; and Ditsch & Barthlott, 1997, embedded in Kulzer’s Technovit (2-hydroethyl meth- for epicuticular waxes). acrylate). A stepwise infiltration was conducted to Caryocar L. was regarded as close to Sapindaceae enhance infiltration with the following ratios of 100% (Endlicher, 1836–1840, 1841) or positioned in Pari- ethanol to Technovit solution (50 : 50, 25 : 75, 0 : 100). etales (Engler, 1925; Pilger, 1925) or Theales Embedded material was sectioned using a Microm HM (Bentham & Hooker, 1862–1867; Cronquist, 1981; 355 Rotary microtome with a conventional knife D. Thorne, 1983, 1992). For a more detailed historical The 7-mm thick sections were stained with ruthenium account, see Prance & da Silva (1973). An early hint red and toluidine blue and mounted in Histomount. of a relationship with Linales came again from For SEM studies, specimens were post-fixed in 2% Hallier (1921) who assumed that Caryocaraceae origi- osmium tetroxide (Fluka), dehydrated in ethanol and nated from Linaceae (but also some other, unrelated acetone, critical-point dried, sputter coated with gold families, as currently perceived). and examined with either a Hitachi S-4000 or a Joel

Table 1. List of taxa and collections studied

Floral stage, sex Taxon studied (if not bisexual) Material Collection details

CARYOCARACEAE Caryocar brasiliense Cambess. Buds, open flowers Liquid-fixed s.n. (Campo Grande, Brazil); received from L. Kinoshita, UNICAMP, Brazil CTENOLOPHONACEAE Ctenolophon englerianus Mildbr. Buds, open flowers Dry G. McPherson 16911 (Gabon); [MO]

ERYTHROXYLACEAE Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 Aneulophus africanus Benth. Open flowers Dry J. M. Reitsma 1254 (Gabon); [MO] Erythroxylum cuneifolium Buds, open flowers Liquid-fixed B. Marazzi B213 (Argentina) O.E.Schulz Nectaropetalum kaessneri Engl. Open flower Dry T. Kässner 306 (Tropical Africa); [Z] IRVINGIACEAE Irvingia smithii Hook.f. Buds, open flowers Dry D. J. Harris & M. Fay 1567 (Central African Republic); [MO] LINACEAE Hugonioideae Hugonia acuminata A.Chev. Buds, open flowers Dry G. Zenker 1287 (Cameroon); [Z] (Figs 81, 110, 111, 124) Hugonia acuminata A.Chev. Buds Dry G. Zenker 4341 (Cameroon); [Z] Roucheria griffithiana Planch. Bud, open flowers Dry H. Surbeck 445 (Sumatra); [Z] Linoideae Linum kingii S.Watson Buds, open flowers Liquid-fixed P. K. Endress 04–31 (Utah, USA) Reinwardtia indica Dum. Buds, open flowers Liquid-fixed P. K. Endress 9862 (cult. BGZ) RHIZOPHORACEAE Gynotrocheae Engl. Carallia borneensis Oliv. Buds, open flowers Liquid-fixed A. Juncosa s.n. Oct 1981 (Brunei) Carallia suffruticosa Ridl. Buds, open flowers Liquid-fixed C. F. Symington 44923 (Malaysia); [K] Crossostylis grandiflora Buds Liquid-fixed A. Juncosa s.n. Sept 1981 (New Brongn. & Gris Caledonia) Gynotroches axillaris Blume Buds, open flowers; Liquid-fixed A. Juncosa s.n. Oct 1981 (Sarawak) functionally male Gynotroches axillaris Blume Buds, open flowers; Liquid-fixed A. Juncosa s.n. 9 Oct 1981 (Sarawak) functionally female Pellacalyx cristatus Hemsl. Buds, open flowers Liquid-fixed A. Juncosa s.n. 10 Oct 1981 (Sarawak) Marcarisieae A. Schimp. Anopyxis klaineana Pierre Buds, open flowers Dry Ill 1352 (Cameroon); [K] (Figs 101, 120) Anopyxis klaineana Pierre Buds, open flowers Dry M. G. Le Testu 8803 (Cameroon); [K] (Figs 2, 3, 63, 84, 85, 102, 126, 174) Cassipourea congensis R.Br. Buds, open flowers Liquid-fixed s.n. 30948 8 May 1952 (Nigeria); [K] Cassipourea elliptica Poir. Buds Liquid-fixed A. Juncosa s.n. s.d. (Costa Rica) Rhizophoreae Bruguiera cylindrica Blume Buds, open flowers Liquid-fixed T. M. A. Utteridge 46 (Indonesia); [K] (Fig. 12, 173E) Bruguiera cylindrica Blume Buds Liquid-fixed A. Juncosa s.n. s.d. (Sarawak) (Figs 11, 41, 58, 75, 135, 151, 160, 173D, 180) Ceriops decandra (Griff.) Ding Buds Liquid-fixed P. K. Endress 9206 (North Queensland, Hou Australia) Ceriops tagal C.B.Rob. Buds, open flowers Liquid-fixed P. K. Endress 9205 (North Queensland, Australia) Rhizophora mucronata Lam. Buds, open flowers Liquid-fixed P. K. Endress 10–01 (Florida, USA) Rhizophora ¥ lamarkii Buds Liquid-fixed P. K. Endress 6209 (North Queensland, Australia)

6360LV scanning electron microscope. Permanent Angiospermy types (mode of carpel closure). Type 1: slides of the microtome sections are deposited at the angiospermy by secretion; Type 2; angiospermy by a Institute of Systematic Botany, University of Zurich, continuous secretory canal and partial postgenital Switzerland (Z). This is also true for vouchers if the fusion at the periphery; Type 3: angiospermy by a material is not from K or MO. partial secretory canal and postgenital fusion along the entire length of the ventral slit at the carpel periphery; Type 4: angiospermy by postgenital fusion FLORAL DESCRIPTIONS along the entire length of the ventral slit (for discus- Floral structure is described for selected representa- sion, see Endress & Igersheim, 2000).

tives of all six families, including the three tribes Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 within Rhizophoraceae s.s. and subfamilies of Syntropous and antitropous ovule curvature direction: Linaceae. Description of all floral parts, with the Syntropous ovules are curved (anatropous or campy- exception of the gynoecium, is based on advanced lotropous) in the same direction as the carpels, anti- floral buds (in which male meiosis has taken place). tropous ovules are curved in the reverse direction (see This stage was preferred over anthetic flowers as the Endress, 2011a). perianth organs are still in an upright position and thus entire flowers could be studied in transverse section series. The gynoecium is described at anthe- RESULTS sis. Flowers are generally described from the apex, RHIZOPHORACEAE downwards. The course of the pollen tube transmit- Anopyxis klaineana (Macarisieae) ting tract (PTTT) is described in the morphology section for practical reasons. Morphology: Flowers are medium-sized, bisexual, polysymmetric, pentamerous, isomerous and obdiplostemonous (see Glossary for term) (Figs 2, 3). Sepals are the protective organs in advanced buds. GLOSSARY Aestivation is strongly revolute–valvate, resulting in Flower size (open flowers): Flowers are measured in a distinctly star-shaped bud in transverse section. terms of their length, from the base of the receptacle to Sepals are thick in the median region, thinner along the tip of the stigma. Flowers generally range from their revolute flanks; they have a broad base and a Յ small ( 5 mm) to medium-sized (up to c. 15 mm); only pointed tip and are congenitally united for c. 1/3 of Caryocar brasiliense Cambess. was large (c.4cm). their length (Fig. 2F–O), postgenitally connected by interlocking hairs above. In the upper part of the Diplostemonous and obdiplostemonous androecium: congenitally united region, the intersepalous areas This distinction in stamen position can only be made form five short vertical ridges (Fig. 2G). Petals are with certainty when the carpels are isomerous with thick and elaborate; they are elongate and strap-like the two stamen whorls. Flowers with an antesepalous with a narrow base and a lobed apex: a long median carpel position are diplostemonous, flowers with an lobe with a rounded tip flanked by one or two short antepetalous carpel position are obdiplostemonous lateral lobes, the median lobe incurved into the centre (see Matthews et al., 2001; Bachelier & Endress, of the bud (Figs 2D and 63). Aestivation is open. 2009; Endress, 2010b). Whether the antesepalous or Antesepalous and antepetalous stamens are of the antepetalous stamens are more towards the similar length; their narrow, thin filaments are free outside of the other stamen whorl is often difficult to only for a short distance above a long nectariferous, establish because the filaments may have different androecial tube bearing ten short lobes alternating thicknesses and their proportions may change during with ten stamens around the rim (Figs 2E–O, 84, 85). development (discussion in Endress, 2010b). For con- The tube is slightly longer in the antesepalous sectors venience, we use the term diplostemonous for all than the antepetalous ones; antesepalous stamens cases with an anisomerous gynoecium. are positioned more to the outside than the antepetalous ones. Filaments are slightly shorter than anthers still at anthesis. Anthers are tetrasporangiate, Postgenital fusion incomplete and complete. Incom- x-shaped, dorsifixed towards the base of the connec- plete: carpel flanks postgenitally fused such that the tive, latrorse and versatile (Figs 101, 102). Each theca epidermis of the ventral slit is discernible in trans- dehisces by a longitudinal slit; the slits are not con- verse microtome sections. Complete: carpel flanks tinuous over the connective. The connective is thin postgenitally fused such that the epidermis of the and endothecium-like tissue does not extend into it; a ventral slit is not discernible in transverse microtome protrusion is short or absent. The gynoecium is syn- sections. carpous (Figs 2B–O, 3); it is of angiospermy type 2 (or

A Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021

BCD E

F G H I

JKLM

NOPQ S

Figure 2. Anopyxis klaineana (Marcarisieae; Rhizophoraceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. A–F, level of free revolute–valvate sepals. B–K, level of symplicate gynoecium. B–D, level of completely postgenitally fused ventral slits of carpels (gap in centre of gynoecium artefact of herbarium material?). B, level of capitate stigma. C–H, level of style. C–G, level of gap in centre of gynoecium (artefact?). D–N, level of free petals. D, level of incurved petal tips. E–O, level of fused sepals and androecium. E, F, level of anthers and short free filaments. F, level of partial androecial tube. G–O, level of androecial tube. H–I, level of dorsally bulged-up carpels. J–O, level of nectary (shaded) on androecial tube. L–M, level of synascidiate zone of gynoecium. N–P, level of floral cup with nectary (shaded); level of gynophore. P, level of nectar recesses surrounding gynoecium base. Q–S, floral base and pedicel. Scale bar, 1 mm.

B C D F G E F B C D E H I

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J K L M

N O P Q

I J K L M N O P Q R S R S T U T A U

Figure 3. Anopyxis klaineana (Marcarisieae; Rhizophoraceae). Pentamerous gynoecium at anthesis; pollen tube transmitting tissue (PTTT) shaded. A, schematic median longitudinal section; ventral slit and PTTT drawn without a central gap in the gynoecium (assuming that the gap in transverse sections is likely an artefact of herbarium material). Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines; postgenitally fused areas hatched. B–U, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. B–R, level of compitum. B–Q, symplicate zone. D–L, level of completely postgenitally fused ventral slits (E–K, gap in centre likely an artefact). B–E, level of capitate stigma with pronounced vasculature (arrows). C–D, broad ring of vasculature (arrows). J–L, level of dorsally bulged-up carpels. M–Q, level of open ventral slits. M–N, level of apical septum. N–T, level of collateral ovules. N–Q, level of developmentally secondarily unilocular ovary. R–T, synascidiate zone. U, Gynoecium base below locules. Scale bars, 500 mm.

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 338 M. L. MATTHEWS and P. K. ENDRESS type 4, depending upon whether the gap is an arte- extends into the stigma as a massive ring, which fans fact, see below); carpels are antepetalous. The globu- out into the stigmatic lobes (Fig. 3B–D). Directly lar, superior hairy ovary is synascidiate up to below below the stigma this ring separates into individual the placenta, symplicate above, this zone extending bundles, which are broad in the upper style, narrow- up to the stigma; it is shortly and abruptly bulged up ing into smaller bundles lower down. The much on the dorsal side above the level of insertion of the shorter main lateral carpel bundles extend up to the style so that the star-shaped style (in transverse ovary (Fig. 3L). Additional lateral bundles extend up section) appears sunk into it (Figs 2H, I, 3J, K, 120, to the placenta and supply the ovules, forming syn- 126). The dorsally bulging area of each carpel joins laterals below the locules (Fig. 2N). The ovule bundle with adjacent neighbouring carpels and with the style ends in the chalaza. Below the locules the main dorsal along its median region resulting in short commis- and lateral carpel bundles join, and then the synlat- Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 sural slits between the ovary and the stylar base erals. Lower down in the floral base antepetalous (Figs 2I, 3L). The large syncarpous capitate stigma stamen bundles, petal bundles and lateral sepal with a depression in its centre is unicellular–papillate bundles join as do the corresponding antesepalous (Fig. 3A–E). Completely postgenitally fused (see Glos- stamen bundles and median sepal bundles (Fig. 2Q). sary for term) ventral slits extend throughout the Together with the carpel bundles they form a stele. style (Fig. 3A). PTTT is present as an extensive, more or less continuous strand (with large intercellular Histology: Tanniferous tissue is present in the sepals, spaces) in the upper style, which narrows from the stamen filaments, androecial tube and gynoecium. A stigma to the ovary; in the mid to lower style a short distinct layer of large cells with tannins and numer- gap is present in the gynoecium (artefact of her- ous vesicles (laticifers?) is present in the sepal hypo- barium material?). An apparent compitum extends dermis (and ovary wall, although less distinct) throughout the symplicate zone (Fig. 3B–R). An (Fig. 174). The outer wall of the ventral sepal epider- apical septum is present in the symplicate zone of the mis is thick and mucilaginous. Oxalate druses are ovary (Figs 2J, 3M, N); ventral slits are open and the present in all floral organs. Unicellular, lignified hairs ovary is unilocular until below the placenta (Figs 2K, are dense on the dorsal and ventral edges of the 3N–Q); the carpel margins are covered with c. four or valvate sepals and scattered on the median ventral five cell layers of PTTT. Placentation is axile and portion; they are also present on the dorsal side and lateral. Obturators are present. Two collateral anti- margins of the petals; they are dense on the ovary tropous (see Glossary for term) ovules are present and sparse on the style. Stomata are present on the per locule (Fig. 3N–T). Ovules are anatropous (to ventral surface of the androecial tube (nectar pores). hemianatropous), bitegmic and crassinucellar; the micropyle is formed by both integuments. The semi- annular outer integument is four or five cell layers Cassipourea congensis (Macarisieae) thick; it is much longer on the antiraphal side and Morphology: Flowers are small, bisexual and polysym- surrounds the obturator. The inner integument is metric (Fig. 4). The perianth is tetramerous. Sepals seven cell layers thick. Both integuments are lobed. are the protective organs in advanced buds. They are An endothelium is present. The nucellus appears to thick, have a broad base with a pointed tip and are disintegrate around the embyo sac. A very short gyno- valvate; they are tightly postgenitally connected in bud phore is present (Figs 2N, O, 3U). Towards the base of by interdigitation of unicellular papillae along their the flower the petals join both the androecial tube and margins; congenital union between sepals is absent. sepals at approximately the same level, resulting in Petals are elaborate, long, narrow and strap-like; they five concavities between the sepals and tube (Fig. 2N, have a narrow base and a dissected apex (two short O). Similarly the ovary base joins the tube at inter- and two longer finger-like protrusions, c. 1/3 of petal vals, resulting in cavities between the gynoecium and length) (Fig. 62). The androecium is polystemonous, androecial tube where nectar may accumulate with 13–16 stamens (Fig. 4C–J). The pattern can (revolver flower with only very short canals) (Fig. 2P). tentatively be described as two whorls with single The pedicel is articulated. antesepalous and double or triple antepetalous stamens. Anthers are tetrasporangiate, x-shaped, dor- Anatomy: Sepals have three (to five) main (and sifixed almost at the base, latrorse and non-versatile c. 12–14 secondary) vascular bundles; the main (Fig. 100). The connective is broad and thin; a protru- bundles remain separate in the fused calyx, but form sion is absent. Thecae dehisce by longitudinal slits, synlaterals within the floral base (e.g. Fig. 2Q). Petals which are not continuous over the connective; have three main (and one to four secondary) vascular endothecium-like tissue extends into the connective for bundles and one vascular trace. Stamens have a some distance but is not continuous across it. Fila- single vascular bundle. The dorsal carpel bundle ments are already longer than anthers in bud. The

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Figure 4. Cassipourea congensis (Marcarisieae; Rhizophoraceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. A–I, level of free sepals. B–J, level of free petals with incurved marginal elaborations. C–H, level of free stamens. C–F, level of completely postgenitally fused ventral slits of carpels. C, level of capitate stigma. D–F, level of symplicate style. G–I, level of synascidiate zone of gynoecium. H–J, level of androecial tube and nectary (shaded). I–J, level of floral cup. K–O, floral base and pedicel. K, nectary (shaded) in floral base. Scale bar, 500 mm. trimerous gynoecium is completely syncarpous (Figs 4, the style appears sunk into it (Figs 5G, 121). An apical 5); it is of angiospermy type 4. The globular superior septum is absent. Locules are widely separated ovary is synascidiate up to above the placenta (Fig. 5A, because of a massive floral centre. Below the placenta K, O); its dorsal side is shortly and abruptly bulged the septa epidermis shows signs of disintegration. The upwards above the level of insertion of the style so that short unicellular-papillate stigmatic lobes together

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Figure 5. Cassipourea congensis (Marcarisieae; Rhizophoraceae). Trimerous gynoecium at anthesis; pollen tube transmitting tissue (PTTT) shaded. A, schematic median longitudinal section. Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines; completely postgenitally fused areas are double-hatched; incompletely postgenitally fused areas are single-hatched. B–P, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. B–J, symplicate zone; level of compitum. B–H, level of completely postgenitally fused ventral slits. B–D, level of capitate stigma. I–J, level of incompletely postgenitally fused ventral slits. J–K, level of obturators. K–O, synascidiate zone; level of collateral ovules. P, Gynoecium base. Scale bars, 250 mm.

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 FLOWERS IN RHIZOPHORACEAE AND RELATIVES 341 form a single capitate stigma (the upper part of which stamen bundles to form bundle complexes. At some appears deceptively commissural as a result of the places, stamen bundles join petal bundles, or petal reflexing of the carpel tips) (Figs 5A–D, 130); secretion bundles join lateral bundles of adjacent sepals, each appears to be absent at anthesis. Completely postgeni- forming bundle complexes. Together these bundle tally fused ventral slits extend throughout the style to complexes constitute a stele. below the stigma (Figs 4C–E, 5A–H); they are incompletely postgenitally fused (see Glossary for term) in Histology: Tanniferous tissue is present in all floral the symplicate zone of the ovary. Individual carpellary organs. A distinct band of large cells with tannins and stylar canals and a gap in the centre of the gynoecium numerous vesicles (laticifers?) is present in the meso- are absent. PTTT is confined to the inner carpellary

phyll of the sepals and ovary (Figs 175, 182, 186). In Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 angle of the ventral slits for the majority of the style; the ovary, to the outside of this band the tissue is it lines the ventral slits as c. 12–15 cell layers below small-celled and cytoplasm-rich. Cells with oxalate the stigma, diminishing to c. eight cell layers at the crystals and druses are present in the sepals, anthers mid style, c. five cell layers in the lower style and three and gynoecium. Stomata are present on the dorsal cell layers at the top of the ovary. Below the placental surface of the sepals (raised) and on the androecial region, PTTT is still present for a short distance on the tube (nectar pores). Unicellular lignified tanniferous ventral wall of the locule. A short compitum is present hairs are present on both surfaces of the sepals and at the stigma and also in the lower style and sympli- on the lower style and ovary. cate region of the ovary (Fig. 5B–J). Placentation is lateral, axile and apical; multicellular obturators are present (Figs 5J, K, 158). Two collateral antitropous Cassipourea elliptica (Macarisieae) ovules are present per locule. Ovules are bitegmic, Morphology: (based on floral buds only, also that of the anatropous and (weakly?) crassinucellar (Fig. 173A). gynoecium). Flowers are bisexual and polysymmetric The upwards-facing, transverse micropyle is zigzag- (Fig. 6). The perianth is mostly tetramerous (two of 11 shaped. The semi-annular outer integument is four or buds observed with a pentamerous calyx, 11 buds five cell layers thick, the inner integument five cell observed). Sepals are the protective organs in the layers thick; both integuments are lobed. A distinctive tightly packed buds. They are thick, have a broad base endothelium of radially elongate cells is present. with a pointed tip and are valvate; they are congeni- However, the entire inner integument (and inner cell tally united into a calyx tube (Fig. 6A–D), tightly layers of the outer integument) is cytoplasm-rich, postgenitally connected above this tube by interdigita- together with the lobes of the outer integument near tion of short papillae (Figs 37, 38). The elaborate petals the micropyle. Adjacent stamen filaments join to form are slightly conduplicate; they have a narrow clawed a short androecial tube before joining the sepals and base and a broader blade with long dorsiventrally petals in a short floral cup. The inner surface of the flattened fimbriae along the margins (see also Endress androecial tube (especially in alternistaminate posi- & Matthews, 2006a); aestivation is open. Each petal is tions) and floral cup are nectariferous (Fig. 4H–J). intimately associated with a group of stamens, the Sepal margins are decurrent for a short distance on the petal fimbria incurved into the centre of the bud and floral base. The pedicel is articulated. protruding between the anthers such that it is not possible to remove a petal without also removing the Anatomy: Sepals have three (to five) main (and two to group of associated stamens in bud. Only very few four secondary) vascular bundles and three to five stamens are not associated with a petal in bud. The vascular traces (Fig. 4). Petals have three vascular androecium is polystemonous (c. 32 stamens) (Fig. 6). bundles and a single vascular trace; each finger-like The pattern can be tentatively described as two whorls protrusion of the petals has a single vascular bundle with multiple positions in the antesepalous and ante- (Fig. 4B, C). Stamens have a single vascular bundle. petalous radii. A nectariferous androecial tube with a In the carpels a broad dorsal band of bundles extends corona-like extension on its ventral side surrounds the to just below the stigma (Figs 4D, 5E). Much shorter base of the ovary (Fig. 6A–C): filaments of collateral lateral carpel bundles extend up to the lower style, pairs of antepetalous stamens join each above the including secondary lateral bundles. Synlateral carpel other stamens (Fig. 6B), which join individually lower bundles extend through the centre of the gynoecium down. Anthers are tetrasporangiate, elongate, sagit- up to the placenta where they anastomose and supply tate, dorsifixed (towards the base of the anther), the ovules (Fig. 5L–O). The ovule bundle ends in the introrse (but almost latrorse towards the apex of the chalaza (Fig. 173A). In the floral base, adjacent anther) and non-versatile; they are irregularly packed lateral sepal bundles join, some forming synlaterals; within the bud. The connective is broad; a short lateral carpel bundles also join at this level. Further protrusion is present; endothecium-like tissue is not down, dorsal and lateral carpel bundles join nearby continuous over the connective. Thecae dehisce by

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Figure 6. Cassipourea elliptica (Marcarisieae; Rhizophoraceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; A–D, level of fused sepals, androecial tube with nectary (shaded) and synascidiate zone of ovary. A, level of staminal corona on the ventral side of the still free stamen filaments. B, level of pairs collateral antepetalous stamen filaments joining. C–D, level of narrow petal bases joining androecial tube. Scale bar, 1 mm. longitudinal slits, which are not continuous over the petal fimbria is supplied by a single vascular bundle. connective. Filaments are shorter or of similar length Petals and stamens each have a single vascular trace. to the anthers in advanced bud. The trimerous gyno- The dorsal carpel bundle extends up to just below the ecium is completely syncarpous; it is of angiospermy stigma and it appears as a broad band of bundles in type 4. The globular superior ovary is synascidiate up the upper and lower style. Smaller, shorter main to above the placenta; its dorsal side is shortly and lateral carpel bundles extend from the ovary up to the abruptly bulged upwards above the level of insertion of lower to mid style; in the ovary wall, additional the style so that the style appears sunk into it. The lateral bundles are also present surrounding the short unicellular–papillate stigmatic lobes together locules. Large synlateral bundles extend up to the form a capitate stigma (the upper part of which placenta and supply the ovules. The ovule bundle appears deceptively commissural, the result of the ends in the chalaza. In the calyx tube, lateral bundles reflexing of the carpel tips). Individual carpellary of adjacent sepals may join to form synlaterals, which stylar canals are absent, but a short central gap is are joined by secondary lateral bundles in the floral present in the gynoecium, which extends from the base. In the androecial tube, bundles of collateral upper style to the stigma. The ventral slits appear to be antepetalous stamens join (Fig. 6C, D). Lower down completely postgenitally fused in the upper to mid in the floral base stamen bundles join petal bundles style, incompletely fused lower down. PTTT lines the and the synlateral carpel bundles join the dorsal and slits in the upper style as c. five to seven cell layers in lateral carpel bundles to form a ring of bundles the inner carpellary angle of the slits and narrows to in the centre of the flower. This ring is joined by one or two cell layers along the outer margins; it the stamen bundles and stamen/petal complexes. The diminishes to c. four cell layers lining the entire slits in sepal bundles are the last to join the ring, the syn- the lower style. A compitum appears to be present for lateral bundles joining the ring above the median the entire symplicate zone. Placentation is axile, sepal bundles. Together they form a stele. lateral and apical; extensive obturators are present. An apical septum is absent. Two pendant, collateral, Histology: Tanniferous tissue is present in all floral antitropous ovules fill each locule. Ovules are bitegmic, organs. A distinctive band of large cells with tannins anatropous, and crassinucellar. The micropyle is and numerous vesicles (laticifers?) are present in the formed by both integuments; it is a transverse slit. The sepals (Fig. 176); similar cells are present in the semi-annular outer integument is five cell layers thick, anther connective and androecial tube and form a the inner integument six (or seven) cell layers. Both distinct layer in the ovary mesophyll. Stomata are integuments are lobed. An endothelium is present. present on the dorsal sepal surface (some stomata Petals and then the ovary join the androecial tube a raised) and inner surface of the androecial tube short distance above the floral base. The pedicel is (nectar pores). Lignified, unicellular hairs are dense articulated. on the ventral side and sparse on the dorsal side of the sepals. Unlignified, unicellular hairs are sparse Anatomy: Sepals have three main (and two to four on the dorsal side of the petals and dense on the secondary) vascular bundles and three vascular ventral side and the margins. Cells with oxalate crys- traces (one median and two synlateral) (Fig. 6). Each tals are present in the sepals, petals, androecial tube

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 FLOWERS IN RHIZOPHORACEAE AND RELATIVES 343 and gynoecium (plus druses). Oxalate druses are also column). Only at the very base of the flower is present in cells of the anther connective. SEM images the tissue solid (Fig. 7T, U). In the symplicate zone, suggest that secretion is present in the ovary locule; the central column separates into five ridges (corre- however, this was not obvious in sections. sponding to the shared walls between the carpels) and they form incomplete remaining septa in the placental region. Each incomplete remaining septum Carallia suffruticosa (Gynotrocheae) supports two ovules (representing the ovules of two Morphology: (based on floral buds only, also that of adjacent carpels). Two collateral antitropous ovules the gynoecium). Flowers are bisexual, pentamerous, are present per carpel (Fig. 159); placentation is axile, isomerous, obdiplostemonous (see Glossary for term) lateral and apical. Obturators are absent. Ovules are and polysymmetric (Fig. 7). Sepals are the protective bitegmic, anatropous and (weakly?) crassinucellar. Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 organs in advanced buds (Fig. 31). They are thick, The median longitudinal slit-like, upwards facing have a broad base with a pointed tip and are micropyle is formed by both integuments. The semi- revolute–valvate; they are congenitally united for annular outer integument is five or six cell layers some distance above a floral cup and postgenitally thick, the inner integument seven or eight cell layers. connected in their free region. The elaborate petals Both integuments are lobed. An endothelium of radi- are conduplicate in bud; each petal enwraps a single ally elongate cells (but not cytoplasm-rich) cells is antepetalous stamen (Figs 7B–E, 52, 60). Petals have present. Petals and antepetalous stamen filaments a shortly bifid tip and a narrow base, the margins join the floral cup above the antesepalous stamen have slightly flattened lateral appendages, some of filaments. Nectary lobes in alternating positions with which have clusters of hairs arising from their tips the stamens protrude upwards and inwards from the (Figs 66, 67); aestivation is (somewhat involute–) rim of the floral cup (Fig. 7G); below the lobes, the valvate. Within the androecium, antepetalous thickened nectary tissue is continuous on the inner stamens attach slightly more to the outside than the wall of the cup (Fig. 7H, I). The flower is sessile and antesepalous stamens. The filaments of antepetalous articulated. stamens are longer and broader (but thinner) than antesepalous stamens. Anthers are tetrasporangiate, Anatomy: Sepals have three main (and one secondary) sagittate, dorsifixed towards the base of the connec- vascular bundles and three vascular traces (median tive, introrse and versatile (Fig. 103). The connective and two synlateral) (Fig. 7). Petals have c. four to is broad and thin; a short protrusion is present. seven vascular bundles and one vascular trace. Thecae dehisce by longitudinal slits, which are not Stamens have a single vascular bundle. A broad continuous over the connective; endothecium-like dorsal carpel bundle extends throughout the style up tissue does not extend into the connective. Filaments to below the stigma (Fig. 7A); lateral carpel bundles and anthers are of similar length. The completely are absent except for synlaterals, which supply the syncarpous gynoecium is of angiospermy type 2 ovules and extend up to the placenta (Fig. 7M, N); (Fig. 7A–N). The carpels are antepetalous. The infe- they form a ring in the central column in the synas- rior ovary is synascidiate up to below the placenta. All cidiate zone (Fig. 7P). The ovule bundle branches in five carpels together form a single capitate stigma the chalaza into several bundles, which extend into which is unicellular–papillate (Fig. 132). Five ventral the outer integument (Fig. 7M–P). In the floral cup slits extend up to below the stigma; they are incom- adjacent lateral sepal bundles join to form synlateral pletely postgenitally fused in the upper and lower- bundles and petal bundles join these to form bundle most parts of the style and in the placental region, complexes. Stamen bundles remain separate in the open in between. A central gap is present between the cup joining with either the sepal/petal complex (ante- carpels in the upper half of the style and above the petalous stamens) or the median sepal bundle (ante- placenta (Fig. 7B–G); individual carpellary stylar sepalous stamens) at the base of the cup. In the canals are absent. An apical septum is absent. The inferior part of the gynoecium, above the locule, the periphery of the ovary roof and locule walls mainly dorsal carpel bundles join the sepal/petal/stamen consists of tissue with large intercellular spaces. The complex to form a ring of ten large bundle complexes originally pentalocular ovary becomes entirely alternating with ten smaller bundle complexes (sepal/ unilocular during development, the result of disinte- antesepalous stamen); below the locule these bundle gration of most of the septal tissue and part of the complexes join the ring of synlateral carpel bundles to locular walls (Fig. 7J–P). A remaining central column form a stele of ten complex bundles. extends throughout the synascidiate zone and below (Fig. 7O, P). The centre of the gynoecium below the Histology: Tanniferous tissue and cells containing level of the ovules is mainly hollow because of almost oxalate druses are present in all floral organs. A complete tissue disintegration (except for the distinct layer of large cells is present in the dorsal

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Figure 7. Carallia suffruticosa (Gynotrocheae; Rhizophoraceae). Floral bud, bisexual, transverse section series; morphological surface drawn with a thicker continuous line, vascular bundles with thinner continuous lines; tissue remaining after partial disintegration of floral base drawn with a dotted line; postgenitally fused areas indicated by dashed lines. A–N, level of symplicate zone of gynoecium. A–H, level of style. A–F, level of free petals with marginal elaborations. A–E, level of free sepals. A, G–J, level of incompletely postgenitally fused ventral slits of carpels. B–G, level of gap in centre of gynoecium. B–F, level of free stamens. B–E, level of conduplicate petals surrounding antepetalous stamens. B–C, level of antepetalous anthers. D, level of antesepalous anthers. E, level of fused sepals. F–I, level of floral cup. G–I, level of nectary (shaded) on floral cup. G, level of nectary lobes (shaded) alternating with stamens. I, level of ovary roof. J–S, level of inferior ovary and floral base with disintegrating tissue. J–P, level of inferior ovary with disintegrating tissue including ovary septa. M–P, level of secondarily unilocular ovary and ovules; level of numerous vascular bundles in outer integuments. M–N, level of placenta. O–R, level of ovary and floral base with remaining central column. O–P, level of Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 synascidiate zone of gynoecium. Q–U, floral base and pedicel. Scale bar, 500 mm. ᭣ sepal hypodermis, floral cup and inferior part of the congenitally united along their outer margins for some flower (Fig. 179). Stomata are present on the dorsal distance above a floral cup (Fig. 8C–G) and are valvate side of the sepals and inner surface of the floral cup and postgenitally connected in their free region. The (raised nectar pores). thick elaborate petals are conduplicate in bud (Fig. 8B–E); each petal partially enwrapping an ante- Pellacalyx cristatus (Gynotrocheae) petalous stamen and the free tips of adjacent carpels Morphology: (based on stereo microscope and SEM (Fig. 59). Petals have a narrow base and a bilobed tip observations). Flowers are bisexual, polysymmetric, with several terete multicellular lateral appendages pentamerous, isomerous and obdiplostemonous. and a median arista (see Endress & Matthews, 2006a Sepals are the protective organs in advanced buds. for details); all appendages are inflexed into the centre They have a broad base, a pointed tip and are valvate. of the bud (Fig. 8B–G); petal aestivation is irregularly Sepals are congenitally united above the floral base valvate. Stamens are incurved in bud such that and postgenitally connected in the free region. The anthers of the longer, outer whorl of antesepalous elaborate petals are conduplicate and have terete stamens surround the style. Anthers are tetrasporan- vermicular appendages (see Endress & Matthews, giate, x-shaped, dorsifixed, introrse and versatile. The 2006a) (Fig. 65). Antepetalous stamens are longer than connective is broad without a protrusion. Thecae antesepalous ones. Their filaments fused into a long dehisce by longitudinal slits, which are not continuous tube but the free parts are very short, even at anthesis over the connective; endothecium-like tissue does not (Figs 86, 87). The upper part of the androecial tube is extend into the connective. Filaments are longer than on the dorsal side of the antesepalous stamens (i.e. the anthers already in bud; antesepalous filaments are antesepalous anthers are positioned on the inside wall broader than antepetalous ones. The (penta-) octo- to of the tube) (Fig. 87). Anthers are tetrasporangiate, decamerous gynoecium is of angiospermy type 4 x-shaped, dorsifixed (towards the base of the anther), (Figs 8, 9, 143–146); it is syncarpous for three quarters latrorse and versatile; thecae dehisce by longitudinal of its length; the free parts are reflexed in bud and at slits, which are not continuous over the connective anthesis; pairs of adjacent carpels may be united above (Fig. 104). All carpel tips together form a large capitate the completely syncarpous region (Fig. 144). The stigma and a thick style (Fig. 131); the mostly superior mostly superior, globular ovary is synascidiate in the ovary contains numerous ovules (eight or more per lower half of the locules (up to the mid-placental carpel). A floral tube is present. region) (Figs 8G–I, 9A, L, M), symplicate up to three quarters of the length of the style, and plicate above; Histology: Multicellular stellate hairs with unicellular its dorsal side is shortly and abruptly bulged upwards rays are present on the dorsal surface of the sepals. above the level of insertion of the style so that the style appears sunk into it (Figs 8E, 9A, G, 122, 127, 143). A short apical septum is present (Figs 8F, 9I). Locules Gynotroches axillaris (functionally female) are widely separated because of a massive floral (Gynotrocheae) centre. The capitate stigmas are unicellular–papillate; Morphology: Flowers are small, morphologically secretion appears to be present at anthesis (Fig. 145). bisexual, apparently functionally unisexual, polysym- Ventral slits extend up to below the stigma; in the metric, tetramerous (except for gynoecium) and diplos- plicate and upper symplicate zone they are open along temonous (see Glossary for term) (Figs 8, 9). Sepals are their outer flanks, incompletely postgenitally fused the protective organs in advanced buds. They are thick along their inner carpellary angle (Fig. 9A, C, D). The and have a broad base with a pointed tip; they are entire slits are incompletely postgenitally fused lower

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Figure 8. Gynotroches axillaris (Gynotrocheae; Rhizophoraceae). Floral bud, functionally female flower, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. A–E, level of free valvate sepals. B–F, level of free petals with marginal elaborations; level of symplicate zone of gynoecium with incompletely postgenitally fused ventral slits. B–E, level of conduplicate petals; level of style. B–C, level of stigmas. C–G, level of fused sepals. C–E, level of free incurved stamens. E, level of dorsally bulged-up carpels around style (on left side). F–G, level of androecial tube with nectary (shaded). G–I, level of synascidiate zone of gynoecium. G–H, level of floral cup with nectary (shaded). G, level of narrow petal bases joining androecial tube. I–M, floral base. I, level of inferior part of ovary. N, Pedicel. Scale bar, 500 mm. ᭣ down in the symplicate zone. A central gap is present the locules. In the floral cup, lateral sepal bundles Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 between the carpels in the upper style (Fig. 9A, C, D); join to form synlaterals and these are joined by petal individual carpellary stylar canals are absent. PTTT is bundles. The stamen bundles remain separate for confined to the inner carpellary angle of the ventral some distance, only joining the dorsal carpel bundles slits as a narrow strand of tissue (two or three cell below the level of the ovary. Median sepal bundles layers) in the upper symplicate zone; it lines the entire also join this bundle complex and in the stele four ventral slit of each carpel lower down, potentially large bundle complexes are present (Fig. 8N). forming a compitum (Fig. 9A, C–K). In the ovary PTTT lines the ventral slits as one (or two) cell layers. Histology: Tanniferous tissue and cells with oxalate Placentation is lateral and axile; four to six alternat- druses are present in all floral organs. Additionally a ing, syntropous ovules are present per locule (Figs 9A, distinct layer of large, radially elongate cells with 143, 146). Obturators and apical septa are absent. tannins and numerous vesicles (laticifers?) is present Ovules are anatropous, bitegmic and weakly crassinu- in the ovary wall (Figs 183, 187). Stomata (nectar cellar (Fig. 173B, C). The nucellus disintegrates pores) are present on the ventral surface of the andro- around the embryo sac. The integuments form a zigzag ecial tube and floral cup. Special mucilage cells and micropyle. The semi-annular outer integument is two unspecified mucilage cells (for terms, see Matthews & or three cell layers thick, the inner integument five or Endress, 2006) form a distinct layer in the mesophyll six cell layers. Both integuments are lobed. An endot- of both the perianth and inferior ovary region of the helium is present. Stamen filaments are united at the flower (Fig. 190). In the sepals they are present on the base into a short androecial tube, to which first the dorsal and ventral sides as two distinct layers and in petals and then the median parts of the sepals join the petals as a single dorsally positioned layer. Scat- (Fig. 8F, G) to form a short floral cup surrounding the tered mucilage cells are also present in these organs. gynoecium (Fig. 8H). A nectary is present on the inner In anthetic flowers (and to a lesser degree in bud) the surface of the floral cup and androecial tube (Fig. 8F– tissue at the base of the locules and within the ovary H). The pedicel is articulated. septum is spongy, with large intercellular spaces. This tissue may disintegrate in later development. Anatomy: Sepals have three main (and two second- Tanniferous unicellular lignified hairs are present on ary) vascular bundles and three vascular traces the sepal tips. (median and two synlateral) (Fig. 8). Petals have four to six vascular bundles and one vascular trace; a single bundle extends into each of the petal append- Gynotroches axillaris (functionally male) ages (Fig. 8B–G). Stamens have a single vascular (Gynotrocheae) bundle. The dorsal carpel bundle extends into the free Morphology: Flowers are small, morphologically region of the style below the stigma and follows the bisexual, probably functionally unisexual, tetra- bulged contour of the ovary wall from the style (penta-) merous (except for the gynoecium), polysym- (Figs 8, 9). The shorter main lateral carpel bundles metric and diplostemonous (Figs 9B, 10). Sepals are (and smaller additional lateral bundles) are restricted the protective organs in advanced buds (Fig. 32). to the ovary (Fig. 9I–M); they extend up to the ovary They are thick and have a broad base with a pointed wall near the upper part of the locules and may also tip; they are congenitally united for a short distance form synlateral bundles in the ovary wall. Lateral above a nectariferous floral cup, valvate and postgeni- bundles in the inner part of the septa supply the tally connected (by cuticular dentation) in their free ovules (Fig. 9K, L), extending into the lower sympli- regions (Figs 10D–I, 39, 40). The thick elaborate cate zone of the placenta (Fig. 9K); the ovule bundles petals are conduplicate; each petal surrounds an end in the chalaza (Fig. 173B, C). Below the placenta, antepetalous stamen and their marginal appendages the placental bundles form a ring in the centre of the are incurved into the centre of the flower (Figs 10B, gynoecium and join the dorsal carpel bundles below E, 53, 54, 64). The petal elaborations resemble those

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Figure 9. Gynotroches axillaris (Gynotrocheae; Rhizophoraceae). Gynoecium at anthesis; pollen tube transmitting tissue (PTTT) shaded. A–B, schematic median longitudinal sections; two carpels shown in median view. Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines; postgenitally fused areas are hatched. A, functionally female flower. B, functionally male flower. C–M, transverse section series of gynoecium of a functionally female flower; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. C–K, symplicate zone; level of compitum and incompletely postgenitally fused ventral slits. C–E, level of incomplete postgenital fusion of inner angle of ventral slits, flanks open. C–D, level of gap in centre of gynoecium. G, level of dorsally bulged-up carpels surrounding style. I–M, level of ovules. I, level of apical septum. L–M, synascidiate zone. M, level of inferior part of ovary. Scale bars, 250 mm. ᭣ Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 of the female flower; aestivation is quincuncial; it is Anatomy: Sepals have three main (and no or one open at the base. Petals have a very narrow attach- secondary) vascular bundles and three vascular traces. ment zone. Stamens are incurved in bud and at Petals have c. three vascular bundles and one vascular anthesis (Fig. 10C–H); antesepalous stamens are trace; a single bundle extends into each of the petal more incurved than antepetalous ones (Fig. 10C–E); appendages (Fig. 10). Stamens have a single vascular both whorls together form a nectariferous androecial bundle, which remains separate from other bundles in tube (nectary on inner surface of tube) with lobes the floral cup and also for some distance in the floral between the free filament bases (Fig. 88). Anthers are base (Fig. 10B–H). The dorsal carpel bundle ends in tetrasporangiate, x-shaped, dorsifixed (antesepalous the base of the column (topographically above the level ones at the base of the connective, antepetalous ones of the stigmas) and two branches from this bundle slightly above the base), introrse and versatile. They extend into each stigma (Fig. 10G). Synlateral bundles have crescent-shaped thecae, their base and apex are present in the centre of the gynoecium between the curved away from each other. The connective is thin locules and may also extend into the base of the and is broad on the dorsal side; a protrusion is absent. column. These synlaterals supply the ovules, ending in Thecae dehisce by longitudinal slits, which are not the raphe. Additional lateral bundles are present at continuous over the connective; endothecium-like the level of the locules. The lateral traces of adjacent tissue does not extend into the connective. Antesepa- sepals form synlaterals in the floral cup and these are lous stamens have slightly longer filaments and their joined by the adjacent petal trace. Lower down in the anthers are broader than antepetalous ones. Fila- floral base, antesepalous stamen bundles join the ments are longer than anthers already in bud. The median sepal bundles and antepetalous stamen completely synascidiate, 8–9-merous gynoecium is bundles join the sepal/petal bundle complex. Below the very short and located deep in the floral cup; it is of locules all carpel bundles merge and together they join angiospermy type 4 (Figs 9B, 10D–M, 147–149). Indi- the closest sepal/stamen or sepal/petal/stamen com- vidual unicellular–papillate stigmas (with secretion plex. These bundle complexes rearrange themselves present at anthesis) are located at the base of a into a stele of four vascular complexes (Fig. 10P). columnar protrusion (Figs 148, 149). The inner morphological surfaces of each carpel extend along the Histology: Tanniferous tissue and cells with oxalate columnar protrusion (Figs 9B, 10H); they do not druses are present in all floral organs. Raised stomata appear to communicate over the centre. PTTT is are present on the dorsal sepal surface and on the present in the stigma and appears to extend upwards inner surface of the floral cup (nectar pores). Special for a short distance into the column (Fig. 9B). No such mucilage cells are present in the mesophyll of the tissue was discernable at the level of the ovules or sepals, petals, ovary centre (column) and floral cup connecting the stigma to the ovary locules. A compi- (Fig. 191). Unicellular hairs are present at the sepal tum appears to be absent. Locules begin in the supe- tips and along the petal midrib. The tissue in the rior region below the level of the stigmas and outer periphery of the floral base is spongy and has continue into the inferior region (Figs 9B, 10I–M). large intercellular spaces. They are not equidistant, resulting in thick or thin septa between them. Placentation is axile and lateral. Obturators are absent. Each locule contains two or Bruguiera cylindrica (Rhizophoreae) three alternating, syntropous ovules. Ovules appear Morphology: Flowers are bisexual, polysymmetric, to be bitegmic, anatropous and weakly (?) crassinu- octomerous (except for the dimerous gynoecium) and cellar with an endothelium. Integuments and micro- diplostemonous (Figs 11, 12). Sepals are the protec- pyle are abnormally shaped. Petals join the tive organs in advanced buds. They are thick and androecial tube before joining the sepals to form a have a broad base with a pointed tip (Fig. 41); they floral cup. are congenitally united for a short distance (Fig. 11H,

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Figure 10. Gynotroches axillaris (Gynotrocheae; Rhizophoraceae). Floral bud, functionally male flower, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines. A–E, level of free sepals. B–E, level of free conduplicate petals with incurved elaborate margins. C–H, level of free incurved stamens. C–F, level of fused sepals. C–E, level of antepetalous anthers. E–M, level of synascidiate zone of gynoecium. D–J, level of nectary (shaded). D–H, level of antesepalous stamens. D–F, level of stylar column. D–E, level of androecial tube with nectary (shaded). E–I, level of floral cup with nectary (shaded). G, level of stigmas. H–L, level of locules. J–P, level of floral base and pedicel. J–K, level of placenta. Scale bar, 500 mm.

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Figure 11. Bruguiera cylindrica (Rhizophoreae; Rhizophoraceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; A–H, level of free valvate sepals. B–H, level of free conduplicate petals with marginal elaborations. B, level of plicate carpels. C–M, level of symplicate zone of gynoecium. C–L, level of gap in centre of gynoecium. C–I, level of style. D, level of petals enwrapping antepetalous anthers. E–G, level of petals enwrapping antepetalous and antesepalous stamens. H, level of androecial tube and petals joining androecial tube. I, level of ﬂoral cup with nectary (shaded). M–P, level of inferior ovary. N–P, level of synascidiate zone of gynoecium. Q–R, ﬂoral base and pedicel. Scale bar, 1 mm.

I) and are (slightly revolute–) valvate and are post- other) (Figs 11B–H, 58, 75; see also Endress & genitally connected for the remaining length by inter- Matthews, 2006a); each petal enwraps two stamens: digitation of their papillate margins (Figs 41, 42). The an antepetalous one towards the outside of the ﬂower elaborate petals are conduplicate for their entire and an antesepalous one towards the centre of the length and the margins of each petal are postgenitally ﬂower (Figs 11D–G, 58). Petals have a thick narrow coherent (ridged cuticles appressed against each base and a bilobed tip; they have a median arista,

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Figure 12. Bruguiera cylindrica (Rhizophoreae; Rhizophoraceae). Dimerous gynoecium at anthesis; pollen tube transmitting tissue (PTTT) shaded. A, schematic median longitudinal section. Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines. B–O, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. B′–E′, enlargement of B–E. B–J, level of open ventral slits. B, plicate zone. C–J, symplicate zone. C–I, level of compitum. C–H, level of gap in centre of gynoecium. H, level of apical septum. I–N, level of collateral ovules. I, level of micropyle. J–L, level of inner integument present on antiraphal side (absent on raphal side). J, level of unilocular ovary. K–N, synascidiate zone. L, level of extremely narrow septa between locules. O, Gynoecium base below locules. Scale bars, A, B–O, 500 mm; B′–E′, 250 mm. ᭣ Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 which is terete at its apex and crescent-shaped at its 13–19 cell layers thick, the shorter inner is eight cell base, plus two or three terete bristles on each side, layers thick. In bud, the inner integument is very arising from the upper part of the petal flanks. The short on the antiraphal side compared with the arista and the two adjacent bristles join the main raphal side (Figs 12J–L, 173D, E). Both integuments petal lower down than the more laterally positioned are lobed. The nucellus appears to disintegrate at bristles. Petal aestivation is valvate. Antepetalous anthesis along with part of the inner integument that stamens are longer than antesepalous ones. Antepeta- surrounds the embryo sac; on the remaining parts, a lous filaments are much thicker near their apex than cytoplasm-rich endothelium is present (Fig. 173D, E). at their base, where they are thinner and broader Stamen filaments are united at their base to form an than antesepalous ones. Stamen filaments are longer androecial tube (Fig. 11H); this tube is also joined by than anthers already in bud. Anthers are tetraspo- the petals lower down before fusing together with the rangiate, sagittate, dorsifixed (near the base of the sepals to form a floral cup whose inner surface is connective, thecae continue for a short distance below nectariferous (Fig. 11I). The pedicel is articulated. the connective), introrse (almost latrorse) and non- versatile. The connective is thick and it is broad on Anatomy: Sepals have three to five main (and c. four the dorsal side; a protrusion is present. Thecae to six secondary) vascular bundles and three (to five) dehisce via longitudinal slits, which are not continu- vascular traces (Fig. 11). Petals have c. eight to ten ous over the connective. Endothecium-like tissue does vascular bundles and one vascular trace. A vascular not extend into the connective. The gynoecium is bundle extends to the base of the arista and each of syncarpous, free only at the stigma; it is of the bristles (Fig. 11C, D). Stamens have a single angiospermy type 2 (Figs 11, 12). The deeply inferior vascular bundle. A dorsal carpel bundle extends ovary with a thick roof is synascidiate up to the mid almost up to the stigma. Lateral carpel bundles are region of the apical placenta (Fig. 12A, K–N). A short absent in the style (Fig. 12C–E, C′–E′). Ovules are apical septum appears to be present (Fig. 12H). Below supplied by a branch from a synventral bundle the placenta the septa are very thin, consisting of two (Fig. 12K). This bundle extends to the chalaza. It cell layers with large intercellular spaces. They are branches into the outer integument from the attach- thicker above and below this region. The punctiform ment region of the ovule and also from the chalaza stigma is unicellular–papillate (Fig. 135); secretion (Fig. 173E). Towards the base of the locules, the syn- appears to be present at anthesis. An open ventral slit lateral bundles join the synventral bundle; this extends throughout the symplicate zone as a gap in bundle splits into two smaller bundles, which extend the centre of the gynoecium (Figs 11C–L, 12C–H) and downwards and join the stele without fusing with is also present in the plicate zone. In the upper other bundles (Fig. 11L). Within the floral cup, vas- symplicate zone, this gap is lined by one or two cell cular bundles of the different floral organ whorls layers of PTTT and by two or three cell layers in the remain separate, joining only in the floral base where lower symplicate zone. A compitum appears to be antepetalous stamen and petal bundles join to form present for the majority of the style, absent only in bundle complexes. Lower down, at the level above the the uppermost part of the symplicate zone (Fig. 12A, ovary locules, petal/stamen complexes and antesepa- C–I). Placentation is axile, lateral and apical. Obtu- lous stamen bundles join to form a ring of bundles. rators are absent. Two pendant, collateral and anti- The dorsal carpel bundles may also join this ring. tropous ovules with an extensive median attachment Lateral bundles of adjacent sepals join to form syn- zone are present per carpel (Figs 156, 173E). They are laterals in the floral base and these together with the bitegmic, anatropous and crassinucellar (Fig. 173D, median sepal bundles form an outer ring of 16 E). The zigzag, open (T-shaped) micropyle faces bundles, which remains separate from the other upwards towards the roof of the locule (Figs 12I, 160). bundles down the pedicel. At the level of the placenta, The semi-annular, much longer outer integument is the petal/stamen/dorsal carpel bundle complexes

Figure 13. Ceriops tagal (Rhizophoreae; Rhizophoraceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; tissue remaining after partial disintegration of floral base drawn with a dotted line. A–I, level of free sepals. B–J, level of symplicate zone of gynoecium with a gap in the centre. B–I, level of conduplicate petals with marginal elaborations. B–F, level of style. C–I, level of petals enwrapping stamens. C–D, level of antepetalous anthers. D–E, level of antesepalous anthers. F, level of postgenital connection of petals via hairs. H–J, level of nectary (shaded). I–J, level of fused sepals. I, level of androecial corona on the ventral side of the still free stamen filaments. J–Q, floral base and pedicel. J–N, level of inferior ovary. J, level of unilocular (developmentally primary) ovary. K–P, level of partially disintegrated ovary and floral base. K–N, level of synascidiate zone of ovary, disintegrated ovary septa and developmentally secondarily unilocular ovary. P, level of central column. Scale bar, 1 mm. ᭤ Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 separate forming an inner and outer ring (Fig. 11M, has large intercellular spaces except at the zone with N); the bundles of the inner ring join to form two the coiled hairs. Antepetalous stamens are longer broad carpel synlateral bundles. In the pedicel, the than antesepalous ones, with a thicker filament. The outer ring of sepal bundles and the inner ring of androecial tube is very short (Figs 13J, 89). Anthers bundle complexes join to form a stele. are tetrasporangiate, sagittate, dorsifixed (towards base of anther), versatile and introrse in bud, second- Histology: Tanniferous tissue and cells with oxalate arily extrorse at anthesis because of the anther flip- druses are present in all floral organs. A distinct layer ping backwards. The connective is narrow and has a of large cells is present in the mesophyll of the sepals protrusion. Thecae dehisce by longitudinal slits, (Fig. 180). The tips of the arista and smaller bristles which are not continuous over the connective. contain elongate tracheoids (transfusion tissue). Endothecium-like tissue does not extend into the con- Stomata are present on both sepal surfaces (subsid- nective. The broad filaments are longer than the iary cells large in longitudinal section and extending anthers already in bud; they are S-shaped at their above the level of the guard cells on the sepal epider- apex. The gynoecium is syncarpous (Figs 13, 14); it is mis) and on the inner surface of the floral cup (nectar of angiospermy type 2. The inferior ovary is synas- pores). Unusual lignified, unicellular hairs with a cidiate up to above the placenta (Fig. 14I–M) and short stalk and an elongate bulbous top are present symplicate higher up. The short punctiform stigma on the petal flanks. The tissue of the ovary below the has short lobes (which appear falsely commissural, locules and also towards the base of the septum is the result of the reflexing of the carpel tips) (Fig. 14B, spongy and has large intercellular spaces (Fig. 151). C); they have unicellular elongate papillae; secretion The epidermis of the ventral sepal surface and the appears to be present at anthesis (Fig. 133). Open style are papillate. ventral slits extend throughout the symplicate zone and together form a central secretion-filled gap; this gap is largest above the placenta (Fig. 14D–H). PTTT Ceriops tagal (Rhizophoreae) is three or four cell layers thick in the regions Morphology: Flowers are medium-sized, bisexual, between the carpels in the upper style diminishing to polysymmetric, pentamerous (except for the trimer- two cell layers in the lower style. In the ovary roof it ous gynoecium) and diplostemonous (Figs 13, 14). is two or three cell layers thick in both median and Sepals are the protective organs in advanced buds. commissural regions. A compitum appears to be They are thick, have a broad base with a pointed tip present throughout the symplicate zone (Fig. 14A–H). and are valvate; they are postgenitally connected for An apical septum is absent. The lower part of the a short distance by the dentation of their thick ovary is entirely unilocular at anthesis, the result of cuticles above their congenitally united bases. The disintegration of most of the septum tissue between elaborate petals are conduplicate (see Endress & the carpels below the placental region (only a central Matthews, 2006a, for a detailed description) and each column and partial septa remain on the walls of the petal partly enwraps two stamens (Figs 13B–I, 51): locule) (Figs 14K–M, 152–157); at the base of the an antepetalous stamen towards the outside of the locule also the central column disappears and there flower and an antesepalous one towards the centre of are only detached remnants of spongy tissue the flower; aestivation of the incurved petals is (Fig. 14M). The axile placenta is lateral and apical; contort, open lower down. Adjacent petals are post- obturators are absent. Two collateral antitropous genitally linked together for a short distance at ovules are present per carpel. Ovules are hemianat- their mid length via helically coiled hairs (Juncosa & ropous, bitegmic and crassinucellar. The median slit- Tomlinson, 1987; Endress & Matthews, 2006a) like micropyle is formed by both integuments and is (Figs 13F, 51, 70, 74); the tissue of the petal flanks zigzag-shaped. The thicker semi-annular outer

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Figure 14. Ceriops tagal (Rhizophoreae; Rhizophoraceae). Trimerous gynoecium at anthesis; morphological surface drawn with a continuous line; tissue remaining after partial disintegration of floral base drawn with a dotted line; pollen tube transmitting tissue (PTTT) shaded. A–A′, schematic median longitudinal section; outline of parts just out of the median plane drawn with dashed lines. A, after disintegration of tissue in the ovary and confluence of the locules. A′, younger gynoecium with inner morphological surface before tissue disintegration. B–P, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines. B′–E′, enlargements of B–E. B–H, symplicate zone; level of compitum. B–C, level of reflexed stigma (appearing deceptively commissural). C–H, level of open ventral slits. D–H, level of gap in centre of gynoecium. G–M, level of inferior ovary. H, level of unilocular ovary (developmentally primary). I–M, synascidiate zone. J–M, level of collateral ovules and disintegration of septa (arrows). K–P, level of tissue disintegration in floral base including ovary. K–N, level of numerous vascular bundles in raphes. L–M, level of developmentally secondarily unilocular ovary; level of ‘central column’ by disintegration of septa Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 (arrows). K, level of micropyles. N–P, level of secondarily extended locule due to tissue disintegration in the floral base. Scale bars, 500 mm (A, A′, B–P); 250 mm(B′–E′). ᭤ integument is 11–15 cell layers thick; the inner four present in the partially disintegrated septum at the cell layers. Both integuments are lobed. The nucellus base of the locule. Additional smaller carpel lateral appears to disintegrate at anthesis along with part of bundles surround the locule and towards the base of the inner integument which surrounds the embryo the flower these bundles join the bundle complexes sac. An endothelium is absent. Above the very short forming a stele. androecial tube nectary lobes alternate with the stamens (Fig. 13H). Pairs of adjacent lobes join each Histology: Tanniferous tissue and cells with oxalate other on the ventral side of the antepetalous stamens druses are present in all floral organs. A few larger (Fig. 13I); these pairs join to form a corona-like thick- cells are present in the mesophyll of the sepals, ened nectariferous ring on the inside of the stamen without forming a distinct layer; similar cells are filaments (Figs 13I, 89). Petals join this tube. A floral present in the ovary wall (Figs 184, 188). The sepal cup is absent. The flower is sessile. epidermis is papillate and has a thick cuticle; the mesophyll contains sclereids concentrated on the Anatomy: Sepals have three (to five) main (and five to ventral side. Stomata are present on the dorsal seven secondary) vascular bundles and up to five surface of the sepals (stomata raised) and dorsal vascular traces in the upper part of the floral base, surface of the nectary lobes (nectar pores). Tracheoids reduced to three vascular traces (median and two are present in the thickened tips of the petal bristles. synlateral) lower down near the level of the locules Lignified, tanniferous, unicellular hairs are present (Fig. 13). Petals have c. 13 vascular bundles and one on the petals: straight hairs are sparse on the dorsal vascular trace. Stamens have a single vascular bundle. surface, whereas helically coiled hairs are dense on A dorsal carpel bundle extends up to just below the the margins. The tissue of the ovary septa and sur- stigma (Fig. 14D). Main lateral carpel bundles are only rounding the locules is spongy, with large inter- present in the ovary (and lower style), together with cellular spaces (e.g. Figs 152–157). additional secondary lateral carpel bundles (Fig. 14F). These secondary bundles may join the dorsal carpel Rhizophora mucronata (Rhizophoreae) bundles or adjacent lateral bundles. Synlaterals Morphology: Flowers are medium-sized, elongate, extend into the septa of the ovary and supply the bisexual, polysymmetric, tetramerous (except for the ovules; they form a ring of bundles in the remaining dimerous gynoecium) and diplostemonous (Figs 15, central column of the ovary. The ovule vasculature 16). Sepals are the protective organs in advanced buds; forms a semi-circular bundle complex in the raphe near the apex their ventral surface is irregular, (Fig. 14K, L), which extends as individual bundles into marked by impressions of the tightly packed inner the chalaza and outer integument (Fig. 14M). In the organs, especially the petals (Fig. 15A–F). Their tips floral base, lateral bundles of adjacent sepals join to are incurved forming a prominent median ridge form synlaterals, and antepetalous stamen bundles flanked on either side by a petal (Fig. 15A–C). Sepals join petal bundles. Petal/stamen complex bundles join are thick, have a broad base with a pointed tip and a the sepal synlaterals lower down to form large complex congenitally united base is largely absent. They are bundles in antepetalous positions. Antesepalous valvate and are postgenitally connected by interdigi- stamen bundles and median sepal bundles join to form tation of their papillate margins. The thick, narrow additional complexes. Additionally, at the level of the petals have two or three short lateral lobes at their locule, dorsal carpel bundles may join adjacent petal/ apex (median lobe absent) and a narrow attachment stamen complexes. Synlateral carpel bundles are (Fig. 68). They are incurved in bud and reflexed at

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Figure 15. Rhizophora mucronata (Rhizophoreae; Rhizophoraceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. A–G, level of free valvate sepals and conduplicate petals. B–G, level of anthers. C, level of plicate carpels with open ventral slits. D–J, level of symplicate zone of gynoecium. D–H, level of incompletely postgenitally fused ventral slits of carpels. G–I, level of floral cup with nectary (shaded). G, level of short stamen filaments (partially fused with floral cup). J–M, level of inferior ovary. I–J, level of gap in centre of gynoecium. K–M, level of synascidiate zone of ovary. N, floral base. Scale bar, 1 mm.

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 FLOWERS IN RHIZOPHORACEAE AND RELATIVES 359 anthesis; each petal enwraps an antepetalous stamen to be present in the symplicate zone (Fig. 16A, E–K). (Figs 15A–G, 47, 48). Petals are caducous. The andro- Individual carpellary stylar canals are absent. The ecium has an outer whorl of shorter antesepalous axile placenta is lateral and almost apical; two stamens and an inner whorl of longer antepetalous pendant, collateral antitropous ovules are present per ones; their filaments may join to form a partial andro- carpel (Fig. 161). Obturators are absent. Ovules are ecial tube or they may join directly with the ventral bitegmic, anatropous, crassinucellar and pachycha- side of the sepals (antesepalous stamens) or petals lazal (Fig. 173F). An endothelium is present as a layer (antepetalous stamens) (Fig. 15G). The elongate, of cytoplasm-rich cells (but not radially elongate). The wedge-shaped anthers are sagittate, dorsifixed (almost nucellus appears to disintegrate at anthesis along with basifixed), introrse and non-versatile (Fig. 105); the part of the inner integument, which becomes contigu- antesepalous anthers are broader than the antepeta- ous with the embryo sac. The upwards facing zigzag Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 lous ones. Anthers are polysporangiate (Fig. 15C–G); micropyle is formed by both lobed integuments; the pollen sacs are divided transversely and longitudinally semi-annular outer integument is longer on its anti- into many smaller microsporangia (c. nine in trans- raphal side. The outer integument is c. 16–19 cell verse section). Already in advanced buds, individual layers thick; the inner integument c. 11–16 cell layers microsporangia become confluent within a theca. At thick. Above the ovary a floral cup is present which the anther apex, dehiscence is via a single median, appears to be lined by nectary tissue (Fig. 15G–I). The longitudinal slit between the thecae (not continuous margins of the sepals are decurrent on the floral cup. over the connective) (Fig. 15B), which lower down The pedicel is articulated. bifurcates into two slits, one in each theca to form a median valve to release the pollen (Fig. 15C, D). The Anatomy: Sepals have three main (and c. seven sec- anther connective is thick and narrow; it is especially ondary) vascular bundles and c. three vascular traces, thick in the region where up to four microsporangia are although a few additional bundles may continue into present per theca at the same level (in transverse the floral cup (Fig. 15). Petals have c. seven to ten section). The connective has a pointed protrusion. vascular bundles and a single vascular trace. Endothecium-like tissue is continuous over the dorsal Stamens have a single ring-shaped vascular bundle in side of the connective as a single cell layer in the upper the filament and floral base. In the floral cup, petal half of the anther, and as up to c. five cell layers in the bundles form bundle complexes with the lateral lower half. Anthers are almost sessile also at anthesis bundles of adjacent sepals (Figs 16H–I); median sepal (Fig. 105). The gynoecium is syncarpous, free only in bundles and stamen bundles remain separate in this the upper part of the style and stigma (Figs 15, 16); it region, joining adjacent bundles only in the zone of is of angiospermy type (2) – 3. The inferior ovary is the inferior ovary. Carpel vasculature extends up to synascidiate up to above the placenta (Fig. 16A, L–O). below the stigma where it forms a broad band, which An apical septum is absent. The septum between the separates into a dorsal and two lateral bundles in the carpels is thick at the level of the placenta, becoming lower plicate region (Fig. 16D). In the symplicate very thin and partially disintegrating in the lower part region of the style and below, numerous additional of the locule (gynoecium becoming unilocular) secondary lateral carpel bundles surround the main (Figs 16A, N, O, 150). The punctiform stigma is carpel bundles. In the inferior part of the gynoecium, unicellular–papillate (Fig. 136); secretion appears to secondary carpel bundles join with the main carpel be present at anthesis. Within each carpel a ventral bundles. Some additional lateral bundles extend into slit extends up to the stigma; it is mostly open along its the placenta and form synlaterals, which supply the outer margins (forming a gap in the centre of the ovules (Fig. 16M). The ovules are heavily vascularized gynoecium in the symplicate zone, especially above the and numerous bundles branch from the raphal side placenta) and incompletely postgenitally closed by and chalaza of the ovule into the outer integument PTTT along the median carpel regions in the style (Figs 16M–O, 173F). Below the placenta, carpel, (Fig. 16A). At the base of the style and in the ovary roof stamen, petal and sepal bundles join to form bundle (and for a short distance in the upper style) the entire complexes that surround the ovary locules. Below ventral slit is incompletely postgenitally closed. The the ovary locules, these bundle complexes form the slit is lined by c. five to seven cell layers of PTTT along stele. the inner carpellary angle and one to three cell layers line flanks in the plicate and upper to mid symplicate Histology: Tanniferous tissue and cells with oxalate zones, decreasing towards the base of the style to three druses (except sepals) are present in all floral organs; or four cell layers and one (or two) cell layers, respec- in the perianth organs, oxalate crystals are also tively; the epidermis of the PTTT is papillate. In the present. A distinct layer of large, radially elongate ovary roof, PTTT is restricted to a narrow band of cells is present in the ovary wall. Stomata are rare on tissue near the ovule attachment. A compitum appears the dorsal surface of the sepals and on the inner

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Figure 16. Rhizophora mucronata (Rhizophoreae; Rhizophoraceae). Dimerous gynoecium at anthesis; pollen tube transmitting tissue (PTTT) shaded. A, schematic median longitudinal section. Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines; postgenitally fused areas are hatched. Nucellus and part of inner integument disintegrated at anthesis. B–O, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines; d, dorsal vascular bundle. B–D, plicate zone. B, C, J, K, level of open ventral slits. D–I, level of incompletely postgenitally fused ventral slits. E–K, symplicate zone; level of compitum. K–O, level of inferior ovary. K, level of unilocular ovary (developmentally primary). L–O, synascidiate zone. M–O, level of collateral ovules. N, O, level of extremely thin septum. Scale bars, 500 mm. ᭣ Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 surface of the floral cup (nectar pores). Scattered non-versatile; they have a narrow (broader towards sclereids are present in the sepals and continue into the base) and thin connective with a short papillose the floral cup as clusters of cells. The sepal epidermis protrusion (Fig. 107). Thecae dehisce by longitudinal is papillate with longer papillae on the ventral side. slits, which are not continuous over the connective. Petals have dense unicellular, tanniferous, lignified Endothecium-like tissue does not extend into the con- hairs on the ventral surface and lateral flanks on the nective. The filaments are slightly shorter than the dorsal side. Spongy tissue with large intercellular anthers in advanced buds, longer at anthesis; they are spaces is present surrounding the locules and includ- united to form an androecial tube in their lower half ing part of the ovary roof, the septa below the pla- (Figs 17E–J, 90). The upper rim of the androecial tube centa and for some distance below the locules forms a short lobe on the dorsal side of each antepeta- (Fig. 150). Only at the placenta does the tissue consist lous stamen and on the lateral sides of each antesepa- of small, densely packed cells. lous stamen (Figs 17E, 90). The gynoecium is trimerous but with only one carpel fertile, and is therefore pronouncedly monosymmetric; it is of ERYTHROXYLACEAE angiospermy type 4 (Figs 17, 18). Carpels are free in Erythroxylum cuneifolium the upper half of the style, syncarpous below. The Morphology: Flowers are small, bisexual, polysymmet- ovary is synascidiate up to the middle of the placenta ric (monosymmetric in the gynoecium), pentamerous of the fertile carpel, symplicate above (Fig. 18A). The (except for the trimerous gynoecium) and diplostemon- synascidiate zone is slightly shorter in the sterile ous (Figs 17, 18). Sepals are short with a broad base carpels (Fig. 18H). Locules of the sterile carpels espe- and pointed tip; they are revolute–valvate, making the cially are widely separated from each other because of bud pentangular at the base, and postgenitally con- a massive floral centre (Fig. 18H–O). The dorsal side of nected by interdigitation of the marginal papillae in each carpel is shortly and abruptly bulged upwards younger buds; they are congenitally united for a short above the level of insertion of the style so that the style distance (Figs 17J–M, 43, 44). Petals become longer appears sunk into it (Figs 18A, F, 123, 128). The than sepals and are the protective organs in advanced dorsally bulged area of each carpel joins with adjacent buds (Fig. 33). They are conduplicate with a rounded neighbouring carpels and with the style along its tip and a thick narrow base with an extremely narrow median region, resulting in short commissural slits attachment zone (Fig. 17A–K); they are three-lobed between the ovary and the base of the style (Fig. 18G). with two longer lateral lobes and one shorter central This bulging is more pronounced in the sterile carpels lobe and a ventral scale at the base (Figs 17C–G, 80); than in the fertile one. The upper part of the ovary the central lobe enwraps the filament of the antepeta- forms a thick roof over the locules (Fig. 18A). The lous stamen and each lateral lobe enwraps the theca of stigmas are capitate and 1–3-cellular–papillate an adjacent antesepalous anther (Figs 17B–E, 55, 56, (Fig. 138); secretion appears to be absent at anthesis. 61). The petal flanks and ventral scales of adjacent The free parts of the styles are apparently unifacial petals are postgenitally hooked together (Fig. 77). (Fig. 18A–C). In the symplicate zone, ventral slits may Petal margins are thin (including those of the ventral be either completely or incompletely postgenitally scale). Aestivation is quincuncial, valvate only at the fused. Only at the level of the placenta are all three base. The androecium has a whorl of shorter antese- carpels connected by incompletely postgenitally fused palous stamens and a whorl of longer antepetalous ventral slits (Fig. 18G, H); a compitum may be present ones, which attach almost at the same level. Antese- in this zone (Fig. 18A, E–I). Individual carpellary palous stamens have thicker and broader filaments stylar canals are absent but a small, short central gap than antepetalous ones. Anthers are tetrasporangiate, is present between the carpels in the symplicate zone basifixed, sagittate, latrorse (slightly introrse) and of the bud (absent at anthesis) (Fig. 17C). PTTT

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Figure 17. Erythroxylum cuneifolium (Erythroxylaceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. A–K, level of free petals. B–E, level of free stamens. B, level of unifacial zone of carpels and capitate stigmas. C–K, level of free sepals. C–G, level of ventral scales of petals. C–F, level of symplicate zone of monosymmetric gynoecium with one fertile carpel. E–J, level of androecial tube. E–G, Level of petals postgenitally hooked together above a free valvate base. G–I, level of androecial tube with nectary (shaded) in alternistaminal positions; level of synascidiate gynoecium. H–L, level of revolute valvate sepals. J–M, level of fused sepals. J, level of valvate petal bases; level of androecial tube with nectary (shaded) surrounding gynophore. K–M, level of petals joining androgynophore. K, level of androgynophore. L–Q, floral base and pedicel. Scale bar, 500 mm. ᭣ Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 extends as a narrow central strand in each carpel ovary but are absent in the style, or only rudimenta- throughout the style, up to the stigma. Because the rily present in the symplicate zone (Fig. 18G). Addi- carpels are unifacial here, it is not connected to the tional smaller lateral carpel bundles are present in morphological surface in this region. PTTT extends as the ovary, extending above the placenta. A median one or two cell layers over the entire upper placental ventral bundle supplies the ovule of the fertile carpel region of the fertile carpel. In the symplicate region of (Fig. 18K); it is joined by smaller lateral carpel the ovary, PTTT is present as 1–2 cell layers lining the bundles at this level. The sterile ovules of the other ventral wall of the locule of the sterile carpels. An two carpels are supplied in the same way, somewhat apical septum is absent. The single antitropous ovule lower down. The three median ventral bundles from in the fertile carpel has a median axile placenta which the ovules are supplied are reorganized lower (Figs 162, 163). It fills the locule; it is anatropous, down and appear to form two synlaterals between the bitegmic, weakly crassinucellar and pendant fertile carpel and the two sterile carpels plus two (Fig. 173G). An obturator is present (Figs 18H–J, 162). lateral bundles on the flanks of the two sterile carpels The narrow and thin micropyle formed by the inner as they are further apart from each other (see above, integument faces upwards (Fig. 162). The outer ovary symmetry). The broad ovular bundle (some- integument is semi-annular, it is three cell layers times appearing as two collateral bundles) ends in the thick, the inner five to eight cell layers; both integu- chalaza (Figs 18O, 173G). Below the ovary locules, ments are lobed. An endothelium is present. The the lateral and synlateral carpel bundles are joined nucellus disintegrates around the sides and apex of the by smaller lateral bundles; lower down, the dorsal embryo sac at anthesis. In each of the two sterile and lateral bundles form a central complex. At the carpels an elongate, incompletely developed, convo- floral base, at first antesepalous stamen bundles, then luted ovule is present (although sterile, the locule size antepetalous stamen bundles and then petal bundles and ovary wall resemble that of the fertile carpel) join the central bundle complex. Smaller lateral sepal (Figs 18A, 163); placentation is axile and asymmetri- bundles join the main lateral sepal bundles towards cal (although tending towards median, it is slightly and in the floral base. Lateral bundles of adjacent offset from the midpoint of the carpel) and is at mid sepals form synlaterals in the floral base such that length of the locule (Fig. 18K–L). A short gynophore together ten sepal traces are present, which join the and androgynophore are present (Fig. 17J–M). The central complex to form a stele, with the synlateral floral base is convex, such that the sepals attach below traces joining slightly above the median ones. the other organs. A nectary is present on the outer side of the androecial tube, alternating with fused stamen Histology: Tanniferous tissue is present in all organs. filaments; at the base of the tube it gives the impres- A distinct hypodermal layer of large rounded cells sion of being restricted to the ventral side but does not (laticifers?) is present in the mid region of the sepals appear secretory on that side (Fig. 17H–J). The pedicel (Fig. 177). In the ovary, the hypodermis is distin- is articulated. guished by radially elongate cells with a rich cytoplasm and wavy anticlinal walls which are joined Anatomy: Sepals have three (to five) main (and one to together like jigsaw puzzle pieces (Figs 185, 189). three secondary) vascular bundles and three vascular Cells with oxalate crystals are present in the sepals, traces (one median and two synlateral) (Fig. 17). The petals and ovary. Stomata are present on the dorsal petal blade has five vascular bundles and the ventral sepal surface and outer surface of the androecial tube scale has two main and two to four secondary vascu- (nectar pores), although cytoplasm-rich tissue is more lar bundles. Each petal has a single vascular trace. concentrated toward the inner surface of the andro- Stamens have a single vascular bundle. In each ecial tube. The tissue of the ventral scale of the petal carpel, the dorsal bundle extends up to the stigma contains large intercellular spaces. The ventral sepal (Fig. 18B), lateral bundles extend up to the top of the epidermis is papillate.

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Figure 18. Erythroxylum cuneifolium (Erythroxylaceae). Trimerous, monosymmetric gynoecium at anthesis with one fertile and two sterile carpels; pollen tube transmitting tissue (PTTT) shaded. A, schematic median longitudinal section; upper sterile carpel (from transverse section series) also projected into the plane of the fertile carpel (on left). Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines; completely postgenitally fused areas are double-hatched; incompletely postgenitally fused areas are single-hatched;. B–P, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. B–C, unifacial style and stigma (only one carpel shown, B). C–F, level of completely postgenitally fused ventral slits. D–H, symplicate zone. E–I, level of incompletely postgenitally fused ventral slits and compitum. E–F, level of incompletely postgenitally fused ventral slits between fertile carpel and one sterile carpel with a compitum, the ventral slit of the other sterile carpel is completely postgenitally fused and the PTTT is conﬁned to the inner angle of the slit. H–J, level of obturators. I–O, synascidiate zone. J–O, level of ovules. Scale bars, Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 250 mm. ᭣

Nectaropetalum kaessneri lateral bundles extend up to the ovary. Two synlateral Morphology: (based on a single herbarium open bundles extend into the ovary septum and supply the flower). Flowers are medium-sized, bisexual, pentam- ovules. The ovule bundle is broad (composed of a few erous (except for the dimerous gynoecium), polysym- smaller bundles?) and ends in the chalaza. Below the metric and diplostemonous. Sepals have a broad base locules the dorsal bundle is joined by the lateral and and a pointed tip; they are congenitally united at their synlateral carpel bundles. The bundles of the outer base and valvate above. The conduplicate petals are organs remain separate in the floral cup and floral much longer than the sepals in open flowers and are base. Lower down antepetalous stamen bundles join likely the protective organs in bud. They are elaborate petal bundles forming bundle complexes. These com- with a two-lobed ventral scale at the base. Anthers are plexes plus the antesepalous stamen bundles are tetrasporangiate, elongate, x-shaped, basifixed, non- joined by the ovary bundles. The sepal bundles form versatile, latrorse and without a connective protru- a ring that surrounds the central ring of bundles and sion. Thecae dehisce via longitudinal slits, which are lower down all bundles form a stele. not continuous over the connective. Endothecium-like tissue does not extend into the connective. Filaments Histology: Tanniferous tissue is present in all floral are much longer than anthers at anthesis; they join at organs. A distinct layer of large, radially elongate their base to form an apparently entirely nectariferous cells (laticifers?) is present near the periphery of the androecial tube, which surrounds the gynoecium and ovary wall. Sclereids are prominent in the sepals joins the perianth organs lower down, forming a nec- associated with the vascular bundles and extending tariferous floral cup. The gynoecium is syncarpous up into the floral base; sclereids also form a layer on the to the upper style; it is of angiospermy type 4. The outer epidermis of the inner integument of the ovules. superior ovary appears to be synascidiate up to above the placenta. The capitate stigmas are unicellular– Aneulophus africanus papillate. A compitum appears to be present in the Morphology: (based on open flowers only). Flowers are symplicate zone. Both a gap in the centre of the small, bisexual, polysymmetric, pentamerous (except gynoecium and individual stylar canals appear to be for the trimerous gynoecium) and diplostemonous absent. Placentation is axile and lateral. An apical (Fig. 19). Sepals are thick, have a broad base with a septum and obturator appear to be absent. Two ovules pointed tip and are valvate (slightly revolute); they are present per locule, a larger, fully developed upper are postgenitally connected for a short distance above ovule and a smaller undeveloped lower one. Ovules a short congenitally united zone by interdigitation of are bitegmic, anatropous (?) and crassinucellar (?). their papillate margins. Petals are the protective The outer integument is c. four cell layers thick, the organs in advanced buds (based on the presence of inner c. five cell layers. An endothelium is present. very short sepals and long petals in the open flower). Sepal margins are decurrent on the floral cup. The They appear slightly conduplicate with a thick, flowers are sessile. narrow base and a pointed tip; petal aestivation is valvate towards the base. The antesepalous stamens Anatomy: Sepals have c. ten main vascular bundles are slightly shorter and have a narrower, thinner and vascular traces. Petals have c. ten vascular filament than the antepetalous ones. Anthers are bundles and a single vascular trace. Stamens have tetrasporangiate, elongate, sagittate, basifixed (or a single vascular bundle. A dorsal carpel bundle slightly dorsifixed) latrorse and versatile (Fig. 108). extends up to below the stigma. The much shorter The connective is narrow and thin and has a short

of angiospermy type 4 (Fig. 19A). The superior ovary is synascidiate up to above the placenta. The stigmatic lobes together form a flattened receptive surface (individual stigmas are more capitate than punctiform in appearance) (Fig. 139); they are unicellular–papillate. Individual carpellary stylar B canals and a central gap in the gynoecium are absent. Open ventral slits are present in the stigmas; they are incompletely postgenitally fused in the base of the stigma and in the style (Fig. 19A). In the stigma three or four cell layers of papillate PTTT line the open Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 ventral slits, with six to eight cell layers of PTTT lining the slits in the plicate zone of the style, diminishing to four cell layers in the mid-symplicate zone C and two or three cell layers in the lower style. A compitum possibly extends throughout the symplicate zone. A short apical septum is present in the ovary (Fig. 19B). Locules are widely separated because of a massive floral centre. Placentation is apical, lateral and axile. Obturators are present (Fig. 19A, B). Two B collateral, pendant, antitropous ovules are present D per locule. Ovules are bitegmic, anatropous and C crassinucellar. The micropyle appears to be formed by both integuments; the outer integument surrounding the obturator. Both integuments appear to be three D cell layers thick. An endothelium is present. Nectarif- erous tissue appears to be present in the androecial tube, alternating with the stamens in the upper part E A E of the tube and lining the entire tube lower down (Fig. 19D, E). Petals may join the androecial tube Figure 19. Aneulophus africanus (Erythroxylaceae). above the floral base or at the convex floral base. Anthetic flower with trimerous gynoecium, bisexual; pollen tube transmitting tissue (PTTT) shaded dark grey; post- Anatomy: Sepals have one median and two (shorter) genitally fused ventral slits indicated by broken lines. A, lateral vascular bundles and three vascular traces schematic median longitudinal section of gynoecium. Mor- (median and synlaterals or laterals) (Fig. 19). Petals phological surface drawn with a continuous line; outline of have c. five to eight vascular bundles and one vascu- parts just out of the median plane drawn with broken lines; lar trace. Stamens have a single vascular bundle. postgenitally fused areas are hatched. B–E, transverse Lateral carpel bundles extend up to the upper sym- sections; morphological surface indicated by thicker con- plicate zone of the style, while the shorter dorsal tinuous lines, vasculature by thinner continuous lines; level carpel bundles do not surpass the ovary; additional of free perianth. B–D, level of free stamen filaments. B, secondary lateral bundles are present in the ovary symplicate zone and level of apical septum. C–E, synascidi- wall. In the upper synascidiate zone above the pla- ate zone. D–E, level of androecial tube with nectary (shaded centa, lateral carpel bundles join to form a synven- light grey); it is not clear from the herbarium material whether the secretory surface is on the inner side of the tral, which supplies the ovules. The ovule bundle ends androecial tube. D, nectariferous areas alternating with in the chalaza. Adjacent lateral sepal bundles may stamens. Scale bars, 200 mm (A); 500 mm (B–E). join to form synlaterals in the congenitally united sepals or in the floral base. Antepetalous stamen bundles join petal bundles in the floral base and these protrusion. Thecae dehisce by longitudinal slits, complex bundles join sepal synlaterals; lower down which are not continuous over the connective. antesepalous stamen bundles join median sepal Endothecium-like tissue does not extend into connec- bundles. Together the bundles join the central ring of tive. Filaments and anthers are of similar length at bundles to form a stele in the pedicel. anthesis. The lower part of the filaments is flattened and adjacent stamens are united into a short andro- Histology: Tanniferous tissue is present in all floral ecial tube (Figs 19D, E, 91). The gynoecium is syn- organs. Additionally, a distinctive layer of large carpous, free only in the upper style and stigma; it is tannin-filled cells (laticifers?) is present in the sepal

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 FLOWERS IN RHIZOPHORACEAE AND RELATIVES 367 Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021

A B C D

E F G H

Figure 20. Ctenolophon englerianus (Ctenolophonaceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. A–F, level of corolla. A–B, level of unifacial style and stigma. A–D, level of free stamens. B, level of antepetalous anthers. C–F, level of synascidiate zone of gynoecium. C–E, level of free sepals and androecial tube. C–D, level of corona-like androecial tube (corona; shaded) on the dorsal side of the still free stamen filaments. E–F, level of convex floral base. E, level of short androgynophore. F, level of fused sepals; level of petals joining androgynophore. G–H, floral base and pedicel. Scale bar, 500 mm. hypodermis (Fig. 181). Similar cells are scattered in (Figs 20A–F, 34). They are simple with a narrow base the petals and form a hypodermal layer in the stamen and a rounded tip and are contort; they are postgeni- filaments and lower style and ovary. Cells with tally connected in bud along their overlapping oxalate druses and crystals are absent. Stomata are margins by dense stellate hairs on their exposed present on the dorsal surface of the sepal; stomata dorsal surfaces and margins (Fig. 76). The ten (nectar pores) were not observed on the androecial stamens are basally united into an androecial tube tube. Hairs are absent. (Figs 20C–E, 92–94). Alternating with them are ten lobes, which also form a corona-like tube at the base on the dorsal side of the stamens (Figs 20C, D, 92–94). CTENOLOPHONACEAE This tube unites with the androecial tube from the Ctenolophon englerianus dorsal side. Antesepalous stamens are longer than Morphology: (gynoecium description based on both antepetalous ones. Anthers are tetrasporangiate, sag- buds and anthetic flowers). Flowers are medium-sized, ittate, dorsifixed (near the base of the connective), bisexual, polysymmetric, pentamerous (except for the introrse and versatile (Fig. 109). The connective is dimerous gynoecium) and diplostemonous (Figs 20, broad on the dorsal side and a protrusion is present. 21). Sepals have a broad base with a rounded tip and Thecae dehisce by longitudinal slits, which are not are quincuncial; they are congenitally united for a continuous over the connective. Endothecium-like short distance. Petals are much longer than sepals tissue does not extend into the connective. Filaments and are the protective organs in advanced buds

B C B C D E

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Figure 21. Ctenolophon englerianus (Ctenolophonaceae). Dimerous gynoecium at anthesis. Pollen tube transmitting tissue (PTTT) shaded. A, schematic median longitudinal section. Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines. B–K, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; developmentally severed edge of septum drawn with dotted lines. B, plicate zone (one carpel shown). C–E, symplicate zone; level of gap in centre of gynoecium, open ventral slits and compitum. F–L, synascidiate zone. H–L, level of collateral ovules. H, level of obturators. I–J, level of micropyles. J–L, level of secondarily unilocular ovary because of developmentally severed septum. K′, enlargement of K showing central portion of ovary with incomplete, developmentally severed septum (arrows). Scale bars, 500 mm (A, B–K); 150 mm(K′).

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 FLOWERS IN RHIZOPHORACEAE AND RELATIVES 369 are much longer than anthers already in bud. The gynoecium is syncarpous, free only in the upper style and stigma; it is of angiospermy type 3 (Figs 20, 21). The mostly superior ovary (locules extending downwards into androgynophore) is synascidiate up to above the placenta; an apical septum is absent. Below the placenta the ovary becomes developmentally secondarily unilocular in parts, the result of the partial disintegration of the thin septa (Fig. 21J–L, K′). The capitate stigmas are unicellular–papillate (Fig. 140). Ventral slits are absent in the plicate zone (carpels Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 apparently unifacial) (Figs 20A, B, 21A). In the symplicate zone they are present as open slits, which Figure 22. Roucheria griffithiana (Hugonioideae; Lina- together form a gap in the centre of the gynoecium ceae). Transverse section of anthetic trimerous mono- (Fig. 21C–E). In bud, PTTT is present as isolated symmetric gynoecium; morphological surface indicated by central strands (c. ten cell layers) in the lower stig- thicker continuous lines, vasculature by thinner continu- matic regions and uppermost part of the styles. Short ous lines; pollen tube transmitting tissue (PTTT) shaded individual carpellary stylar canals in the upper sym- grey. Scale bar, 200 mm. plicate zone are lined by five cell layers of PTTT. At anthesis c. five cell layers line the central gap. Placen- tation is lateral, axile and apical with two pendant, the floral base, androecial and gynoecial bundles join. collateral, antitropous ovules present per locule Lower down, petal bundles join this bundle complex. (Fig. 164). Ovules are bitegmic, anatropous and Lateral sepal traces may join adjacent lateral sepal (weakly) crassinucellar (Fig. 173H); small obturators traces to form synlateral traces and these, together appear to be present (Fig. 165). The upwards-facing with the median sepal traces, join the ring of bundle micropyle is formed by both integuments and is complexes to form a stele in the pedicel. zigzag-shaped (Fig. 21I). Both integuments are lobed and the tips of the outer integument show small, Histology: Tanniferous tissue is present in all floral cytoplasm-rich cells. The semi-annular outer integu- organs. Cells with oxalate druses are present in the ment is c. five cell layers thick, the inner integument stamens. Special mucilage cells are scattered in the c. ten to 11 cell layers. A distinct endothelium is mesophyll of the sepals (Fig. 194). Stomata are rare present. The nucellus appears to mostly disintegrate on the dorsal surface of the petals and the outer around the embryo sac at anthesis. The androecial surface of the androecial tube (nectar pores). Stellate, tube joins the ovary near its base to form a short multicellular tanniferous hairs with unicellular rays androgynophore (Fig. 20E). The floral base is pro- are dense on the floral base, dorsal surface of the nouncedly convex and the gynoecium, androecium sepals and on the exposed parts of the petals but and corolla join the floral base well above the absent from those petal flanks that are covered by calyx (Fig. 20E, F). Distinctly defined nectariferous other petals (Fig. 76); below the level of the sepals, tissue was not identified in the androecial tube; the stellate hairs on the petals are not tanniferous. however, it is likely to be nectariferous. The pedicel is Unicellular, lignified tanniferous hairs are present on articulated. the lower style and ovary and on the petal margins near their base. Anatomy: Sepals have three to eight main (and c. six to 11 secondary) vascular bundles and one to three LINACEAE vascular traces (Fig. 20). Petals have c. 15–18 vascular bundles and one vascular trace. Stamens have a Roucheria griffithiana (Hugonioideae) single vascular bundle. The dorsal carpel vasculature Morphology: Flowers are small, bisexual, polysym- extends up to below the stigma as a broad crescent- metric, pentamerous (except for the trimerous gyno- shaped band of bundles (Fig. 20B); in the lower ecium, Fig. 22) and diplostemonous. The free sepals plicate zone it differentiates into a dorsal carpel are thick, have a broad base with a pointed tip and bundle and two lateral carpel bundles (Fig. 21D), are quincuncial. Petals are longer than sepals and are which form synlaterals in the lower style. Here and in the protective organs in advanced buds. They are the ovary additional lateral bundles are present. Two elongate, narrow and strap-like with an extremely synlaterals extend into the septum, where they join, narrow attachment zone; petals are conduplicate near branching in the placenta and supplying the ovules. their apex: they are contort and postgenitally con- The ovule bundle ends in the chalaza (Fig. 173H). In nected (free in their lowermost portion) via their

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 370 M. L. MATTHEWS and P. K. ENDRESS cuticles along their overlapping margins and together Hugonia acuminata (Hugonioideae) form a tube in bud. The androecium has a whorl of Morphology: (based on SEM and stereo microscope longer and broader antesepalous stamens and a whorl observations). Flowers are medium-sized, bisexual, of shorter and narrower antepetalous ones. Filaments polysymmetric, pentamerous, isomerous and are much longer than anthers already in advanced obdiplostemonous. Sepals are the protective organs in bud. The stamens form a nectariferous androecial bud except for just before anthesis, when the petals tube towards their base. Anthers are tetrasporan- are much longer. Sepals are quincuncial, thick, espe- giate, sagittate, dorsiﬁxed, introrse and versatile; a cially the outer three (the inner two are completely short protrusion may be present. Thecae dehisce by enclosed in bud and are thinner and more petal-like) longitudinal slits, which are not continuous over the

and elongate with a broad base and a pointed tip. Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 connective. Endothecium-like tissue is continuous Sepals reflex in bud and at anthesis. Petals are over the dorsal and ventral sides of the connective. clawed, with a narrow base and a very narrow attach- The gynoecium is syncarpous to just above the supe- ment zone and a broad, rounded blade; they appear to rior ovary, free above; it is of angiospermy type 4 be peltate with a cross zone at the base (Fig. 81). (Fig. 22A). The ovary is synascidiate up to within the Aestivation is contort. The androecium has a whorl of placenta. The two-lobed, capitate stigmas are longer, narrower antepetalous stamens and shorter, unicellular–papillate. A ventral slit is present up to broader antesepalous ones; they are joined at their the stigma; it is incompletely postgenitally fused base into an androecial tube, which is thickened and along its inner carpellary angle, open at its flanks. nectariferous on the dorsal side in the antepetalous PTTT appears to line the ventral slit as c. two cell sectors. Anthers are tetrasporangiate, sagittate, dor- layers in the plicate and symplicate zones and a sifixed, and versatile; a connective protrusion is compitum appears to be present in the symplicate present (Figs 110, 111). Thecae dehisce by longitudi- zone. A central gap between the carpels is present in nal slits, which are not continuous over the connec- the upper symplicate zone and just above the synas- tive. Filaments are much longer than anthers at cidiate zone; carpellary stylar canals are absent. anthesis. The gynoecium is syncarpous in the supe- Locule size is unequal between the three carpels rior ovary, free above. The stigmas are capitate. The (Fig. 22). A short apical septum may be present in carpels are antepetalous; they are shortly and some carpels, absent in others. Obturators are abruptly bulging upwards above the level of insertion present. Placentation is lateral and axile; two collat- of the style so that the style appears sunk into it eral antitropous ovules are present per carpel. Ovules (Fig. 124). Placentation is axile in the uppermost part are anatropous and bitegmic. An endothelium is of the ovary. Two collateral antitropous ovules are present. The micropyle is formed by both integu- present per locule. Obturators appear to be present. ments. The floral base is slightly convex; the sepals The pedicel is articulated. are the last organs to join the floral base. Flowers are sessile. Linum kingii (Linoideae) Anatomy: Sepals have c. three to five main (and Morphology: Flowers are medium-sized, bisexual, c. seven to nine secondary) vascular bundles and one polysymmetric, pentamerous, isomerous and haplos- to five vascular traces. Petals have c. nine vascular temonous (Fig. 23). Sepals are thick, have a broad bundles and a single vascular trace. Stamens have a base, toothed margins and a pointed, terete tip; they single vascular bundle. A dorsal carpel bundle are congenitally united for a short distance and are extends up to below the stigma; the shorter lateral quincuncial above (Fig. 23K, L). Petals are longer bundles extending up to the mid style. Additional than sepals and are the protective organs in advanced lateral bundles are present in the lower style and buds (Figs 23A–G, 35); they are clawed with a narrow some extend up to the placenta and supply the base (and an even narrower attachment region) ovules; they may join to form synlaterals at or (Figs 82, 83) and a broad, rounded tip. A thickened above the placenta. Antepetalous stamen bundles ventral midrib is especially well developed towards join the petal bundles. Petal/stamen complexes, the base of the petal, contributing to the revolver antesepalous stamen bundles and carpel bundles architecture of the flower (Figs 23E–G, 82, 83). join before forming a stele together with the sepal Midribs of adjacent petals delimit a nectar canal, bundles. together with a stamen filament; aestivation is contort in the blade region (the bud shown has an Histology: Tanniferous tissue is present in all floral irregular interpetal position, which has disrupted the organs. Stomata are present on the dorsal sepal contort pattern), valvate near the base. Close to the surface. Nectar pores were not found on this her- level of attachment of the petals adjacent petals are barium material. postgenitally hooked together and are probably

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E F G

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Figure 23. Linum kingii (Linoideae; Linaceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. A–G, level of free petals. B–J, level of free sepals. B–C, level of unifacial zone of styles. D, level of plicate zone of styles. C–G, level of free antesepalous stamens. D–E, level of incompletely postgenitally fused ventral slits of carpels. E, level of symplicate zone of gynoecium. F–H, level of synascidiate zone of gynoecium. H–J, level of petals postgenitally hooked together above a free valvate base and petal attachment via a narrow base. H–I, level of androecial tube. I–L, level of convex ﬂoral base. I–J, level of nectary (shaded) on dorsal side of androecial tube. I, level of partial androgynophore and gynophore. J–L, level of fused sepals. L–P, ﬂoral base and pedicel. Scale bar, 250 mm.

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 372 M. L. MATTHEWS and P. K. ENDRESS involved in providing a strengthened access canal to ary septum is rich in intercellular spaces. Obturators the nectar chamber below (Figs 23H–J, 71, 78). are present (Figs 24I, J, 166, 167). Two collateral, Stamens are antesepalous; they are united into an pendant antitropous ovules per carpel completely fill androecial tube, to which the petals are attached the locule (Fig. 166); they are bitegmic, anatropous (Figs 23H–J, 95). Each stamen has two small lateral and incompletely tenuinucellar (Fig. 173I). The micro- appendages just above the rim of the androecial tube pyle is formed by the inner integument. An endothe- (Figs 23G, 95). Antesepalous nectaries are present on lium is present. The narrow nucellus disintegrates the outside of the stamen bases below the level of around the embryo sac. The shortly annular outer attachment of the petals (Figs 23I, J, 95); it is likely integument extends around the obturator (Fig. 24J); that nectar would accumulate in the cavities created it is unlobed and two cell layers thick. The lobed inner by the interlocked margins of adjacent petals. Anthers integument is seven to ten cell layers thick; the inner Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 are tetrasporangiate, elongate, sagittate, dorsifixed integument and nucellus are elevated above the towards the base of the connective, slightly introrse outer integument by a short basal stalk. A short (almost latrorse) and versatile (Fig. 112). Thecae are gynophore is present above the floral base. The floral bulged outwards such that the dorsal side of the base is extremely convex and the gynoecium, andro- connective is partially hidden. The connective is ecium and corolla join the floral base well above the narrow and thin near the apex and broad and thick sepals (Fig. 23I–L). The petal base bulges downwards towards the base of the anther; a protrusion is absent. into the cavity between the convex floral base and the Thecae dehisce by longitudinal slits, which are not sepals. The pedicel is weakly articulated. continuous over the connective. Endothecium-like tissue does not extend into the connective. Filaments Anatomy: Sepals have one main (and c. four second- are shorter than anthers in advanced bud but longer ary) vascular bundles forming three vascular traces at anthesis. The antepetalous carpels are united up to (median and two synlateral) (Fig. 23). Petals have the base of the long, narrow free styles, which reflex c. eight to 11 vascular bundles and one vascular trace. at anthesis; the gynoecium is of angiospermy type 4 Stamens have a single vascular bundle. A median (Figs 23, 24). The superior ovary is synascidiate up to carpel bundle extends throughout the style up to just above the placenta (Fig. 24A, G–J). Capitate stigmas below the stigma (Fig. 24). Individual lateral carpel are unicellular–papillate (Fig. 141); secretion appears bundles are absent, but synlateral bundles extend to be absent at anthesis. The free styles are unifacial along the ovary wall (Figs 24I–N). Additional (inner) except at their base (Fig. 24B–D). At the stylar base synlateral bundles supply the ovules (Fig. 24K, L); there is a symplicate zone, where the ventral slits are below the placenta they form a ring of bundles in the incompletely postgenitally fused along the inner car- centre of the gynoecium. The ovule bundle ends in the pellary angle and open at the flanks (Fig. 24A). Above chalaza (Fig. 173I). Above the floral base the petal the ovary locules the ventral slits are incompletely trace joins the androecial tube and petal and stamen postgenitally fused. In the upper synascidiate zone traces alternate in the base of the tube. The dorsal the slits are present inside the locule between the carpel bundles join the ring of synlaterals bundles in obturators. A short central gap is present in the the gynophore (Fig. 24P). Petal and stamen traces uppermost part of the symplicate zone (Fig. 24E, F); remain separate down to the convex floral base, when individual carpellary stylar canals are absent. PTTT the outer synlateral carpel bundles join the stamen is present as a central strand in the upper free styles traces to form five complexes alternating with the five (c. 12 cell layers in diameter); towards the base it petal traces. The carpel/stamen bundle complexes join moves more towards the ventral side of the free the central ring of bundles. Each petal trace and styles. Six cell layers are present, lining the inner median sepal bundle initially remain separate, then carpellary angle of the ventral slit at the base of the petal traces join synlateral sepal bundles. Together free styles, diminishing to three to five cell layers in these bundle complexes plus each median sepal the upper symplicate zone, and two or three in the bundle join the central ring of bundles to form a stele lower symplicate and upper synascidiate zones. Uni- in the pedicel. cellular secretory papillae line the central gap and are continuous with the PTTT lining the ventral slits. A Histology: Tanniferous tissue is present in the stigma compitum is potentially present throughout the sym- and ovary. Special mucilage cells are present in the plicate zone. Placentation is lateral, axile and apical. dorsal and ventral sepal epidermis (Fig. 196). An apical septum is absent, but each locule is subdi- Stomata are present on both sepal surfaces and on vided by a secondary septum that protrudes from the the nectary (nectar pores). The petal epidermis shows dorsal side (Fig. 24H–O). It is most conspicuous at the multiple periclinal divisions near the margins. Sclere- base where each locule is completely subdivided ids are present in the ventral epidermis of the sepals (Fig. 24O). The tissue of the upper part of the second- towards their base. Unlignified, unicellular hairs are

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Figure 24. Linum kingii (Linoideae; Linaceae). Pentamerous gynoecium at anthesis. Pollen tube transmitting tissue (PTTT) shaded. A, schematic median longitudinal section. Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines; postgenitally fused areas are hatched. B–P, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines. B–D, level of unifacial style and stigma (only one carpel shown). B′–D′, enlargement of B–D. B, level of stigma. D–E, plicate zone. E–J, level of incompletely postgenitally fused ventral slits. E–H, symplicate zone. E–F, level of gap in centre of gynoecium. F–H, level of compitum. I–O, synascidiate zone. H–O, level of secondary septa. I–J, level of obturators and incomplete postgenital fusion of ventral slits in synascidiate zone. J–N, level of ovules. J, level of micropyles. O, base of locules; level of complete division of locules by secondary septa. P, gynoecium base below locules. Scale bars, 500 mm (A); 250 mm (B–P, B′–D′).

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 374 M. L. MATTHEWS and P. K. ENDRESS present on the ventral surface of the petals. Two more extensive in their lateral portions (Fig. 142); distinct adjacent files of cells radiate from the centre they are unicellular–papillate with large round papil- of the gynoecium in alternicarpellous positions and lae; secretion appears to be absent at anthesis. An are probably involved in fruit dehiscence. The outer open ventral slit is present directly below the stigma. c. three cell layers of the ovary are particularly In the remaining plicate and in the upper symplicate cytoplasm-rich. The tissue in the centre of the ovary zone the slits are open along their flanks and incom- has large intercellular spaces. pletely postgenitally fused along their innermost carpellary angles (Fig. 26A, C–E). In the lower style and symplicate region of the ovary the entire slits are Reinwardtia indica (Linoideae) incompletely postgenitally fused, also in the upper Morphology: Flowers are medium-sized, bisexual, synascidiate zone of the ovary. Individual carpellary Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 polysymmetric, pentamerous (except for the trimer- stylar canals are absent; a central gap is present at ous gynoecium) and diplostemonous (Figs 25, 26). the transition from the plicate to the symplicate zone. Sepals are the protective organs in bud except for just PTTT is confined to the inner carpellary angle of the before anthesis, when the petals are much longer. ventral slit for the entire plicate and upper sympli- Sepals are thick, have a narrow base with a pointed cate zone. In the upper style it lines the slit as c. five tip and are quincuncial; their margins are thin (two or six cell layers diminishing to three or four in the cell layers) when protected by an overlapping sepal upper symplicate zone, and one or two cell layers in flank. They are congenitally united for a short dis- the lower symplicate zone, where a compitum appears tance (Fig. 25L, M). Petals are clawed, with a narrow to be present (Fig. 26A). An apical septum is absent. base and a pointed tip; aestivation is contort in the Placentation is lateral, axile and almost apical. Each blade, valvate at the base. Individual petals are locule is subdivided by a secondary septum, which hooked together in the clawed region both in bud and protrudes from the dorsal side (Fig. 26A, H–M); only at anthesis via opposingly directed submarginal edges at the top of the locule is the septum incomplete; (the tissue tears when petals are separated) locules are filled with secretion. Obturators are (Figs 25F–K, 72, 79). The covered flank forms the present (Figs 26G–I, 168, 169). Two pendant, anti- outer hook and the covering flank the inner. The tropous collateral ovules are present per carpel androecium has a whorl of long antesepalous stamens (Figs 168, 169). Ovules are anatropous, bitegmic and and a whorl of shorter, filamentous antepetalous incompletely tenuinucellar ovules are present per staminodes (Figs 25G–I, 96, 97). Together they are carpel (Fig. 173J). The raphe is constricted along its united into a basal androecial tube to which the length (Fig. 26J, K). The upwards-facing micropyle is petals are attached (Figs 25I–K, 96). Stamen fila- formed by the inner integument and is closely asso- ments are much shorter than anthers in advanced ciated with the obturator (Figs 26I, 169). The annular bud and much longer at anthesis. Above the andro- outer integument is two or three cell layers thick; the ecial tube the stamen filaments are laterally extended inner integument seven to nine cell layers; both and these extensions are connected over the ventral integuments are lobed. A pronounced endothelium is side (Figs 25H, I, 97). Anthers are tetrasporangiate, present (Fig. 173J). The gynoecium has a short gyno- x-shaped, elongate, latrorse, versatile and dorsifixed phore (Figs 25K, 26N). Petals join the androecial tube towards the base of the connective; thecae are bulged above the floral base; they have an extremely narrow out such that the dorsal side of the connective is attachment zone and bulge downwards below this hidden (pseudopit; for term see Endress & Stumpf, zone (Fig. 25M). Nectariferous tissue is present in 1991) (Fig. 113). The connective is narrow and thin antesepalous positions on the outer surface of the near the anther apex and thick towards the base; a androecial tube close to and below the level of petal protrusion is absent. Thecae dehisce by longitudinal attachment (Fig. 25J–L). Access to the nectar is cana- slits, which are not continuous over the connective; lized by the ventral surface of two adjacent petals endothecium-like tissue extends into the septa (revolver flower) (Fig. 25J–L). The floral base is between the pollen sacs but is not continuous over the convex; sepals join the floral base well below the other connective. The gynoecium is syncarpous in the ovary floral organs (Fig. 25L, M). The pedicel is articulated. and lower one quarter of the long, narrow styles; it is of angiospermy type 4 (Figs 25, 26). The superior Anatomy: Sepals have three main (and five to eight ovary is synascidiate up to above the placenta secondary) vascular bundles and three to five vascu- (Fig. 26H–M). Six longitudinal ridges on the upper lar traces (Fig. 25). Petals have c. 12–15 vascular ovary wall are present in median and commissural bundles and one vascular trace. Stamens have a positions (e.g. Fig. 26G). Locules are relatively widely single vascular bundle (lacking in staminodes). The separated because of an enlarged floral centre. The dorsal carpel bundle extends throughout the style to capitate stigmas are dorsiventrally flattened and are just below the stigma (Fig. 26). Individual lateral

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Figure 25. Reinwardtia indica (Linoideae; Linaceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. A–L, level of free sepals. B–J, level of free petals. C–H, level of free antesepalous stamens. C–D, level of plicate carpels. D–F, level of open ventral slits of carpels. E–F, level of symplicate zone of gynoecium. F–K, level of petals postgenitally hooked together above a free valvate base. G–J, level of synascidiate zone of gynoecium. G–I, level of filamentous antepetalous staminodes. H, level of lateral extensions of stamen filaments. I–K, level of androecial tube. J–L, level of petal attachment via narrow base to androecial tube; level of nectary (shaded). K, level of gynophore. L–Q, floral base and pedicel. L–M, level of fused sepals and convex floral base. M, below level of petal attachment. Scale bar, 1 mm.

Figure 26. Reinwardtia indica (Linoideae; Linaceae). Tri- C merous gynoecium at anthesis. Pollen tube transmitting B tissue (PTTT) shaded. A, schematic median longitudinal D section. Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn B with broken lines; postgenitally fused areas are hatched. B–N, transverse section series; morphological surface indi- E cated by thicker continuous lines, vasculature by thinner continuous lines. B–C, plicate zone (one carpel shown). B, F level of stigma. C–H, level of incompletely postgenitally

fused ventral slits. C–E, level of open ventral slits along Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 C carpel margins and incompletely postgenitally fused ventral slits at inner angle of ventral slits. D–G, sympli- G cate zone. F–G, level of compitum. G–I, level of obturators. H–M, synascidiate zone; level of secondary septa. H, level H of incomplete postgenital fusion of ventral slit in synascidiate zone. I–M, level of ovules. I, level of micropyle. K–M, level of complete division of locules by secondary septa. N, gynoecium base below locules. Scale bars, 500 mm. ᭣

carpel bundles are largely absent; instead synlateral I bundles extend into the base of the styles in the symplicate zone. In the ovary the dorsal and synlaterals are situated below the six longitudinal ridges (e.g. Fig. 26G). Additional inner lateral bundles extend into the upper synascidiate zone and supply the ovules. The ovule bundle ends in the chalaza J (Fig. 173J). Petal and stamen traces form a ring of ten separate bundles in the united petal and androecial tube, which extend into the convex floral base (Fig. 25K). There, synlateral and inner lateral carpel bundles join, followed by dorsal carpel bundles to D form a ring of bundles in the centre of the flower. Stamen traces join this ring, followed by petal traces; together these bundles form five large alternisepalous K bundle complexes. Sepal traces join this ring to form a stele in the pedicel.

Histology: Tanniferous tissue is present in small E amounts in all ﬂoral organs but mainly conﬁned to epidermis. Cells with oxalate druses are present in the sepals. Special mucilage cells are present in the L sepal epidermis and hypodermis and pedicel hypodermis and mesophyll (Fig. 197). Stomata are present on the dorsal side of the sepals and one stoma (nectary pore) is medianly positioned on each nectary (see F G above). Large intercellular spaces are present in the H anther connective and the large thecal septa. Hairs I are absent. J K M IRVINGIACEAE ML Irvingia smithii Hook.f. N A Morphology: Flowers are small, bisexual, polysym- N metric, pentamerous (except for the dimerous gynoecium) and diplostemonous (Figs 27, 28). Sepals have

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 FLOWERS IN RHIZOPHORACEAE AND RELATIVES 377 a broad base and a rounded tip. They are congeni- Anatomy: Sepals have three (to five) main (and two to tally united for a very short distance (Fig. 27L) and four secondary) vascular bundles and three (or four) are cochlear at their free base and open above. Petals vascular traces (Fig. 27). Petals have c. eight to 12 are longer than sepals and form the protective organs vascular bundles and three to five vascular traces. in advanced bud (Figs 27A–K, 36). They are simple Stamens have a single vascular bundle. The dorsal with a narrow base and a broad, rounded tip; carpel bundle extends up to below the stigma along aestivation is cochlear or quincuncial. Antesepalous with two to four lateral bundles, which split into stamens are longer than antepetalous ones. Anthers several bundles below the stigma (Fig. 28C). In the are tetrasporangiate, x-shaped, basifixed, introrse upper ovary synlaterals are present, which form a (antesepalous stamens) or almost latrorse (antepeta- large synventral bundle at the level of the extensive lous stamens, because of a broader connective on the attachment zone of the ovule (Fig. 28I, J); branches Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 ventral side); they are versatile (Fig. 114). The con- from this synventral placental bundle extend into the nective is broad on the dorsal side in both stamen flanks of the outer integuments for a short distance; types; a protrusion is absent. Thecae dehisce by lon- lower down, they also extend from the raphe into the gitudinal slits, which are not continuous over the outer integument (Fig. 173K). The main ovule bundle connective. Endothecium-like tissue is continuous ends in the chalaza. Close to the base of the locules over the ventral and dorsal sides of the connective. secondary lateral carpel bundles and the dorsal Stamen filaments are already longer than anthers in bundle join the central bundles to form a ring of bud where they are S-shaped. The gynoecium is syn- bundles in the centre of the flower. The numerous carpous; it is of angiospermy type 4 (Figs 27, 28). The vascular bundles supplying the large nectary disc also style is folded over the ovary in bud and to a lesser join this central ring, followed by the antepetalous degree at anthesis (Fig. 27C). The superior ovary is and the antesepalous stamen traces, the petal traces synascidiate up to above the placenta. The united and lastly the sepal traces. Together they form a stele carpels form a unicellular–papillate capitate stigma in the pedicel. (Fig. 134). Completely postgenitally fused ventral slits extend throughout the symplicate zone of the Histology: Tanniferous tissue is present in the style; at the base of the style the slits are incom- nectary. Large special mucilage cells are present in pletely postgenitally fused (Fig. 28E–G). The ventral the mesophyll of the sepals, petals, anther connective slits are lined by two to four cell layers of PTTT and ovary (Fig. 195). In the centre of the floral base throughout. A potential compitum is present and pedicel, a massive mucilage canal is present; throughout the symplicate zone (Fig. 28A–G). An smaller canals extend to below the ovary and are also apical septum is absent. Obturators are present present in the ovary and surround the central canal (Figs 28F–H, 170). Ovules have an attachment zone in the pedicel. Stomata are present on the dorsal that extends for much of the length of the locule surface of the sepals, petals, ovary, and sunken into (Figs 28A, 173K). Placentation is axile and median. A deep pits on the nectary disc (nectar pores). The single, antitropous ovule fills each locule (Fig. 170); it cytoplasm-rich nectary tissue is patchy in the nectary is bitegmic, anatropous and crassinucellar; it has a disc and is especially concentrated around the short raphe and is dorsiventrally flattened at its stomata. Sclereids surround the vasculature in the chalazal end (Figs 28A, 173K). The open median slit- pedicel. Hairs and cells with oxalate druses or crys- like micropyle is formed by both integuments and the tals are absent. outer integument partially surrounds the obturator. The semi-annular outer integument is three cell CARYOCARACEAE layers thick, the inner three or four cell layers. An endothelium is absent. The nucellus has cytoplasm- Caryocar brasiliense rich peripheral cell layers filled with starch grains; Morphology: Flowers are large, bisexual and polysym- especially at the nucellus apex, the epidermal cells metric (Fig. 29). The perianth is pentamerous. Sepals are radially elongate. A lobed, fleshy interstaminal are thick, have a broad base, a shallowly bilobed tip nectary disc surrounds the gynoecium; its surface is and ciliate margins (Fig. 45). They are congenitally papillate (Fig. 27G–L). The floral base is pro- united for some distance (Fig. 29H, I) and are quin- nouncedly convex (Fig. 27F–M). The antepetalous cuncial above; the two innermost sepals are slightly stamen filaments join the floral base below the longer than the two outermost ones. Petals are longer nectary disc above the antesepalous ones and nectary than sepals and are the protective organs in advanced lobes protrude between the filament bases (Fig. 27I– buds (Fig. 29A–E); they are quincuncial. Petals are L). Sepals are the last organs to join the floral base; thick, with a narrow base and a broad, rounded tip; they bulge downwards below their attachment although not elaborate, their margins are not entire, region. The pedicel is articulated. but rather irregularly dissected (Fig. 73); their

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Figure 27. Irvingia smithii (Irvingiaceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines; postgenitally fused areas indicated by broken lines. A–K, level of free petals. B–D, level of antesepalous anthers. C–D, level of symplicate zone of gynoecium. C, level of stigma and style. D, level of incompletely postgenitally fused ventral slits of carpels. E–G, level of synascidiate zone of gynoecium. E, level of antepetalous anthers. F–M, level of convex ﬂoral base. G–L, level of free sepals. G–L, level of lobed nectariferous disc (shaded). I–L, level of attachment of antepetalous stamens. J–L, level of attachment of antesepalous stamens. K–M, level of petal attachment. L–M, level of sepal attachment. N, pedicel and sepal bases below attachment zone. Scale bar, 500 mm. ᭣ Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021

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Figure 28. Irvingia smithii (Irvingiaceae). Dimerous gynoecium at anthesis. Pollen tube transmitting tissue (PTTT) shaded. A, schematic median longitudinal section; note extensive attachment zone of ovules. Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines; completely postgenitally fused areas are double-hatched; incompletely postgenitally fused areas are single-hatched. B–K, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines. B, level of stigma. B–G, symplicate zone; level of compitum. B–E, level of completely postgenitally fused ventral slits. E–G, level of incompletely postgenitally fused ventral slits. F–K, level of ovules. F–H, level of obturators and micropyles. H–K, synascidiate zone. Scale bars, 250 mm.

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Figure 29. Caryocar brasiliense (Caryocaraceae). Floral bud, bisexual, transverse section series; morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines. A–F, level of numerous fertile stamens. A–D, level of free petals. A–C, level of unifacial styles. B–H, level of free sepals. B–D, level of free filamentous staminodes. B, level of staminodes (surrounding styles) with a wart-like surface. C–H, level of androecial tube. C–E, level of symplicate zone of gynoecium. C–D, level of androecial tube with nectary on inner surface (shaded). C, level of dorsally bulged-up carpels surrounding styles. E–H, level of petal attachment to androecial tube. E, level of open ventral slits of carpels. F–H, level of synascidiate zone of gynoecium. G–I, level of fused sepals. H–L, floral base and pedicel. H–I, level of convex floral base. Scale bar, 2 mm. ᭣ ventral surface is uneven because of the impressions (Fig. 30Q). The stigmas are restricted to a small, Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 made by stamens in the tightly packed bud (e.g. sunken area in the centre of the punctiform apex of Fig. 29C, D). The second initiated petal is longer and the style (Fig. 137); they are unicellular–papillate; broader than the others. The androecium is polyste- secretion appears to be absent at anthesis. Stigmas monous, with c. 300 tightly packed stamens (57–750 and styles are unifacial (Fig. 30B–P). Only at the top for Caryocar, Dickison, 1990; 350–500 Gribel & Hay, of the ovary above the placenta are distinct, mostly 1993) and an inner series of c. 40 staminodes (Figs 29, open, ventral slits present (Fig. 30Q, R); they are 98, 99, 115–119). Stamens and staminodes (together lined by PTTT. In the symplicate zone, individual with the style) fill all available space in bud. The long carpellary stylar canals are absent, but a narrow stamen filaments (and style) are S-shaped to accom- central gap is present lined by papillae. PTTT is modate their length in bud; filaments are incurved present as a central strand in the style, narrowing only in the distal part and are much longer than towards the base of the style from 24 cell layers in the anthers already in bud; they are of unequal length. uppermost part of the style below the stigma to 13 cell Anthers are tetrasporangiate, x-shaped, introrse and layers in the mid to lower style and just above the versatile (Figs 115, 116). The connective is broad on symplicate zone. In the lower symplicate zone, two the dorsal side; a protrusion is mostly absent. Thecae cell layers line the open ventral slits. In the sympli- dehisce by longitudinal slits, which are not continu- cate zone of the ovary above the locules, cytoplasm- ous over the connective. Endothecium-like tissue does rich papillae fill the central gap; a compitum appears not extend into the connective. Anthers of outer to be present in this zone (Fig. 30A, Q, R). In the stamens are larger than those of inner ones and have synascidiate zone above the placenta, the ventral a thicker and broader filament (Fig. 115). The outer surface of the locule is lined by four or five cell layers anthers are dorsifixed towards the base of the con- of papillate PTTT. The tissue surrounding the locule nective, while the inner ones are basifixed in a is distinctly small-celled. Placentation is median and pseudopit (Fig. 116). Staminodes are much shorter axile. Obturators are absent; however, the ventral than fertile stamens; they are filamentous with a margins of the carpels are papillate in the region of rudimentary anther and a thickened nectariferous the micropyle. The attachment zone of the single base (Figs 98, 99, 117–119). They are united with antitropous ovule is narrow, but very extensive in the adjacent stamens into an androecial tube surrounding median direction and occupies almost the entire the gynoecium (Figs 27C–H, 98, 99). A wart-like length of the locule (Fig. 30A, A′, 173L). The single surface structure is present on the filaments of both ovule per carpel has a short raphe and is hemianat- stamens and staminodes; it is restricted to the upper- ropous, bitegmic and weakly crassinucellar (Figs 171, most portion of the filament in stamens (Figs 29B, 172, 173L). The nucellus is extremely elongate below 115–119). Closer to the floral base, adjacent stamen the embryo sac, which is positioned towards the filaments unite and join with the androecial tube raphal side within the nucellus. Already in bud, the (Fig. 29C–F). Fusion takes place from the inside of apical lobes of the integuments partially disintegrate the flower towards the outside (convex floral base). (Figs 172, 173L). The open micropyle is formed by The three (or four) carpels are united in the ovary and both integuments. The annular outer integument is have long free styles; the gynoecium is of three to five cell layers thick, the inner integument angiospermy type 4 (Figs 29, 30, 125). The almost five to seven cell layers. An endothelium is absent. superior globular ovary is synascidiate up to above The entire nucellus, especially the peripheral layers, the placenta; its dorsal side is shortly and abruptly is cytoplasm-rich and filled with starch grains: at the bulged upwards above the level of insertion of the nucellus apex the epidermal cells are radially style so that the style appears sunk into it (Figs 29C, elongate. The floral base is convex and the petals 30A, N, O, 125, 129). It has thick walls and the join the dorsal side of the androecial tube some dis- locules are widely separated because of a massive tance above the sepals (Fig. 29E–H). The pedicel is floral centre. A short apical septum is present articulated.

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J V K L W M N O P Q RS T U V W X A A’ X

Figure 30. Caryocar brasiliense (Caryocaraceae). Tetramerous gynoecium at anthesis. Pollen tube transmitting tissue (PTTT) shaded. A, A′, schematic median longitudinal section; note extensive attachment zone of ovules. Morphological surface drawn with a continuous line; outline of parts just out of the median plane drawn with broken lines. A, entire gynoecium. A′, close-up of ovary. B–X, transverse section series (B–K, only one carpel shown); morphological surface indicated by thicker continuous lines, vasculature by thinner continuous lines. B–P, unifacial zone of carpels. B, level of stigma. N–R, symplicate zone. N–P, zone of dorsally bulged ovary. Q–W, level of ovules. Q–S, level of micropyles with apices of inner and outer integuments disintegrating. Q–R, level of open ventral slits and compitum. S–W, synascidiate zone. X, Gynoecium base below locules. Scale bars, 1 mm. ᭣

Anatomy: Sepals have c. five main (and five to ten Stomata are present on the dorsal side of the sepals, Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 secondary) vascular bundles and three vascular traces petals, anthers and style. Nectar pores were not (median and two synlateral) (Fig. 29). Petals have found. The wart-like structures on the stamens and eight to ten main (and 20–25 secondary) vascular staminodes are cytoplasm-rich, unicellular or multi- bundles and c. three vascular traces. Stamens and cellular (Figs 117–119). On the dorsal side of the staminodes have a single vascular bundle. Two small sepals near the apex, a gland is present in median lateral carpel bundles extend into the upper style, position (Figs 45, 46). Whether it is an extranuptial below the stigma (Fig. 30D). These bundles are joined nectary or an oil gland is unknown. Its conspicuous by other smaller bundles slightly lower down forming epithelium with a thick cuticle is reminiscent of an a network. Additional bundles extend into the upper oil gland as described by Vogel (1974) for other mid-style region either joining the two main lateral angiosperms. In the gland, the cuticle is separated bundles or remaining separate and forming a ring from the epidermis and the epidermis is differenti- around the PTTT (e.g. Fig. 30I). At the base of the ated into cytoplasm-rich, narrow, radially elongate style, most bundles have joined the main lateral cells with secondary transverse divisions. The hypo- bundles, which extend downwards into the ovary, one dermal cells are also cytoplasm-rich. Unicellular, lig- positioned on each side of the ventral slit. The ovary nified hairs are present on both surfaces of the sepals. wall is heavily vascularized. Some bundles join the lateral carpel bundles, while others mostly remain in the outer wall of the ovary. Whereas the lateral DISCUSSION bundles are in the centre of the gynoecium, numerous smaller bundles appear at the periphery of the ovary FLORAL STRUCTURE OF RHIZOPHORACEAE S.L. AND wall, but a distinct dorsal bundle is not apparent. A POTENTIALLY RELATED FAMILIES ventral bundle extends halfway up the attachment Flower size, shape, merism, symmetry, sex zone of the ovule and serves the ovule, with short distribution and floral biology branches extending into the flanks of the outer integu- Flowers are small (Յ 5 mm; especially Gynotrocheae, ment (Figs 30U–W, 173L). It also has a branch from Erythroxylaceae, Irvingiaceae, Linaceae p.p.) to the raphe to the chalaza, which also branches into the medium-sized (6–15 mm; especially Rhizophoreae, outer integument from both areas (Figs 30W, 173L). Nectaropetalum of Erythroxylaceae, Ctenolopho- Petal and stamen/staminode bundles do not form naceae, Linaceae) or large (4 cm; Caryocaraceae). complexes in the corolla/androecial tube, but petal They are mostly widely open (plate-like), most pro- bundles of each petal unite and within the androecial nouncedly so in Irvingiaceae, except for some Rhizo- tissue, adjacent staminode and stamen bundles join to phoraceae (Rhizophoreae) with explosive pollen form a ring of complex bundles. Adjacent sepal release, Pellacalyx with tubular flowers and some bundles unite, and in the fused sepals, lateral bundles Linaceae with salverform flowers (Anisadenia Wall., of adjacent sepals form synlaterals. In the floral base, Tirpitzia Hallier f., the latter with a long tube) or stamen/staminode bundles join the closest petal traces funnel-shaped flowers (Linum). In some Linaceae to form large bundle complexes. The ventral and revolver flowers are present, the separate nectar lateral carpel bundles join the central bundles. Lower canals formed by longitudinal ribs on petals (this down the stamen/petal complexes join to form even study) (Figs 23, 25). A floral cup is present in Rhizo- larger antepetalous complex bundles, which are then phoreae (Figs 11, 15), Gynotrocheae (long in Pellaca- joined by sepal traces; together they join the central lyx, Ding Hou, 1958) (Figs 7, 8, 10, 147), Cassipourea bundles to form the stele. congensis of Macarisieae (Rhizophoraceae) (Fig. 4) and Nectaropetalum (Erythroxylaceae) (this study). Histology: Tanniferous tissue is present, but is not The pedicel is articulated in all six families (also abundant in the sepals, petals and staminodes. Cells mentioned for Linaceae and Caryocaraceae by with oxalate crystals are present in the ovary. Hallier, 1921).

whorls is rather rare (Anopyxis, Fig. 2; Carallia, Fig. 7; Pellacalyx of Rhizophoraceae; Linum, Fig. 23, and Hugonia of Linaceae). Tetramery throughout the flower is present in Radiola (Linaceae, Winkler, 1931). The perianth is only tetramerous in Rhizophora (Fig. 15), Gynotroches (Figs 8, 10), and Cassipourea (Fig. 4) (Rhizophoraceae) (this study) but up to 16-merous in Bruguiera gymnorrhiza, up to octomerous in Carallia (Fig. 7), and up to hexamerous in Pellacalyx (Ding Hou, 1958) and Crossostylis (Setogu- chi, Ohba & Tobe, 1996, 1998); in all these cases Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 (except Crossostylis) the two whorls of the androecium are isomerous with the perianth whorls. Increase in stamen number is strong in Caryocaraceae (this study, Fig. 29; Pilger, 1925; Dickison, 1990) and moderate in Rhizophoraceae, where it evolved independently in three unrelated genera [Cassipourea (Macarisieae), Crossostylis (Gynotrocheae) and Kandelia (Rhizopho- reae); Juncosa 1988)] (see below). Increase in carpel number is present in species of all genera of Rhizophoraceae–Gynotrocheae (Juncosa, 1988) and in Caryocaraceae (Pilger, 1925) (see below). Thus, in both Pellacalyx (diplostemonous) and Crossostylis (polystemonous), the carpels are roughly isomerous with the stamens and alternate with them (Juncosa, 1988: 94). The flowers are polysymmetric, except for the monosymmetric gynoecium in Erythroxylum (Eryth- roxylaceae; this study, Fig. 18; Phillips, 1935; Rao, 1965) (Fig. 18) and in Roucheria Planch. (Linaceae; this study, Fig. 22; Winkler, 1931) (Fig. 22), in both of which two of the three ovary locules are smaller and either sterile or only partly fertile. The flowers are commonly bisexual, with a few deviations. Incipient unisexuality was reported in Crossostylis (Smith, 1981; Juncosa, 1988; recorded for six species by Setoguchi et al., 1998). Functional dioecy occurs in Gynotroches (this study, Figs 8–10); Ding Hou, 1958; Juncosa, 1988) (Figs 8–10) and Steri- gmapetalum Kuhlm. (Juncosa, 1988). Heterostyly is a prominent feature of Erythroxylaceae (Del Carlo & Buzato, 2006) and Linaceae (Planchon, 1848; Darwin, Figures 31–36. Sepals or petals forming the protective organs in bud; entire buds, antesepalous view (arrowhead: 1877; Armbruster et al., 2006; McDill et al., 2009; in sepal). Figures 31–32. Sepals protective (Rhizophoraceae) some Hugonia spp. even tristyly, Lloyd, Webb & Dul- (in Fig. 31, the organs at the base are the remains of berger, 1990; Thompson et al., 1996), also with occa- bracts). Figures 33–36. Petals protective. Fig. 31. Carallia sional evolution of unisexuality, such as in the suffruticosa (Gynotrocheae). Fig. 32. Gynotroches axillaris androdioecious Erythroxylum havanense Jacq. (Rosas (Gynotrocheae); functionally male flower. Fig. 33. Eryth- & Domínguez, 2008). Paradrypetes Kuhlm., if related roxylum cuneifolium (Erythroxylaceae). Fig. 34. Ctenolo- at all with our group (see Floral Structure and Sys- phon englerianus (Ctenolophonaceae). Fig. 35. Linum tematics), would be the only genus with pronouncedly kingii (Linoideae; Linaceae). Fig. 36. Irvingia smithii (Irv- unisexual flowers. ingiaceae). Scale bars, 500 mm. Floral biology: in Rhizophoraceae, two of the four mangrove genera have an explosive floral mechanism Merism of floral organs is unusually diverse, espe- (Bruguiera; Gehrmann, 1911; Tomlinson, 1986; cially in Rhizophoraceae and the highly polystemonous Juncosa & Tomlinson, 1987; Yeo, 1993; and Ceriops; Caryocaraceae. Pentamery is represented in all six Juncosa & Tomlinson, 1987; Yeo, 1993). The struc- families to some extent; however, isomery of all floral tural basis of this explosive mechanism is described

Figures 37–46. Figures 37–44. Sepals valvate and postgenitally connected in bud. Figs 37, 39, 41. Entire buds from above. Figs 38, 40, 42, 44. Transverse sections showing postgenital connection between sepals (arrowheads). Figs 38, 42, 44. Postgenital connection via interdigitation of epidermal cells. Fig. 40. Postgenital connection via cuticular dentation. Figs 37 and 38. Cassi- pourea elliptica (Rhizophoraceae–Marcarisieae). Figs 39 and 40. Gynotroches axillaris (Rhizophoraceae– Gynotrocheae); functionally male ﬂower. Figs 41 and 42.

Bruguiera cylindrica (Rhizophoraceae–Rhizophoreae). Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 Figs 43 and 44. Erythroxylum cuneifolium (Erythroxy- laceae). Fig. 43. Transverse section of entire bud showing revolute–valvate sepals. Figs 45 and 46. Caryocar brasiliense (Caryocaraceae), sepal from bud. Fig. 45. Gland on dorsal surface (arrow). Fig. 46. Transverse section of gland; the cuticle has separated from the gland epithelium (asterisk). Scale bars, 500 mm (Figs 37, 39, 41, 43, 45); 150 mm (Figs 38, 40, 42, 44, 46). ᭣

is by moths (Tomlinson, Primack & Bunt, 1979), in Ceriops decandra by bees and wasps (Raju, Jonathan & Lakshmi, 2006), and in Kandelia by wasps and by Apis and Xylocopa (Tanaka, 1989; Sun, Wong & Lee, 1998). Rhizophora appears to be wind-pollinated (Tomlinson, 1986; Juncosa & Tomlinson, 1987; Kondo et al., 1987; Calleja, Rossignol-Strick & Duzer, 1993). Erythroxylum is mainly pollinated by bees, wasps and ﬂies (Barros, 1998). In Linaeae, Linum is pollinated by bees and ﬂies (Heitz, 1980; Kearns & Inouye, 1994) and Hugonia mystax L. by bees (Aluri et al., 1997), whereas in Caryocaraceae, Caryocar is bat-pollinated (Vogel, 1968; Gribel & Hay, 1993), with sphingids also acting as pollinators (Gribel & Hay, 1993) and Antho- discus G.Mey. is probably insect-pollinated (Prance & da Silva, 1973).

Calyx Sepals are longer than petals and form the protective organs in the advanced floral bud only in Rhizopho- raceae (this study) (Figs 31–36). Sepal aestivation is valvate in Rhizophoraceae and Erythroxylaceae (this study) (Figs 37–44), but quincuncial in Ctenolopho- naceae (this study, Fig. 20; Link, 1992b), Linaceae (this study, Figs 23, 25; Breindl, 1934) and Caryocar- aceae (this study, Fig. 29; Dickison, 1990), and cochlear in Irvingia (this study, Fig. 27). The sepals in Juncosa & Tomlinson (1987), and some aspects also are basally united in taxa of all six families (with only in Gehrmann (1911), Davey (1975), and Yeo (1993). a few exceptions), occurring in most studied species of The large-flowered (explosive) Bruguiera spp. are pol- all three tribes of Rhizophoraceae (this study), in linated by birds (first observed by Werth, 1900; Kondo Erythroxylaceae (this study), Ctenolophonaceae (this et al., 1987, 1991; Tanaka, 1989; Noske, 1993) and study; Narayana & Rao, 1971, 1978e), Linaceae (this perhaps partly by wind (Docters van Leeuwen, 1927), study; Anisadenia, Narayana & Rao, 1969; Cathar- and the small-flowered (non-explosive) species by but- tolinum Rchb., Narayana & Rao, 1976b; Hesperolinon terflies and other insects. In Ceriops tagal pollination (A.Gray) Small, Narayana & Rao, 1977a; Hugonia,

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Figures 47–61. Rhizophoraceae and Erythroxylaceae. Conduplicate petals enwrapping stamen(s) in bud. Figures 47, 49, 53, 55. Buds from above; sepals removed (except Fig. 55) (arrow; single petal). Figures 48, 50–52, 54, 56. Single petal enwrapping a stamen (arrowhead) (in Fig. 51: two petals; Fig. 56: part of a second petal also present on right); from adaxial. Figures 57–61. Transverse sections of single petals enwrapping stamen(s) (in Fig. 61: entire flower). Figs 47–54, 57–60. Rhizophoraceae. Figs 55 and 56. Erythroxylum cuneifolium (Erythroxylaceae). Figs 47 and 48. Rhizophora mucronata (Rhizophoreae). Figs 49 and 50. Ceriops decandra (Rhizophoreae). Figs 51 and 57. Ceriops tagal (Rhizopho- reae). Figs 52 and 60. Carallia suffruticosa (Gynotrocheae). Figs 53 and 54. Gynotroches axillaris (Gynotrocheae); functionally male flower. Fig. 58. Bruguiera cylindrica (Rhizophoreae); petal enwrapping two stamens, one antepetalous, one antesepalous (antepetalous stamen close to midrib of petal). Fig. 59. Gynotroches axillaris (Gynotrocheae); functionally female flower. Fig. 61. Erythroxylum cuneifolium (Erythroxylaceae), petals enwrapping an antepetalous stamen, ventral scales from adjacent petals enwrapping an antesepalous stamen. Scale bars, 500 mm (Figs 47, 56); 1 mm (Figs 48, 51, 52, 61); 250 mm (Figs 49, 50, 53–55); 200 mm (Figs 57–60).

Narayana & Rao, 1977c; Linum, Narayana & Rao, general, sepals are thick in representatives of all six 1976a; Radiola, Narayana & Rao, 1978b), and in families (this study). The sepals join the floral base Caryocaraceae (this study; Dickison, 1990). In addi- well below the other floral organs (thus the floral base tion, the free parts of the sepals are postgenitally is convex) in Erythroxylaceae (not in Nectaropetalum) connected, a feature strictly concomitant with valvate (Fig. 17), Ctenolophonaceae (Fig. 20), Linaceae aestivation in all studied Rhizophoraceae and Eryth- (Figs 23, 25), Irvingiaceae (Fig. 27) and Caryocar- roxylaceae (this study) (Figs 31–32, 37–44). This is aceae (Fig. 29) (this study), and their margins are also correlated with pointed (and not rounded) sepal decurrent on the floral base or floral cup in some tips (only those of Linaceae also have pointed tips). In Rhizophoraceae (especially Rhizophoreae), some

Erythroxylaceae, in Ctenolophonaceae, Caryocar- study); Linaceae (in Linum and Reinwardtia,atthe aceae and Reinwardtia (Linaceae) (this study). Sepals base, but contort above, this study). Petals are thick are caducous in Irvingiaceae but persistent in Eryth- in some Rhizophoraceae, Erythroxylum, Linaceae and roxylaceae (Hallier, 1921) and Linaceae (Addicott, Caryocaraceae. In contrast to thick sepals, the pres- 1977; Tomar, Desmukh & Sinha, 1979; Uno, 1984). As ence of thick petals is only partly correlated with is common in eudicots, sepals of all six families often valvate aestivation. have three vascular traces (this study; Rao, 1965; Petals are postgenitally united in an unusual Narayana & Rao, 1978d; Juncosa, 1986); and there fashion: they are free at the base but united for a are synlaterals (this study; for Rhizophoraceae, see shorter or longer distance above the base in some Saunders, 1939). However, there is a tendency to have Rhizophoraceae (Bruguiera, Ceriops; this study; Ding up to five traces in Rhizophoraceae, Linaceae and Hou, 1958; Juncosa & Tomlinson, 1987; Endress & Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 Irvingiaceae, and Nectaropetalum (Erythroxylaceae) Matthews, 2006a), in Ctenolophonaceae, and Linaceae has ten. In contrast, Ctenolophonaceae have one to (this study, Figs 70–72, 74–79). This postgenital union three traces (this study). takes place in different ways, such as by hooks of the petal margins, by hairs, via cuticles or in a combina- Corolla tion of these features. Petals are hooked together (in Petals are very narrow in young stages, with large valvate fashion, but with originally contort aestiva- interspaces between them in some Rhizophoraceae tion) in Linaceae in Anisadenia (Narayana & Rao, (Crossostylis, Cassipourea, Carallia, Pellacalyx; 1969), Reinwardtia (this study, Figs 2, 72, 79; Juncosa, 1988), and remain narrow also at anthesis in Narayana, 1964a) and Linum (this study, Figs 23, 71, Rhizophoraceae (especially Macarisieae and Gynotro- 78). In Erythroxylum, petal connection is by marginal cheae) and in Roucheria of Linaceae (this study). They interdigitation of dorsal and ventral parts (this study, also have a conspicuously narrow attachment zone in Figs 17, 77). They are somewhat hooked together Rhizophoraceae, Erythroxylaceae and Linaceae (this in Caryocaraceae (Dickison, 1990). In Tirpitzia study, e.g. Fig. 83). However, petals become longer (Linaceae) the petal claws are postgenitally united than sepals in floral bud and form the main protective forming a long tube (Suksathan & Larsen, 2006). In organs in Erythroxylaceae, Ctenolophonaceae, some mangrove Rhizophoraceae, petals are not only Linaceae, Irvingia and Caryocar (this study, Figs 33– postgenitally united with their neighbours but also 36). Petals are conduplicate and enwrap stamens or postgenitally connected among themselves, the release parts of stamens in bud in Rhizophoreae (only basally of the latter bond being responsible for the explosive in Rhizophora; see also Orchard, 1975) and Gynotro- behaviour of the flowers (Juncosa & Tomlinson, 1987; cheae (only slightly conduplicate in Macarisieae) and Endress & Matthews, 2006a). in Erythroxylaceae (this study, Figs 47–61). For the Petals have lateral elaborations in all three tribes explosive flowers of Bruguiera and Ceriops (Rhizopho- of Rhizophoraceae (this study), some Linaceae and, to raceae) the conduplicate stamen-enwrapping struc- a small degree, in Caryocaraceae (this study, Figs 62– ture is the basis for the mechanism (this study, 73; for Linaceae, see also Sharsmith, 1961; O’Donnell, Figs 49–51, 57, 58; Juncosa & Tomlinson, 1987). 2006). In Rhizophora, lateral petal elaborations are Petal aestivation is contort in a few Rhizophoraceae only rudimentary (this study; Endress & Matthews, (Ceriops, Gynotroches; this study), in Ctenolopho- 2006a). In some mangrove Rhizophoraceae, finger- naceae (this study; Narayana & Rao, 1971; van like lateral petal elaborations function in water Hooren & Nooteboom, 1984) and in Linaceae (this economy (Juncosa & Tomlinson, 1987). Petals with study; Narayana, 1964a; Narayana & Rao, 1973, ventral elaborations are present in Erythroxylaceae 1976a, 1977a, 1978a). In Linaceae both directions of (Erythroxylum, Figs 17, 80; Nectaropetalum); this contortion occur within an inflorescence in a special study; Schulz 1931; Baum 1950; Leinfellner 1954; pattern (Eichler, 1878; Tammes, 1918; Schoute, 1935; Endress & Matthews 2006a) and Linaceae (Linum, Endress, 1999). This was not studied, but may also be Hugonia; this study, Figs 23, 81–83; Hebepetalum expected in Ctenolophonaceae and Rhizophoraceae Benth. and Hesperolinon; Winkler, 1931; Sharsmith, (see Endress, 1999, 2001). In contrast, petal aestiva- 1961; Narayana & Rao, 1977a). In Hugonia, the tion is cochlear in Nectaropetalum (Erythroxylaceae) petals are simply peltate (this study, Fig. 81; Winkler, (Rao, 1965), quincuncial in Erythroxylum (this study, 1931). In Erythroxylum, these ventral elaborations Fig. 17; Rao, 1965) and Caryocaraceae (this study, are relatively large and form a corolline corona, with Fig. 29), and cochlear and quincuncial in Irvingia their main function to protect the nectar in the floral (this study, Fig. 27). Valvate aestivation is present in centre (Link, 1989; Endress & Matthews, 2006a) a number of Rhizophoraceae (not in the Macarisieae (Fig. 80). In Hesperolinon (Linaceae) both lateral and studied here), Erythroxylaceae (in Erythroxylum,at ventral elaborations are described as glands the base, but quincuncial above, see above, this (Narayana & Rao, 1977a).

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Both sympetaly and fusion of free stamens with 1984), Linaceae (Addicott, 1977; van Hooren & petals (stapet) are absent in all species studied. Nooteboom, 1984) and Caryocaraceae (this study; However, presence of an androecial tube and fusion Vogel, 1968; Prance & da Silva, 1973; Dickison, between this tube and the petals occurs in part of 1990); in Anthodiscus (Caryocaraceae) all ﬁve petals Rhizophoraceae (e.g. Fig. 6) and Erythroxylaceae fall as a unit, whereas in Caryocar petals and (Fig. 17) and in Ctenolophonaceae (Fig. 20), Linaceae stamens fall as a unit (Vogel, 1968; Prance & da (Figs 23, 25, 95, 96) and Caryocaraceae (this study, Silva, 1973). Fig. 29). Petals have three vascular traces in Caryocaraceae Petals are caducous in Rhizophoraceae (Gynotro- (Fig. 29) and Irvingia (Irvingiaceae) (Fig. 27), but one ches, Rhizophora, this study; Gill & Tomlinson, trace in the other families (this study; for Linaceae, 1969), Ctenolophonaceae (van Hooren & Nooteboom, see also Narayana & Rao, 1978d).

Figures 62–79. Petals with marginal elaborations and postgenitally connected; buds (in Fig. 68: anthetic ﬂower). Figures 62–73. Scanning electron microscopy (SEM) micrographs; petals with marginal elaborations. Figures 74–79. Transverse microtome sections showing postgenital connection between two petals (in Figs 74–76, histological connection; in Figs 77–79, morphological connection). Fig 62–64, 66–69 and 73. Single petals; ventral (in Fig. 66: dorsal). Figs 74 and 76. Postgenital connection via hairs (arrows). Figs 71, 72 and 77–79. Petals hooked together. Fig. 62. Cassipourea congensis (Rhizophoraceae–Marcarisieae). Fig. 63. Anopyxis klaineana (Rhizophoraceae–Marcarisieae). Fig. 64. Gynotro- ches axillaris (Rhizophoraceae–Gynotrocheae); functionally male ﬂower. Fig. 65. Pellacalyx cristatus (Rhizophoraceae– Gynotrocheae); petals with long marginal appendages extending downwards into the androecial tube; sepals and three petals removed. Figs 66 and 67. Carallia suffruticosa (Rhizophoraceae–Gynotrocheae). Fig. 67. Flanks of one petal overlapping on ventral side. Fig. 68. Rhizophora mucronata (Rhizophoraceae–Rhizophoreae); petal apex with short lateral lobes. Fig. 69. Ceriops decandra (Rhizophoraceae–Rhizophoreae). Figs 70 and 74. Ceriops tagal (Rhizophoraceae– Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 Rhizophoreae); petals postgenitally connected at their mid length via coiled hairs. Fig. 75. Bruguiera cylindrica (Rhizophoraceae–Rhizophoreae); postgenital connection via cuticle. Fig. 76. Ctenolophon englerianus (Ctenolophonaceae); postgenital connection via stellate hairs. Fig. 77. Erythroxylum cuneifolium (Erythroxylaceae); dorsal (one) and ventral (two) margins of the left-hand petal (black arrowheads), interdigitating (hooking) with the dorsal and ventral margins of the right-hand petal (white arrowheads). Figs 71 and 78. Linum kingii (Linaceae–Linoideae). Figs 72 and 79. Reinwardtia indica (Linaceae–Linoideae). Fig. 73. Caryocar brasiliense (Caryocaraceae). Scale bars, 500 mm (Figs 62, 63, 66, 67, 70, 71); 250 mm (Figs 64, 65, 68, 69, 72); 100 mm (Fig. 73); 50 mm (Figs 74–79). ᭣

Androecium Diplostemonous or obdiplostemonous flowers are present in at least part of all families (except Caryo- caraceae), i.e. most Rhizophoraceae, Erythroxylaceae, most Linaceae, Ctenolophonaceae and Irvingiaceae (this study; for Rhizophoraceae, see also Juncosa, 1988; for Erythroxylaceae, see also Schulz, 1931; for Ctenolophonaceae, see also Winkler, 1931; for Linaceae, see also Stroebl, 1925; Winkler, 1931; for Irvingiaceae, see also Engler, 1931; Eckert, 1966). Haplostemonous flowers occur only in some Linaceae by reduction (Linum kingii, this study, Fig. 23; Linum austriacum L., Reinwardtia, Radiola, Winkler, 1931); in other Linaceae, the antepetalous organs are present as staminodes (e.g. Reinwardtia) (this study, Figs 25, 96, 97). Staminodes are also present in the inner part of the polymerous androecium of Caryocar (this study, Figs 29, 98, 99, 117–119; Prance & da Silva, 1973; Dickison, 1990). Distinction between diplostemony and obdiplostemony (see Glossary) is often problematic, because (1) the situation may change during development and (2) often antesepalous and antepetalous stamens do not have the same thickness, so that it is not always possible to determine which stamens are farther outside or farther inside (Eckert, 1966; Endress, Figures 80–83. Petals with ventral elaborations (arrow- 2010b). A more obvious criterion is whether the carpels heads); anthesis (in Fig. 80: bud). Figure 80. Erythroxylum are antesepalous (diplostemonous) or antepetalous cuneifolium (Erythroxylaceae); petal with lobed ventral (obdiplostemonous) (Matthews et al., 2001; Bachelier scale. Figures 81–83, Linaceae. Fig. 81. Hugonia acumi- & Endress, 2009; Endress, 2010b). However, this cri- nata (Hugonioideae), petal base with peltate elaboration. terion works only for completely isomerous flowers. Figures 82 and 83. Linum kingii (Linoideae). Fig. 82. That there is no fundamental difference between Entire petal. Fig. 83. Petal base with elaboration and very diplostemony and obdiplostemony is also shown by the small attachment zone (arrow). Scale bars, 250 mm (Figs 80–82); 100 mm (Fig. 83). fact that both forms may occur in the same family, such as Linaceae (see below). In our study group, diploste-

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Figures 84–99. Stamens from buds united into a nectariferous androecial tube, perianth removed (arrowheads, lobes of androecial tube; arrows, filament bases) (in Figs 87, 88, 91, 93, 94, 99, anthetic flowers). Figures 84–89. Rhizophoraceae. Figs 84 and 85. Anopyxis klaineana (Marcarisieae); perianth removed. Fig. 85. Close-up view of rim of androecial tube. Figs 86 and 87. Pellacalyx cristatus (Gynotrocheae). Fig. 87. Partial androecial tube with longer antepetalous stamen and shorter antesepalous one on the inner wall of the tube; ventral (anther, a). Fig. 88. Gynotroches axillaris (Gynotrocheae); functionally male flower; stamen filament with lobes from androecial tube flanking it. Fig. 89. Ceriops tagal (Rhizopho- reae), corona-like lobed androecial tube (stamens removed). Figures 90 and 91. Erythroxylaceae. Fig. 90. Erythroxylum cuneifolium; lobed corona-like androecial tube, antesepalous view. Fig. 91. Aneulophus africanus; base of androecium with short tube. Figures 92–94. Ctenolophon englerianus (Ctenolophonaceae); lobed corona-like androecial tube on dorsal side of stamens. Figures 93 and 94. Androecial tube (upper part of gynoecium removed). Fig. 93. From above, showing filament bases on the inside of the androecial tube. Fig. 94. From side. Figures 95–97. Linaceae; small attachment zone of petals (asterisk) visible on androecial tube. Fig. 95. Linum kingii. Figs 96 and 97. Reinwardtia indica; stamens and filamentous staminodes. Fig. 97. Antesepalous stamen and two staminodes; ventral. Figures 98 and 99. Caryocar brasiliense (Caryo- caraceae); staminodial androecial tube. Fig. 98. Dorsal; stamens removed. Fig. 99. Ventral. Scale bars, 500 mm (Figs 84, 98); 250 mm (Figs 85–87, 89, 90, 92, 96, 99); 100 mm (Figs 88, 91, 93–95, 97).

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Figures 100–119. Anthers of bud, from dorsal (in Figs 109, 117, 118, anthetic flowers). Figures 100–106. Rhizophoraceae. Fig. 100. Cassipourea congensis (Macarisieae). Figs 101 and 102. Anopyxis klaineana (Macarisieae). Fig. 102. Anthers and upper part of androecial tube. Fig. 103. Carallia suffruticosa (Gynotrocheae). Fig. 104. Pellacalyx cristatus (Gynotrocheae). Fig. 105. Rhizophora mucronata (Rhizophoreae). Fig. 106. Ceriops decandra (Rhizophoreae). Figures 107 and 108. Erythroxylaceae. Fig. 107. Erythroxylum cuneifolium. Fig. 108. Aneulophus africanus. Figure 109. Ctenolophon englerianus (Ctenolophonaceae). Figures 110–113. Linaceae. Figs 110 and 111. Hugonia acuminata (Hugonioideae). Fig. 111. Anther apex with connective protrusion of hairs. Fig. 112. Linum kingii (Linoideae). Fig. 113. Reinwardtia indica (Linoideae). Figure 114. Irvingia smithii (Irvingiaceae). Figures 115–119. Caryocar brasiliense (Caryocaraceae); stamens and staminodes with wart-like ornamentations on filaments (arrows). Fig. 115. Outer stamen. Fig. 116. Inner stamen. Figs 117 and 118. Staminodes, malformed anther indicated by arrowheads. Fig. 119. Transverse section of staminode filament. Scale bars, 200 mm (Figs 100–102, 106, 110–113, 115–118); 100 mm (Figs 103, 104, 107–109, 114, 119); 500 mm (Fig. 105).

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Figures 120–129. Anthetic gynoecia with dorsally bulged ovaries and styles (arrows) ‘sunk’ into them. Figures 120–125. Scaning electron microscopy (SEM) micrographs. Figures 126–129. Transverse microtome sections at level of insertion of style and dorsally bulged ovary. Figs 120–122. Styles syncarpous. Figs 123–125. Styles apocarpous. Figs 126 and 128. Carpels individually bulged. Figs 127 and 129. Carpels not individually bulged. Figs 120–122, 126, 127. Rhizophoraceae. Figs 120 and 126. Anopyxis klaineana (Macarisieae). Fig. 121. Cassipourea congensis (Macarisieae). Figs 122 and 127. Gynotroches axillaris (Gynotrocheae), functionally female ﬂower. Figs 123 and 128. Erythroxylum cuneifolium (Eryth- roxylaceae). Fig. 124. Hugonia acuminata (Linaceae). Figs 125 and 129. Caryocar brasiliense (Caryocaraceae). Scale bars, 500 mm (Figs 120, 122, 124, 127, 129); 250 mm (Figs 121, 125, 126, 128); 50 mm (Fig. 123).

mony (with carpels antesepalous) occurs among lous stamens is present in some Linaceae (Linoideae) Linaceae in Hebepetalum (Narayana & Rao, 1966) and (this study, Fig. 23; Winkler, 1931). Hugonia (Narayana, 1964a; Narayana & Rao, 1977c), Polystemonous androecia (i.e. with more than both in Hugonioideae (McDill & Simpson, 2011) and double the number of stamens than sepals) are among Irvingiaceae in Klainedoxa Pierre ex Engl. present in some Rhizophoraceae (this study, Figs 4, 6; (Eckert, 1966). In contrast, in Linaceae, obdiploste- Juncosa, 1988; Setoguchi et al., 1996, 1998; Breteler, mony (with carpels antepetalous) is present in Duran- 2008; see also below) and Caryocaraceae (this study, dea Planch. (Narayana, 1964a) (Hugonioideae) and Fig. 29; Vogel, 1968; Prance & da Silva, 1973; Dicki- Linum (Saunders, 1928; Narayana & Rao, 1976a, son, 1990). In polystemonous flowers of both families, 1977b) and Radiola (Narayana & Rao, 1978b) (both the stamens appear on a ring primordium (Ronse De Linoideae). Obdiplostemony also occurs in Anopyxis Craene & Smets, 1992). In Crossostylis, stamens and (Fig. 2), Carallia (Fig. 7) and Pellacalyx (Rhizophora- staminodes are in two whorls and reach up to 56 ceae; this study), in which the carpels are antepetalous (Setoguchi et al., 1998); however, the so-called stami- and the antepetalous stamens attach morphologically nodes may be mere elaborations of the nectary slightly further outside than the antesepalous stamens (Juncosa, 1988), in which case the androecium organ (topographically higher inside the floral cup). Although number would be up to 28. Among Caryocaraceae, up the antepetalous filaments are longer and broader to 750 stamens per flower were recorded for Caryocar than the antesepalous ones, they are thinner, as and up to 280 for Anthodiscus (Prance & da Silva, expected in obdiplostemonous flowers (Endress, 1973). In polystemonous Cassipourea (Rhizophora- 2010b). Haplostemony by reduction of the antepeta- ceae), a primary ring primordium is formed before

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Figures 130–142. Stigmas at anthesis; from side (in Figs 136 and 139: from above; Fig. 134: bud) (arrow: ventral slit). Figures 130–134. Syncarpous stigmas. Figures 135–142. Apocarpous stigmas. Figs 137, 138, 140, 141. Styles and stigmas unifacial. Figs 130–133, 135, 136. Rhizophoraceae. Fig. 130. Cassipourea congensis (Marcarisieae). Fig. 131. Pellacalyx cristatus (Gynotrocheae). Fig. 132. Carallia suffruticosa (Gynotrocheae). Fig. 133. Ceriops tagal (Rhizophoreae). Fig. 134. Irvingia smithii (Irvingiaceae). Fig. 135. Bruguiera cylindrica (Rhizophoreae). Fig. 136. Rhizophora mucronata (Rhizo- phoreae). Fig. 137. Caryocar brasiliense (Caryocaraceae), stigmatic papillae in a depression in the stigma (arrowhead). Figs 138 and 139. Erythroxylaceae. Fig. 138. Erythroxylum cuneifolium. Fig. 139. Aneulophus africanus. Fig. 140. Ctenolophon englerianus (Ctenolophonaceae). Figs 141 and 142. Linaceae. Fig. 141. Linum kingii (Linoideae). Fig. 142. Reinwardtia indica (Linoideae). Scale bars, 250 mm (Figs 130, 131); 100 mm (Figs 132, 135, 136, 138, 140); 50 mm (Figs 133, 134, 137, 139, 142); 25 mm (Fig. 141).

individual stamens become visible (Juncosa, 1988). In radii (this study). For Ctenolophonaceae, Ronse De other groups studied, the mode of stamen initiation is Craene & Smets (1996) erroneously mentioned double unknown. positions in the antepetalous radii; this was not found As stated by Juncosa (1988), polystemony evolved in the source mentioned by them or in the present independently in three unrelated genera of Rhizopho- study. raceae, and in each genus with different developmen- Among eudicots, in flowers with two stamen whorls, tal patterns, i.e. in Crossostylis (Gynotrocheae): the antesepalous stamens are commonly longer than several antesepalous stamens (see also Setoguchi the antepetalous ones (e.g. Ronse De Craene & Smets, et al., 1998); in Cassipourea (Macarisieae): diploste- 1995; Endress, 2010b). This is the case in Ctenolo- monous or polystemonous (pattern unclear); and in phonaceae (this study; Narayana & Rao, 1971, 1978d; Kandelia (Rhizophoreae): supernumerary stamens Ronse De Craene & Smets, 1995) and a number of associated with petals. Among the species of the Linaceae (this study; Narayana & Rao, 1978d; Ronse present study, collateral double or multiple positions De Craene & Smets, 1995). However, the antepeta- in the androecium (see Endress, 1987, for definition) lous stamens are unexpectedly longer than the were only found in the polystemonous Cassipourea antesepalous stamens in many Rhizophoraceae (Rhizophoraceae), in which stamen arrangement may (Rhizophora, Bruguiera, Ceriops, Carallia, Pellaca- be tentatively interpreted as in two whorls with lyx), in Erythroxylaceae (Aneulophus, Erythroxylum) double or multiple positions in the antepetalous radii and Linaceae (Hugonia) (this study). In Erythroxylum and single or multiple positions in the antesepalous cuneatum, there are flowers with the antepetalous

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Figures 143–149. Gynotroches axillaris (Rhizophoraceae–Gynotrocheae), anthetic gynoecia (in Fig. 147: bud). Figures 143–146. Functionally female flower. Figures 147–149. Functionally male flower. Fig. 143. Longitudinal microtome section of a gynoecium flanked by nectariferous floral cup. Fig. 144. Gynoecium from above with pairs of fused adjacent carpels (arrowheads) joining the syncarpous zone and sharing a ventral slit (arrows) towards the gynoecium centre. Fig. 145. Stigma; ventral. Fig. 146. Exposed ovules within a carpel (one ovule of an adjacent carpel also exposed). Fig. 147. Nectariferous floral cup surrounding a short gynoecial column (asterisk); perianth and stamens removed. Fig. 148. Superior part of gynoecium from side; stigmas (s) surround base of gynoecial column. Fig. 149. Stigma (s); close-up. Scale bars, 500 mm (Figs 143, 147, 149); 100 mm (Figs 144, 146); 50 mm (Figs 145, 148). stamens longer and flowers with all stamens of equal pourea (Rhizophoraceae), the androecial tube has a length, and this in both short-styled and long-styled seam between the stamens, which forms a short lobe morphs (Payens, 1958). in some cases, and the antipetalous filaments are The filaments are shorter than anthers in advanced slightly inside the tube (Floret, 1988), and there are buds but longer at anthesis in Erythroxylaceae and lobes between the stamens on the tube in Anopyxis Linaceae (this study). They remain shorter than the (Fig. 2), Carallia (Fig. 7), Gynotroches (Fig. 88) and anthers at anthesis in Rhizophora and Anopyxis Ceriops (Fig. 13) (this study), Comiphyton Floret (Rhizophoraceae) (this study). (Floret, 1974) and Sterigmapetalum (Steyermark & A basal androecial tube is prominent and occurs in Liesner, 1983). In Pellacalyx, the tube surpasses the all families except Irvingiaceae, which have com- antesepalous stamens on the dorsal side and bears pletely free stamens (this study, Figs 84–99; Harris, the antepetalous anthers on top (Figs 86, 87). In 1999). In contrast, in Anopyxis and Pellacalyx (Rhizo- Erythroxylaceae and Ctenolophonaceae, the andro- phoraceae) the tube is long and only the anthers are ecial tube is elaborated on the dorsal side of the free (this study, Figs 2, 84–87; Hutchinson & Dalziel, stamens into small lobes of irregular shape, giving 1927). The stamens (androecial tube) are fused with the impression of an incipient corona (in Erythroxy- the petals, and they are shed as a unit in Caryocar lum on the dorsal side only in the antepetalous (Vogel, 1968). stamens, but in the antesepalous stamens on the A sometimes minute androecial corona is present in lateral side) (this study, Figs 90–94). In Tirpitzia representatives of Rhizophoraceae (e.g. Figs 6, 13), (Linaceae), each of the five stamens is associated with Erythroxylaceae (Figs 17, 90), Ctenolophonaceae two lobes on the tube and, in addition, two-lobed (Figs 20, 92–94) and Linaceae (Fig. 97). In Cassi- structures represent the five reduced stamens (Suk-

wardtia (this study, Figs 95–97). It is not clear whether and how much these lobes are nectariferous. Anthers are basifixed or nearly basifixed (at base of dorsal side) in most species studied, but more pronouncedly dorsifixed in Gynotroches (female) and Car- allia borneensis (Rhizophoraceae) (Figs 100–119). They are latrorse in Rhizophoraceae–Macarisieae (except Cassipourea elliptica), Erythroxylaceae, Irvin- giaceae and part of Linaceae. They also give the impression of being extrorse in bud in Ceriops (Rhizo- phoraceae); however, they flip over at anthesis and Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 are thus introrse. Anthers are sagittate or x-shaped in all six families and have a connective protrusion in at least some representatives of all six families. Endothecium-like tissue extending over the connective was found in Rhizophora, Cassipourea (Rhizopho- raceae), Roucheria (Linaceae) and Irvingia (this study). An unusual feature restricted to the anthers of Rhizophora is a serial and collateral subdivision of the large pollen sacs into numerous microsporangia (this study, Fig. 15; Warming, 1883; Lakshmanan & Poornima, 1988; Endress & Stumpf, 1990).

Gynoecium Carpel number is often five, three and two, and may increase up to 26. Among Rhizophoraceae, five carpels occur in Gynotroches axillaris (but see also below) (Fig. 9), Carallia suffruticosa (Fig. 7), Pellaca- lyx and Anopyxis (Fig. 3) (this study), among Linaceae in Linum (Fig. 24), Hugonia (this study, Winkler, 1931) and Hebepetalum and Durandea (Winkler, 1931), and among Irvingiaceae in Klainedoxa (Engler, 1931; Eckert, 1966). Carpel number is three among Rhizophoraceae in some Rhizophoreae (Ceriops, Fig. 14; Cassipourea, Fig. 5; this study; Kandelia, Ding Hou, 1958), among Erythroxylaceae in Aneulo- phus (Fig. 19), and Erythroxylum (Fig. 18), this study; (for Aneulophus, see also Winkler, 1931; for Eryth- roxylum, see also Winkler, 1931; Phillips, 1935; Figures 150–157. Rhizophoraceae, disintegrating tissue Narayana, 1960), among Linaceae in Reinwardtia (asterisk) of ovary wall and floral base surrounding ovules. (Fig. 26) and Roucheria (Fig. 22) (this study) (for Figure 150. Rhizophora mucronata, anthetic flower. Fig- Anisadenia, Hesperolinon, Indorouchera Hallier f., ure 151. Bruguiera cylindrica, bud. Figures 152–157. Philbornea Hallier f., Reinwardtia, Roucheria, see Ceriops tagal, transverse sections of ovary (arrows: septa Winkler, 1931; for Reinwardtia, see also Kumar, disintegrating; arrowheads: septa still intact). Figs 152– 1976), and among Caryocaraceae in Caryocar brasil- 154. Young bud. Figs 155–157. Anthetic flower. Figs 152 iense (this study, Fig. 29; see also below). In Eryth- and 155. Level of placenta. Figs 153 and 156. Level below roxylum (Erythroxylaceae) and Roucheria (Linaceae) placenta. Figs 154 and 157. Level below locules (Fig. 154: (Winkler, 1931), there are three locules, but only one base of one locule still present). Scale bars, 250 mm is fertile. Two carpels among Rhizophoraceae occur in (Fig. 150); 500 mm (Figs 151, 155–157); 50 mm (Figs 152– some Rhizophoreae (Rhizophora, Fig. 16; Bruguiera, 154). Fig. 12; this study; Ding Hou, 1958), among Eryth- roxylaceae in Nectaropetalum (this study; Phillips, sathan & Larsen, 2006). In some species of Hesper- 1935), in Ctenolophonaceae (this study, Fig. 21; olinon (Linaceae), two lateral appendages also flank Winkler, 1931), among Linaceae in Linum digynum each stamen filament just above the stamen tube (Winkler, 1931), and among Irvingiaceae in Irvingia (Sharsmith, 1961), slightly also in Linum and Rein- (this study, Fig. 28; Engler, 1931). Four carpels are

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Figures 158–172. Locules with obturators and antitropous ovules; anthetic ﬂower (in Fig. 160: bud) (o, obturator; arrow: part of septum). Figures 158–161, 164–168. Carpels with two collateral ovules. Figures 162, 163, 170–172. Carpels with a single ovule. Figs 165, 167, 169. Close-up of obturators and micropyles. Figs 158–161. Rhizophoraceae. Fig. 158. Cassipourea congensis (Macarisieae). Fig. 159. Carallia suffruticosa (Gynotrocheae), three ovules (1 + 2) visible originating from two different locules because of developmentally secondary unilocular ovary (remaining part of septum indicated, arrow). Fig. 160. Bruguiera cylindrica (Rhizophoreae). Fig. 161. Rhizophora mucronata (Rhizophoreae). Figs 162 and 163. Erythroxylum cuneifolium (Erythroxylaceae). Fig. 162. Micropyle formed by inner integument (arrowhead). Fig. 163. Ovary wall removed to expose fertile (f) and sterile (s) ovules. Figs 164 and 165. Ctenolophon englerianus (Ctenolopho- naceae). Figs 166 and 167. Linum kingii (Linaceae). Fig. 167. Elongate cell from secondary septum present between ovules (arrow). Figs 168 and 169. Reinwardtia indica (Linaceae). Fig. 170. Irvingia smithii (Irvingiaceae). Figs 171 and 172. Caryocar brasiliense. Fig. 172. Ovule from side with disintegrating outer tips of inner integument (asterisk). Scale bars, 100 mm (Figs 158–160, 164, 168, 172); 200 mm (Fig. 161); 50 mm (Figs 162, 163, 165–167, 169, 170); 500 mm (Fig. 171).

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A C D E F G

H I J K L

Figure 173. Schematic median longitudinal sections of anthetic ovules (D, J: immature); embryo sac and vascular bundles indicated by thin lines and a patterned interior; endothelium shaded. A–F, Rhizophoraceae. A, Cassipourea congensis (Marcarisieae). B–C, Gynotroches axillaris (Gynotrocheae) (functionally female ﬂower), showing variation in micropyle position. D–E, Bruguiera cylindrica (Rhizophoreae). D, immature ovule, bud. E, mature ovule. F, Rhizophora mucronata (Rhizophoreae), nucellus and inner cell layers of inner integument disintegrated. G, Erythroxylum cuneifolium (Erythroxylaceae). H, Ctenolophon englerianus (Ctenolophonaceae). I, Linum kingii (Linaceae). J, Reinwardtia indica (Linaceae), immature ovule, bud. K, Irvingia smithii (Irvingiaceae). L, Caryocar brasiliense (Caryocaraceae), lobes of inner and outer integuments disintegrated. Scale bar, 200 mm.

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 398 M. L. MATTHEWS and P. K. ENDRESS Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021

Figures 174–189. Rhizophoraceae and Erythroxylaceae. Transverse microtome sections of sepals and ovaries with a layer of distinctive large cells (laticifers?) (arrowhead) in the mesophyll. Figures 174–181. Sepals; dorsal side above; buds (in Fig. 181: anthetic flower). Figures 182–189. Ovaries; anthetic flowers. Figs 182–185. Layer of distinctive cells (arrow). Figs 186–189. Close-ups. Figs 174–176, 178–180, 182–184, 186–188. Rhizophoraceae. Fig. 174. Anopyxis klaineana (Marcarisieae). Figs 175, 182, 186. Cassipourea congensis (Marcarisieae). Fig. 176. Cassipourea elliptica (Marcarisieae). Fig. 178. Crossostylis grandifolia (Gynotrocheae). Fig. 179. Carallia suffruticosa (Gynotrocheae). Fig. 180. Bruguiera cylindrica (Rhizophoreae). Figs 183 and 187. Gynotroches axillaris (Gynotrocheae); functionally female flower. Figs 184 and 188. Ceriops tagal (Rhizophoreae). Figs 177, 185, 189. Erythroxylum cuneifolium (Erythroxylaceae). Fig. 181. Aneulophus africanus (Erythroxylaceae). Scale bars, 25 mm (Figs 174, 177, 181); 50 mm (Figs 175, 176, 178–180, 189); 500 mm (Figs 182, 183); 250 mm (Figs 184, 185); 100 mm (Figs 186–188). present among Rhizophoraceae in Bruguiera (two to five to ten, Figs 8, 10; Carallia borneensis, six, this four) (Ding Hou, 1958), among Linaceae in Radiola study; Carallia, five to eight, Gynotroches, four to six, and Tirpitzia (Winkler, 1931), and among Caryocar- Pellacalyx, nine to 12, Ding Hou, 1958; Pellacalyx, aceae in Caryocar, see also above) (this study, eight to ten, Crossostylis, up to 20, Juncosa, 1988; and Fig. 30). More than five carpels occur among Rhizo- up to 26 in C. grandiflora, Setoguchi et al., 1996, phoraceae in Gynotrocheae (Gynotroches axillaris, 1998), and among Caryocaraceae in Anthodiscus,

phora and Ctenolophonaceae are type 3 and some Rhizophoraceae are type 2 (this study). The gynoecium is syncarpous in all families. It is completely syncarpous up to the top of the style in some Rhizophoraceae (among them in all Maca- risieae) and in Irvingia (this study, Figs 130–134). Free stigmatic lobes occur in the other Rhizophora- ceae, in Erythroxylaceae, Ctenolophonaceae and Reinwardtia (Linaceae), this study (Figs 135, 136, 138–140, 142). Completely free styles (styluli) are present in Caryocaraceae (Figs 30, 125, 137) and the Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 other Linaceae (this study, Figs 24, 141). Stigmas of individual carpels are capitate in the majority of taxa studied, such as Gynotroches (female) (Rhizophoraceae) (Fig. 145), Erythroxylum (Fig. 138), Nectaropetalum, and Aneulophus (Erythroxylaceae), Ctenolophonaceae (Fig. 140), and Linum (Fig. 141), Reinwardtia (Fig. 142), Hugonia and Roucheria (Linaceae). Syncarpous stigmas are capitate in Anopyxis, Carallia (Fig. 132) and Cassipourea (Fig. 130) (Rhizophoraceae) and in Irvingia (Fig. 134). However, stigmas of individual carpels are punctiform in Rhizophoreae and in Caryocaraceae (this study, Figs 135–137). The stigmatic surface is unicellular– papillate in all families studied here (for Erythroxy- laceae and Linaceae, see also Heslop-Harrison & Shivanna, 1977). However, the papillae are one- to three-cellular in Erythroxylum and one- (or two-) Figures 190–197. Transverse sections of sepals with cellular in Gynotroches (Rhizophoraceae) (this special mucilage cells with a thickened, mucilaginous study). inner tangential wall (asterisk); buds; dorsal side above. Stigmatic lobes are carinal as in most core eudicots. Figures 190–195. Mucilage cells in mesophyll. Figs 190– Only in some Rhizophoraceae with completely united 193. Rhizophoraceae. Figs 190 and 191. Gynotroches axil- carpels (Ceriops, Fig. 14, and Cassipourea)dothe laris (Gynotrocheae), mucilage cells close to the dorsal short stigmatic lobes give the impression of being side. Fig. 190. Functionally female flower. Fig. 191. Func- commissural. However, in contrast to gynoecia with tionally male flower. Fig. 192. Crossostylis grandifolia commissural stigmas (e.g. Matthews & Endress, (Gynotrocheae), mucilage cells close to the ventral side. 2005b), dorsal (and not synlateral) vascular bundles Fig. 193. Rhizophora ¥ lamarckii (Rhizophoreae). Fig. 194. are dominant in the upper part of the gynoecium. Ctenolophon englerianus (Ctenolophonaceae). Fig. 195. In the so-called male flowers of Gynotroches axil- Irvingia smithii (Irvingiaceae). Figures 196 and 197. laris (Rhizophoraceae; Ding Hou, 1958), the stigmas Linaceae. Fig. 196. Linum kingii, mucilage cells in dorsal are not on top of the short columnar protrusion but epidermis. Fig. 197. Reinwardtia indica, mucilage cells in are lower down, close to the upper end of the ovary dorsal hypodermis. Scale bars, 50 mm (Figs 190, 191, 193– (Figs 9B, 10, 147–149). They are superficially remi- 197); 25 mm (Fig. 192). niscent of the secondary stigmas of Sebaea (Gentian- aceae; Kissling, Endress & Bernasconi, 2009). The eight to 20, Caryocar, four to six (Pilger, 1925), Antho- structure and function of these unusual gynoecia, discus, eight to 12, Caryocar three or four (to six) however, is still enigmatic. The ovules appear mal- (Prance & da Silva, 1973). formed and thus are probably sterile. It appears that The ancestral carpel number in Rhizophoraceae was the gynoecium is synascidiate up to the top (thus not probably five and various decreases and increases have comparable with Sebaea), but this needs to be devel- occurred (Juncosa, 1988). However, among the six opmentally studied (Fig. 9B). It also appears that families of this study, only three have representatives PTTT coming from the stigmas curves upwards in the with five carpels, but four have genera with three columnar protrusion, which suggests that the protru- carpels, and five have genera with two carpels. sion forms late in gynoecium development. It should Most species studied here have gynoecia of also be studied whether the pronouncedly different angiospermy type 4 (this study). However, Rhizo- height of the stigmas in ‘male’ (Figs 148, 149) and

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 400 M. L. MATTHEWS and P. K. ENDRESS bisexual flowers (Figs 143–145) reflects any relation- completely septate, except for Anopyxis (Rhizophora- ship with the heterostyly in Erythroxylaceae and ceae), in which the septa are not complete in the Linaceae (unknown as yet in Rhizophoraceae). uppermost part of the placenta (base of symplicate The free styles (styluli) in Erythroxylum coca Lam. zone) (Fig. 3). One of the most interesting floral fea- and Linum bulgaricum Podp. are unifacial based on tures is that the ovary septa are very thin, especially developmental studies (Baum-Leinfellner, (1953). in the basal zone, and partly disintegrate at anthesis Completely round free styles (styluli) with internal- in some Rhizophoraceae (Rhizophora, Fig. 16, Bru- ized PTTT were also found in Ctenolophonaceae (zone guiera, Fig. 12, Ceriops, Carallia, this study; Juncosa, very short) (Figs 20, 21A), Caryocaraceae (Figs 29, 30) 1988) and in Ctenolophonaceae (this study). In other and Linum kingii (Figs 23, 24) (this study). They are Rhizophoraceae, large-celled spongy tissue with large probably also unifacial, but developmental studies are intercellular spaces below the locules disintegrates, Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 needed to confirm this. An open stylar canal in the such as in Gynotroches, Ceriops (Fig. 14), Carallia symplicate zone is absent because of postgenital (Fig. 7), and Pellacalyx (this study, Figs 150–157, 159; fusion of the inner morphological surface, but present Juncosa, 1988). These disintegration processes result in Ctenolophonaceae (this study). However, in many in developmentally secondarily unilocular ovaries groups, this region opens into a small gap at the and, if only the central part of the ovary remains in transition from the style to the ovary (not in a few later development, it gives the wrong impression of a Rhizophoraceae, some Erythroxylaceae and in Irvin- free central placenta. Thus, the statement of a ‘one- giaceae). This central gap is filled with papillate celled ovary with a central axis’ for Kandelia and PTTT, the papillae partly interdigitating in Anopyxis Carallia (Rhizophoraceae) (Ding Hou, 1958) is mis- (Rhizophoraceae), Caryocar and Linum (this study; leading. Extensive disintegration of tissue in the for Linum, see also Sauer, 1933). ovary is mainly present in taxa that form a single The ovary is mostly superior within the six large seed (Juncosa, 1988), which is also shown families, but inferior in many Rhizophoraceae within the single genus Carallia, which contains (Rhizophora, Bruguiera, Ceriops, Gynotroches (male), species with single large seeds and others with Carallia; this study) (superior or slightly inferior in several small seeds (Juncosa, 1988). Spongy tissue Macarisieae, variable in Gynotrocheae, inferior in was also found in Linum and Reinwardtia (Linaceae), Rhizophoreae, Juncosa, 1988), but secondarily supe- especially in the ‘false’ septa (see below). Although the rior in female flowers of Gynotroches (Juncosa, 1988). feature of thin septa is very unusual and therefore The ovary is shortly but conspicuously bulged of special morphological and systematic interest, it upwards so that it gives the impression of an articu- is not uniformly present in Rhizophoraceae, and lation (or that the style pushed into the ovary) among some Linaceae have, in contrast, rather thick septa Rhizophoraceae in Anopyxis (Figs 3, 120, 126), Cassi- (Hugonia, Narayana & Rao, 1977c). pourea (Fig. 121), Gynotroches (this study, Figs 8, 9, Concomitant with the septate ovaries, the placenta 122, 127; Kenfack, Sainge & Thomas, 2006), among is axile in all species studied. The placenta is lateral, Erythroxylaceae in Erythroxylum (this study, Figs 18, except for those groups with uniovulate carpels, in 123, 128; Rao, 1965), Nectaropetalum (Winkler, 1931; which it is median. In most groups, the placenta is in Rao, 1965; Verdcourt, 1981, 1984) and Aneulophus the uppermost part of the locules, but not in Gynotro- (Rao, 1965), among Linaceae in Hugonia (this study, ches (Rhizophoraceae), Irvingiaceae and Caryocar- Fig. 124) and among Caryocaraceae in Caryocar (this aceae (this study). The attachment area for a single study, Figs 29, 30, 125, 129). Anopyxis (Rhizophora- ovule is unusually extensive (in median direction) and ceae) and Erythroxylum are especially similar in encompasses almost the entire length of the locule in detail in also forming slits between the carpels; thus Bruguiera (Rhizophoraceae) (Figs 12A, 173E), Irvin- bulging is not only dorsal but also lateral (Figs 3, 18). gia (Figs 28A, 173K) and Caryocar (Figs 30A, 173L) In addition, there are clefts between the carpels in the (this study). upwardly bulged parts in Erythroxylum as in Chryso- It has long been known that in some Linaceae there balanaceae (but in those everywhere and not only in are ‘false’ septa, i.e. the locules have dorsal secondary the bulged part of the ovary). An apical septum septa subdividing each locule more or less into two (Hartl, 1962), as often present in bulged ovaries, was (van Hooren & Nooteboom, 1984) (e.g. Linum,this found in some Rhizophoraceae, in Aneulophus (Eryth- study, Figs 23, 24; Saunders, 1925; Narayana, 1964a; roxylaceae, Fig. 1), Roucheria (Linaceae) and Caryo- Al-Nowaihi & Khalifa, 1973; Kumar, 1976; Narayana car (Caryocaraceae, Fig. 2) (this study). & Rao, 1976a, 1977b; Reinwardtia, this study, The ovary is synascidiate up to above the placenta Figs 25, 26; Narayana, 1964a; Kumar, 1976; Cathar- except for some Rhizophoraceae and Erythroxylum in tolinum, Narayana & Rao, 1976b; Hesperolinon, which the placenta is located in both the synascidiate Narayana & Rao, 1977a; Radiola, Narayana & and basal symplicate zones (this study). The ovary is Rao, 1978b). In some Rhizophoraceae (Cassipourea;

Rhizophora, Fig. 15M) there is also a faint ridge along primordia become visible on the androecial ring pri- the dorsal side of each locule (this study). mordium in Cassipourea (Juncosa, 1988). A short The ovules fill the locule at anthesis in most cases, gynophore occurs in Anopyxis (Rhizophoraceae) but not in Carallia (Rhizophoraceae) (this study; (Figs 2, 3) and in Linum and Reinwardtia (Linaceae) other cases of non-filling, such as Anopyxis, Nectaro- (Figs 23–26), and a short androgynophore in Eryth- petalum, Roucheria and Ctenolophonaceae, were roxylum (Figs 17, 18) and Ctenolophonaceae (Figs 20, probably attributable to shrinkage in herbarium 21) (this study). specimens). In all six families, the ovules are antitropous (epitropous) (see Glossary) and pendant Ovules (except Gynotroches, female; this study; for the anti- Ovule structure is similar in all six families tropous ovules of Klainedoxa of Irvingiaceae, see (Figs 158–172, 173). However, there are deviations in Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 Engler, 1931) (Figs 158–172). Commonly, there are the mangrove Rhizophoraceae, probably because of two collateral ovules per carpel (Figs 158–161, 164– specialized seed development. Most ovules are weakly 168). However, among Rhizophoraceae there are more crassinucellar (Rhizophoraceae, Karsten, 1891; Cook, than two ovules per carpel in Gynotroches (this study, 1907; Tobe & Raven, 1987b, 1988b); Erythroxylaceae, Fig. 146) (three to eight, Ding Hou, 1958, eight to ten, Boesewinkel & Geenen, 1980; Linaceae, Dorasami & Juncosa, 1988) and Pellacalyx (eight or more; this Gopinath, 1945; Narayana 1964a) or crassinucellar study), and only a single ovule in Erythroxylaceae (Rhizophoraceae, Karsten, 1891; Mauritzon, 1939; (Erythroxylum, this study, Fig. 162, 163; Schulz, 1931; Nikiticheva & Yakovlev, 1985; Erythroxylaceae, Mau- Nectaropetalum, Peglera (under Linaceae), Winkler, ritzon, 1934; Narayana, 1960, 1964b, 1970a; Rao, 1931), Caryocaraceae (this study, Fig. 171; Pilger, 1968; Mametyeva, 1985; Ctenolophonaceae, this 1925; Prance, 1976; Dickison, 1990) and Irvingiaceae study; Linaceae, Narayana, 1964a; Irvingia (this (this study, Fig. 170; Engler, 1931). study); Caryocaraceae (seemingly crassinucellar), In most taxa of the study group, an obturator that Dickison, 1990). Only in a few Rhizophoraceae covers the micropyle(s) is present in the upper ovary (Gynotroches, Pellacalyx; Juncosa & Tobe, 1988) and (this study, Figs 158, 162, 165, 168, 170; for Cassi- some Linaceae (Linum, Reinwardtia, Radiola, pourea and Sterigmapetalum, see also Tobe & Raven, Anisadenia) are the ovules incompletely tenuinucellar 1987b; for Irvingiaceae, see also van Tieghem, 1905; (this study, Mauritzon, 1934; Narayana, 1970b; Harris, 1996; for Linum, see also van Tieghem, 1905; Boesewinkel, 1980). Sutter & Endress, 1995; for Roucheria, see also Rao & Of special interest is that the ovules generally have Narayana, 1965). An obturator is also common in an endothelium (this study; other authors, see below), other Malpighiales, with one or two collateral anti- a feature commonly associated with thin nucelli tropous ovules (e.g. Sutter & Endress, 1995; Merino (Fig. 173). In Rhizophoraceae (not in Ceriops with Sutter, Forster & Endress, 2006; Matthews & early disintegrating inner integument) (Fig. 173A–E) Endress, 2008). However, an obturator is lacking in and perhaps in Erythroxylaceae (Fig. 173G), and Rhizophoreae and Gynotrocheae and in Caryocar Ctenolophonaceae (Fig. 173H), an endothelium is also (this study). The outer integument surrounds the present in crassinucellar ovules, which is a highly obturator, which protrudes into the micropyle, in unusual combination (this study). An endothelium Macarisieae of Rhizophoraceae, Aneulophus of Eryth- was not found in Caryocaraceae (this study). It may roxylaceae and Irvingia (this study). In Linaceae, the be assumed that, in mangrove Rhizophoraceae with obturator is in contact with the inner integument and their large seeds, the ovules became secondarily the micropyle, in Erythroxylum with the inner integu- crassinucellar but retained the endothelium that was ment (this study). ancestrally present in the non-mangrove taxa of the In Rhizophoraceae (except for Rhizophora), lateral family. carpel vascular bundles are lacking in the style and A functional explanation for crassinucellar ovules only extend into the ovary wall. This is also largely with endothelium, also in the other families, could be the case in Erythroxylum. However, in Aneulophus of that, because the nucellus is long and slender, i.e. Erythroxylaceae it is the other way around: the dorsal laterally thin (also in crassinucellar ovules) and the bundles are short and not present in the style, nucellus almost completely disintegrates at the flanks whereas lateral bundles extend up at least to mid- by the expanding embryo sac and thus the embryo sac style level. may laterally come into contact with the inner integu- The gynoecium originates as an annular primor- ment (Fig. 173). In the present study, this was found dium (before individual carpel primordia become in Rhizophoraceae (Anopyxis, Gynotroches, Rhizo- visible) in Cassipourea, Carallia, Bruguiera (Rhizo- phora, Bruguiera, Ceriops), Erythroxylaceae (Eryth- phoraceae; Juncosa, 1988). Furthermore, the gyno- roxylum, Nectaropetalum), Ctenolophonaceae and in ecium primordium is visible before individual stamen Linum (Linaceae). It was otherwise reported in

Bruguiera (Mauritzon, 1939; Juncosa, 1984), Carallia the inner (this study; Cook, 1907), which may be (Tobe, 1987), Ceriops (Tobe & Raven, 1988b), Crosso- interpreted as evolutionarily derived from the condi- stylis (Setoguchi, Tobe & Ohba, 1992), Gynotroches tion in the other, less specialized family members. (Mauritzon, 1939) and Rhizophora (Karsten, 1891) of Developmentally in Rhizophoraceae, Linaceae and Rhizophoraceae, Erythroxylum (Schürhoff, 1924; also other Malpighiales, both integuments are two Mauritzon, 1934; Narayana, 1960, 1964b, 1970a; Rao, cell-layered in the beginning but the inner becomes 1968; Boesewinkel & Geenen, 1980) of Erythroxy- thicker up to anthesis and later (e.g. Juncosa & Tobe, laceae and Linum (Schürhoff, 1924; Dorasami & 1988; Boesewinkel, 1997). Gopinath, 1945; Narayana, 1964a, 1970b; The micropyle is formed by the inner integument Boesewinkel, 1980; Nikiticheva, 1985), Reinwardtia in some Rhizophoraceae (Carallia, Bruguiera, (Narayana, 1964a), Hugonia (Narayana, 1964a) and Nikiticheva & Yakovlev, 1985; but not in material of Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 Roucheria (Rao & Narayana, 1965) of Linaceae. In this study), Erythroxylum (this study, Figs 162, 173G; Bruguiera, the nucellus is not only slender but also Narayana, 1960, 1964b, 1970a; Boesewinkel & much shorter than the massive outer integument Geenen, 1980), Linaceae (this study, e.g. Figures 169, (see below; Mauritzon, 1939; Nikiticheva & Yakovlev, 173J; Roucheria, Rao & Narayana, 1965), and Caryo- 1985). caraceae (Caryocar gracile, Dickison, 1990; but not in Ovules are anatropous or hemianatropous C. brasiliense of this study). However, it is formed by (Figs 158–172, 173), the latter in Ceriops and Anopy- both integuments in some Rhizophoraceae (Anopyxis, xis (Rhizophoraceae) and Caryocaraceae (this study). Carallia, Cassipourea congensis, Figs 158, 173A, Campylotropous anthetic ovules are largely absent, C. elliptica, Gynotroches, Fig. 173B, C, Bruguiera, with the exception of Carallia (Nikiticheva & Yakov- Fig. 173E, Ceriops, Rhizophora, Fig. 173F; this study; lev, 1985) and Bruguiera (Juncosa, 1984) in Rhizo- Crossostylis, Setoguchi et al., 1992; Gynotroches, Pel- phoraceae, and weak campylotropy in Caryocar lacalyx, Juncosa & Tobe, 1988), Erythroxylaceae (Dickison, 1990) becoming more pronounced during (Aneulophus; this study), Ctenolophonaceae (this seed development (Barradas, 1973). study, Figs 164, 165, 173H), Linaceae (Roucheria; The ovules are bitegmic in all six families this study; Linum, Nikiticheva, 1985), Irvingiaceae (Figs 158–172, 173), except for Anthodiscus (Caryo- (this study, Figs 170, 173K; van Tieghem, 1905) and caraceae), where they are unitegmic (Dickison, 1990). Caryocaraceae (Caryocar brasiliense (open), this As in Caryocar the two integuments are united in the study, Figs 172, 173L; Barradas 1973). In addition, lower half, it is likely that unitegmy in Anthodiscus the micropyle is zigzag-shaped in some Rhizophora- originated by complete union of ancestrally two ceae [Cassipourea, Gynotroches, Bruguiera (open integuments (Dickison, 1990). The outer integument zigzag), Ceriops, Rhizophora; this study] and in is mostly semi-annular, but annular in Linum and Ctenolophonaceae (this study). In Linum the micro- Reinwardtia (Linaceae) and Caryocaraceae (this pyle is formed by the inner integument and the outer study). integument on the convex side with the obturator, The inner integument is commonly thicker than the whereas on the raphal side the outer integument is outer (this study; for Rhizophoraceae, see also shorter (Narayana, 1964a; Boesewinkel, 1980), also in Karsten, 1891; Mauritzon, 1939; Juncosa, 1984; Reinwardtia (Narayana, 1964a). Nikiticheva & Yakovlev, 1985; Tobe, 1987; Tobe & Pachychalazal ovules were found in Rhizophora Raven, 1987b; Juncosa & Tobe, 1988; Setoguchi et al., (this study, Fig. 173F) and Bruguiera (only with 1992; for Erythroxylaceae, see also Mauritzon, 1934; regard to the inner integument, Mauritzon, 1939; Narayana, 1964b, 1970a; Rao, 1968; Boesewinkel & Nikiticheva & Yakovlev, 1985) (Fig. 173D, E), prob- Geenen, 1980; for Linaceae, see Guignard, 1893; Mau- ably another adaptation to the specialized seeds in ritzon, 1934; Crété, 1937; Narayana, 1964b; the mangrove habitat. Ovular vasculature extends Boesewinkel, 1980; Nikiticheva, 1985; for Irvingi- into the outer integument in Rhizophoreae (profusely) aceae (not pronounced, see below), see also van (Fig. 173E, F), and Carallia (Rhizophoraceae) (this Tieghem, 1905; Wiger, 1935). This is a conspicuous study, Fig. 7; for Carallia, see also Nikiticheva & tendency in the COM clade and in malvids (Endress Yakovlev, 1985). In Erythroxylaceae, Ctenolopho- & Matthews, 2006b; Endress, 2010a, 2011b). As naceae and Linaceae a single vascular bundle serves exceptions from this tendency in our study group, the the ovule (broad and sometimes appearing as two integuments are of the same thickness in Aneulophus collateral bundles in Erythroxylaceae) and ends in (Erythroxylaceae) (this study) and among Irvingi- the chalaza (this study, Fig. 173G–J; for Erythroxy- aceae in Irvingia (this study; Tobe & Raven, 2011) laceae, see also Narayana, 1960, 1964b; Rao, 1968; and Klainedoxa (van Tieghem, 1905), and, again, the Boesewinkel & Geenen, 1980; for Linaceae, see also mangrove Rhizophoraceae with their specialized Narayana, 1964a; Rao & Narayana, 1965; seeds deviate by the outer integument thicker than Boesewinkel, 1980). In Irvingia and Caryocar the

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 FLOWERS IN RHIZOPHORACEAE AND RELATIVES 403 ovule has an extensive (thick) attachment area at the androecial tube (this study, Fig. 19). The longer the placenta. Instead of a single raphal bundle, bundles androecial tube, the more extensive are the nectaries from the placenta enter the ovule at several levels, in (Link, 1989). In Ctenolophonaceae, corona (dorsal Caryocar extending into the outer integument from skirt) and androecial tube are secretory on the outer there and from the chalaza, in Irvingia forming only surface (this study, Figs 20, 92–94; Narayana & Rao, short lateral branches and ending at the chalaza (this 1971; Link, 1992b). The secretory corona was called study, Fig. 173K, L). The taxa with vascular bundles extrastaminal disk by some authors (van Hooren & extending into the outer integument (Carallia of Nooteboom, 1984). But this term does not do justice to Rhizophoreae, Irvingia) are characterized by large its similarity with some other families of this study seeds. for which this term is not used (but see also Linaceae, Philbornea). In Linaceae, the secretory tissue is on Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 Nectaries the outer slope of the androecial tube in Linum and Nectaries are commonly on the androecial tube (and Reinwardtia (this study, Figs 23, 25, 95, 96), and continuous on the inside surface of the floral cup) in Hugonia (antepetalous positions) (van Hooren & the study group, such as in most Rhizophoraceae (e.g. Nooteboom, (1988b), but on the inner slope (ventral Figs 10, 11), Erythroxylaceae (Fig. 17), Ctenolopho- elaborations) of petals in Cartholinum (Narayana & naceae (Fig. 20), Linaceae (Figs 23, 25) and slightly in Rao, 1976b). In Philbornea there is a prominent thick- Caryocaraceae (Fig. 29). However, we hesitate to call ening (‘extrastaminal disk’) at the base of the outer them discs because the nectariferous area is not or slope of the androecial tube (Narayana & Rao, 1973; only slightly thickened and it is positioned on a steep van Hooren & Nooteboom, 1984). Such a prominent surface. In some Rhizophoraceae the nectaries are thickening is not present in other Linaceae relatively thick structures (Bruguiera, this study; (Narayana & Rao, 1978d, as shown in Narayana & Juncosa & Tomlinson, 1987; Ceriops, this study; Cros- Rao, 1966, 1969, 1974, 1976a, b, 1977a, b, c, 1978a, b). sostylis, Setoguchi et al., 1996, 1998) on the inner Nectaries are lacking in some species of Linum (Well- slope of the androecial tube and in Philbornea wood, 1961) and Hugonia (van Hooren & Nooteboom, (Linaceae) on the outer slope. Only Irvingiaceae are 1988b). In Irvingiaceae, as mentioned above, there is unusual in their simple, open flowers, lack of stamen an intrastaminal disc around the gynoecium, with fusion and a large, intrastaminal nectary disc around lobes between the stamens (Irvingia, this study, the gynoecium (see also Engler, 1931; Link, 1992a; Fig. 27; Link, 1992a). On this disc, areas around Harris, 1996, 1999) (Fig. 27). These three features in single nectar pores are especially cytoplasm-rich, Irvingiaceae are functionally connected, and their comparable with the nectarioles described for some combination was probably also the reason why Irvin- other angiosperms by Vogel (1998). Among Caryocar- giaceae were kept in Simaroubaceae (Sapindales) for aceae, in Caryocar the inner staminodes and the a long time. uppermost part of the inner slope of the androecial In most Rhizophoraceae studied the inner slope of tube are nectariferous (this study, Figs 29, 99; Vogel, the androecial tube (and floral cup if present) shows 1968; Dickison, 1990). In Anthodiscus, a nectary was secretory (nectariferous) tissue (Gynotroches, Figs 8, not identified (Dickison, 1990). 10, Cassipourea elliptica, Fig. 6, Rhizophora, Fig. 15, Bruguiera, Fig. 11, Carallia, Fig. 7; for Carallia, see Histology also Baillon, 1862). In Anopyxis it is the inner and Several Rhizophoraceae have layered water storage outer slope (this study, Fig. 2). In Anopyxis and Cas- tissue on the upper surface of foliage leaves sipourea congensis (Fig. 4) especially, the interstami- (Schimper, 1893). This water storage tissue resembles nal positions of the androecial tube are secretory (this the layered, large-celled tissue found in the sepals of study). In some cases the rim and lobes (corona) of the Rhizophoraceae and Erythroxylaceae in this study androecial tube also seem secretory (Ceriops, this (Figs 174–181), interpreted as laticifers by Juncosa study, Fig. 13; Carallia, this study, Fig. 7; Baillon, (1988). A distinctive hypodermis in the ovary wall 1862; Comiphyton gabonense, Floret, 1974). Among with large, often radially elongate and tanniferous Erythroxylaceae, in Erythroxylum secretory tissue is cells, reminiscent of the laticifers figured for sepals by likewise located close to the inner slope of the andro- Juncosa (1988, fig. 6), is present in most Rhizophora- ecial tube, and also mainly at the interstaminal posi- ceae studied and in Erythroxylaceae (this study, tions, thus resulting in ten nectariferous areas as in Figs 172–189). Erythroxylum has gum-like contents, the mentioned Rhizophoraceae; however, stomata numerous in the cortex (Metcalfe & Chalk, 1950), (nectar pores) are restricted to the outer surface of the which may also correspond. Special mucilage cells in androecial tube (this study, Fig. 17; Link, 1989). In sepals, as defined in Matthews & Endress (2006), Nectaropetalum secretory tissue is at the base of the were found in a few Rhizophoraceae, Ctenolopho- floral cup (this study), and in Aneulophus in the naceae, Linum and Reinwardtia of Linaceae and Irv-

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 404 M. L. MATTHEWS and P. K. ENDRESS ingia (this study, Figs 190–197). In some flowers with clade. Several features are mentioned in more than imbricate aestivation of perianth organs, covered one section, as they have to be considered at different flanks differ from covering flanks, such as in petals of levels of the systematic hierarchy. Ctenolophon (hairs lacking) and in sepals of Hugonia and Reinwardtia (tissue thinner), a feature known (1) Rhizophoraceae and Erythroxylaceae from a number of angiosperms (Endress, 2008). The clade of Rhizophoraceae plus Erythroxylaceae (see Introduction) is well supported by a number of Fruits and seeds shared floral features (this study). Features of special Seeds with an aril are common in the study group. systematic interest at this level (i.e. not randomly They were recorded in some Rhizophoraceae (Tobe & dispersed in Malpighiales but more concentrated in Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 Raven, 1988b; Schwarzbach & Ricklefs, 2000), such some subgroups) are printed in bold. In the phylo- as part of Macarisieae (Juncosa & Tobe, 1988; Comi- genetic analysis by Wurdack & Davis (2009) the phyton, Floret, 1974, 1976; Tobe & Raven, 1988b; small and poorly known genus Paradrypetes appears Blepharistemma, Tobe, 1987; Tobe & Raven, 1988b; as sister to Cassipourea (Rhizophoraceae). We did not Cassipourea, Tobe & Raven, 1987b, 1988b; Breteler, include it in our study. It differs from the families of 2008), Rhizophoreae (Rhizophora, Warming, 1883, our study group by its pronouncedly unisexual and other genera, Juncosa, 1988), and part of flowers, lack of petals, thin, unfused and imbricate Gynotrocheae (Pellacalyx, Gynotroches, Carallia; sepals, and sessile stigmas (see Levin, 1992). A com- Juncosa, 1988, Crossostylis, Corner, 1976; Juncosa & parative study in conjunction with Euphorbiaceae s.l. Tobe, 1988; Tobe & Raven, 1988b; Setoguchi et al., (including Putranjivaceae) will be necessary when 1992, 1998), the same structure forming a wing in sufficient material is available. The list includes fea- Anopyxis, Macarisia and Sterigmapetalum (Tobe & tures shared by Rhizophoraceae and Erythroxy- Raven, 1988b). Among Erythroxylaceae Aneulophus laceae; if they are shared with taxa of other families has an aril (Corner, 1976), Ctenolophonaceae have a of the study group, these are also mentioned in stringy aril (Winkler, 1931; van Hooren & Nooteboom, brackets. 1988a) and in Linaceae Tirpitzia potentially has an aril (Forman, 1965). 1. Floral cup 2. Sepals valvate Fossils 3. Free parts of sepals postgenitally connected Several Late Cretaceous flower fossils from Israel in bud were tentatively ascribed to Rhizophoraceae or rela- 4. Petals with conspicuously narrow attach- tives (Krassilov, 2004). Their state of preservation, ment zone (also in Linaceae) however, does not allow recognition of sufficient 5. Petals conduplicate and enwrapping details to be certain. Other fossil remains (but not stamens or parts of stamens in bud flowers) of more certain affinities with Rhizophora- 6. Petals valvate at least close to the base (also ceae are known from the Eocene onwards (Graham, in Linaceae) 2006). Fossils from the other five families are not 7. Petals postgenitally connected for some dis- known with certainty. tance above the base (also Ctenolophonaceae and Linaceae) 8. Attachment of the stamens of the two FLORAL STRUCTURE AND SYSTEMATICS whorls different: one whorl on the rim, the The following sections summarize floral structural other whorl below the rim: Antesepalous features separately for the major groups treated here stamens on the rim of the tube, but antepetalous and for potential combinations: (1) clade of Rhizopho- stamens slightly inside the tube (Cassipourea, raceae and Erythroxylaceae, features shared by Floret, 1988; Erythroxylum, this study) or ante- the two families; (2) potential clade consisting of sepalous stamens inside the tube (Pellacalyx) Linaceae, Irvingiaceae and Caryocaraceae; (3) poten- 9. Antepetalous stamens longer than antesepa- tial clade consisting of clade 1 plus Ctenolophonaceae, lous stamens (also Hugonia of Linaceae) including features that occur only in one of the two 10. Ovary bulged up on dorsal side (also Hugonia families of clade 1 (Fig. 1B); (4) potential clade con- of Linaceae, Caryocaraceae) sisting of clades 1 and 2, including features that do 11. An apical septum is present in the ovary not occur in each family of clade 1 and/or clade 2 (also Roucheria of Linaceae and Caryocar) (Fig. 1A); (5) potential clade consisting of clades 1 and 12. Ovules antitropous (epitropous) and 2 plus Ctenolophonaceae, including features that do pendant (also in the other four families) not occur in each family of clades 1 and 2; (6) com- 13. Ovules mostly crassinucellar or weakly crassinu- parison at the levels of Malpighiales and the COM cellar (also in the other four families)

14. Nucellus thin and long and early disinte- Wurdack & Davis 2009 (Fig. 1B), and were not grating (also Ctenolophonaceae and Linum) recorded in the three other families. 15. Inner integument with endothelium even in 1. Sepals with less than three vascular bundles (ECt) crassinucellar ovules (probably also Ctenolo- 2. Short androecial tube but filament attachment of phonaceae and Irvingia) one or both of the two stamen whorls not on the 16. The inner integument is thicker than the rim of the tube but slightly inside this tube [RECt; outer at anthesis (also Ctenolophonaceae, in Ctenolophonaceae all stamens, in Cassipourea Linaceae, Caryocaraceae) of Rhizophoraceae and Erythroxylaceae only the 17. Micropyle formed by both integuments in most antepetalous stamens, in Pellacalyx of Rhizopho- Rhizophoraceae and Aneulophus of Erythroxy- raceae only the antesepalous stamens (see above Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 laceae (also Ctenolophonaceae, some Linaceae, for RE)]. Irvingiaceae, part of Caryocaraceae) 3. Short androgynophore (ECt) 18. Nectaries on androecial tube (also Ctenolo- 4. Angiospermy type 3 (Rhizophora of R, Ct) phonaceae, Linaceae, and Caryocaraceae) 5. Ovary septum thin and severed or completely dis- 19. Distinctive layer of large idioblasts in the integrating during development, leading to a mesophyll of the sepals [in Rhizophoraceae developmentally secondarily unilocular ovary (Bruguiera, Cassipourea) (this study; Juncosa, (some R, Ct) 1988) and Erythroxylaceae (Aneulophus, Eryth- 6. Zigzag-shaped micropyle (some R, Ct). roxylum) (this study)]. 7. Lobes of outer integument especially cytoplasm- 20. Aril in many Rhizophoraceae and in Aneulophus rich (RCt) of Erythroxylaceae (Corner, 1976) (also Ctenolo- 8. Seeds with aril (RECt; Rhizophoreae and part of phonaceae) Gynotrocheae, Juncosa, 1988; Aneulophus of 21. Sieve-element plastids of a special subtype Erythroxylaceae, Corner, 1976; Ctenolophonaceae, of protein-containing plastids (PV) (Behnke, Winkler, 1931) 1982) 9. Stellate hairs with each branch representing a cell 22. Long colleters on stipules or close to stipule scars (Pellacalyx of R, Ct; in the latter not unicellular, in (Thiebaut & Hoffmann, 2005), but colleters are contrast to Saad, 1962) also reported from Caryocaraceae (Paiva & Machado, 2006) and other rosid families (4) Rhizophoraceae (R), Erythroxylaceae (E), (Thomas, 1991). They may be present in all fami- Linaceae (L), Irvingiaceae (I) and Caryocaraceae lies of this study but are just understudied (Ca) A number of floral features of interest are present in (2) Linaceae, Irvingiaceae and Caryocaraceae families of this group retrieved as a clade by Soltis This group was retrieved as a clade with weak et al., 2007) (Fig. 1A). Features that are likely plesio- support by Soltis et al. (2007), considering 28 families morphies or synapomorphies are marked with *. Fea- of the current Malpighiales. We did not find any tures that are likely autapomorphies or of very special floral features exclusively shared by Linaceae, uncertain status (because of their rarity in one or more Irvingiaceae and Caryocaraceae among the study of the families where they occur) are not marked. group. Three unusual characters are shared only by Irvingiaceae and Caryocaraceae: (1) Petals with three 1. Sepals with more than three vascular traces vascular traces in Irvingia and Caryocar; (2) attach- (RELI) ment of ovules at the placenta extensive (in median 2. Sepals with sclereids (REL) direction) in Irvingia and Caryocar (to some extent 3. Petals thick (RELCa)* also in Bruguiera); and (3) lack of an endothelium, 4. Petals with extremely narrow attachment area but nucellus periphery cytoplasm-rich and full of (REL)* starch grains, and nucellus apex with radially elon- 5. Petals with ventral elaborations and (EL)* gate epidermal cells. A number of features are shared 6. Petals with lateral elaborations (RLCa)* with families of the other clades studied. Thus, a 7. Petals valvate, at least close to the base (REL)* clade of Linaceae–Irvingiaceae–Caryocaraceae is not 8. Antepetalous stamens longer than antesepalous obviously supported by floral structure. stamens (REL)* 9. Anthers x-shaped (RELICa)* (3) Rhizophoraceae (R), Erythroxylaceae (E) and 10. Gynophore (REL)* Ctenolophonaceae (Ct) 11. Heterostyly (EL)* A number of special features are shared by at least 12. Angiospermy type 4 (RELICa)* one family of the Rhizophoraceae–Erythroxylaceae 13. Ovary bulged up on dorsal side (RELCa) clade and Ctenolophonaceae, a clade retrieved by 14. Apical septum (RELCa)

15. Ovary with partial secondary septa (RL) 22. Inner integument thicker than outer (RECtLCa) 16. Ovary with one fertile and two sterile locules 23. Inner integument with endothelium (also in (Erythroxylum, Roucheria of L) crassinucellar and weakly crassinucellar ovules!) 17. Campylotropous ovules (RLCa) (RECtL) 18. Outer integument surrounding obturator (REI) 24. Micropyle formed by both integuments (all six 19. Carpel dorsal bundle short (ECa) families, with few exceptions) 20. Carpel lateral bundles short and extending only 25. Ovule bundles branching from synlateral bundles up to ovary (RELI)* (RECtLI) 21. Ovular vascular bundle extending into outer 26. Nectaries on androecial tube (RECtLCa) integument (RCa) 27. Aril (RECt, perhaps L) 22. Micropyle formed by inner integument (RELCa) 28. Special mucilage cells in sepals (RCtLI) Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 23. Pollen with capitate bacula (especially in E, 29. Pedicel articulated (all six families) Oltmann, 1968, and L, Saad, 1962)* 30. Opposite leaves (at least part of R, Aneulophus of 24. Similarity of stipule development (EI, Weberling, E, Ct, some L, Caryocar) Lörcher & Böhnke, 1980)* (6) Study group and systematic surroundings, (5) Study group in general especially other Malpighiales, Celastrales and The following features are shared by at least one Oxalidales family of each of the major groups of this study; those The following features are shared by the study group in bold are features of special systematic interest at with taxa of other families of Malpighiales and the this level. other orders of the COM clade, Celastrales and Oxal- idales, and may be symplesiomorphies or synapomor- 1. Convex floral base (sepals join base distinctly phies or apomorphic tendencies for Malpighiales or below other organs) (ECtLICa) the COM clade: 2. Sepals thick (all six families) 3. Synsepaly (RECtLCa, only few exceptions 1. Floral cup (also in Chrysobalanaceae and Euph- within the families) roniaceae, Prance & White, 1988; Endress, 2008; 4. Sepals decurrent on floral base or floral cup and scattered in other Malpighiales) (RECtLCa) 2. Synsepaly (also occasionally in other Malpighi- 5. Petals forming protective organs and not ales, Matthews & Endress, 2008) retarded in bud (ECtLICa) 3. Sepals valvate (scattered in some other Malpighi- 6. Petal aestivation contort (RCtL) ales; common in Oxalidales, Matthews & 7. Petals postgenitally fused (by interdigitat- Endress, 2002; and a number of Myrtales and ing epidermal cells) or hooked together in Malvales) bud (RECtL) 4. Very narrow petal attachment (also in Chrysobal- 8. Androecial tube and petals fuse above floral anaceae s.l., Matthews & Endress, 2008; Myr- base (RECtLCa) tales and Geraniales, e.g. Schönenberger & Conti, 9. Diplostemony or obdiplostemony at least partly 2003; Endress, 2010b) (RECtLI) 5. Petals not retarded and forming protective 10. Androecial corona (RECtL) organs in advanced buds (not common in Mal- 11. Anthers basifixed or nearly basifixed (all six fami- pighiales, only exceptionally in Chrysobalanaceae lies) s.l., Matthews & Endress, 2008, also Achariaceae, 12. Anthers sagittate (RECtL) Bernhard, 1999a, Goupiaceae, Mitchell, 2002; 13. Anthers with connective protrusion (RECtLCa) Humiriaceae, Sabatier, 2002) 14. Gynophore or androgynophore (some R, ECtL) 6. Contort petal aestivation (relatively common in 15. Styles unifacial (ECtLCa) Malpighiales and malvids) 16. Ovary mostly superior (all six families) 7. Conduplicate, stamen-enwrapping petals 17. Synascidiate zone well developed (all six families) (unusual, also present in Elaeocarpaceae and 18. Carpels with one or two (collateral) (median if Tremandraceae of Oxalidales, Matthews & one) antitropous, pendant ovules (all six families) Endress, 2002) 19. Obturator present (except for Rhizophoreae and 8. Postgenitally united petals by postgenital fusion Gynotrocheae of Rhizophoraceae and Caryocar) (not common, also Oxalidaceae, Hartl, 1957, and 20. Ovules mostly crassinucellar or weakly crassinu- Connaraceae in Oxalidales Matthews & Endress, cellar (all six families) 2002; Stackhousia in Celastraceae, Matthews & 21. Nucellus thin and long, early disintegrating Endress, 2005a, and Rutaceae in Sapindales, (before embryo sac is mature) (RECtL) Hartl, 1957)

9. Postgenitally united petals by hooking (unusual, 20. Ovules with endothelium even if crassinucellar also in Oxalidaceae and Connaraceae of Oxal- (because nucellus is slender and partly disinte- idales, Matthews & Endress, 2002) grates early) (unusual, nucellus early disintegrat- 10. Androecial tube (also common in some other ing among other Malpighiales also in families of Malpighiales) Dichapetalaceae, but there the ovules are incom- 11. Gynophore or androgynophore [also in some other pletely tenuinucellar; Boesewinkel & Bouman, Malpighiales, in Oxalidales (rare), and a number 1980; Endress, 2008; for Malpighiales, see also of malvids s.str.; Endress & Matthews 2006b; Tobe & Raven, 2011) Endress 2010a] 21. Zigzag micropyle (quite common in the COM clade 12. Gynoecium becoming visible before individual and in malvids; Endress & Matthews, 2006b) stamens are visible in polystemonous flowers 22. Vascular bundles in outer integument (also in Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 (also in some other Malpighiales, such as Achari- some other Malpighiales, especially Euphorbi- aceae, Bernhard & Endress, 1999; scattered in aceae s.l., e.g. Tokuoka & Tobe, 2006) core eudicots, such as Capparis L., Capparaceae, 23. Nectaries on androecial tube (inner or outer slope Leins & Metzenauer, 1979; Halimium Spach, Cis- of stamen base) (also Oxalidaceae and Con- taceae, Nandi, 1998; Bixa L., Bixaceae, Ronse naraceae of Oxalidales [outer slope because inside Decraene, 1989; Tetracera L., Dilleniaceae, fused], Lepidobotryaceae of Celastrales [inner and Endress, 1997; Couroupita Aubl., Lecythidaceae, outer slope], Geraniales [outer slope because Endress, 1994, 2006; Schima Reinw. ex Blume, inside fused], Endress 2010b; Caryophyllales Theaceae, Tsou, 1998) [inner or outer slope], Rohweder 1967; Zandonella 13. Angiospermy type 4 (among Malpighiales also in 1977) Chrysobalanaceae s.l., Matthews & Endress, 24. Seeds with aril (also in a number of other Mal- 2008; Picrodendraceae, Merino Sutter et al., pighiales, especially the parietal clade and 2006; and also in Celastrales, Matthews & Euphorbiaceae s.l., also Celastrales, Matthews & Endress, 2005a, but not in Oxalidales, where it is Endress, 2005a) mostly type 3, Matthews & Endress, 2002; type 4 25. Articulate pedicel (also common in other Malpighi- also in Anacardiaceae and Burseraceae and ales, Stevens, 2001 onwards, e.g. in all four fami- mostly in Nitrariaceae of Sapindales, Bachelier & lies of Chrysobalanaceae s.l. (Matthews & Endress, 2009; Bachelier, Endress & Ronse De Endress, 2008) Craene, in press) 26. Special mucilage cells in sepals (also in some other 14 Free styles (styluli) non-plicate, round, unifacial, Malpighiales and some Oxalidales, Matthews with internalized PTTT (not common in et al., 2001; Matthews & Endress, 2002, 2006, angiosperms, among Malpighiales also known 2008). from Passiflora, Bernhard, 1999b; otherwise 27. Glands on the outside of sepals occur in Anisad- among rosids from some Cucurbitales, Matthews enia (Linaceae) and Caryocar. These glands have & Endress, 2005b; and Fagales, Endress, 1967) different structures and are likely not a synapo- 15. Ovary dorsally bulged up, commonly associated morphy. However, there are several other Mal- with apical septum (also in a number of other pighiales with glands on the outer sepal surface, Malpighiales, however, not always as tight to the similar to those in Caryocar (e.g. some Chrysobal- style as in the study group) anaceae, Humiriaceae, Malpighiaceae and Passi- 16. Secondary septa in the locules or at least ridges floraceae). The feature may be an apomorphic along the dorsal part of the locules (ridges scat- tendency in Malpighiales. tered in Malpighiales, e.g. Ixonanthaceae, 28. Tristyly is known from Linaceae (Lloyd et al., Narayana & Rao, 1978c, and several Oxalidales; 1990) and Oxalidales (for literature, see Matthews Matthews & Endress, 2002) & Endress, 2002) and is otherwise very rare in 17. Large-celled spongy tissue surrounding the ovary angiosperms locules that disintegrates around the single large seed (also in Fagales (Betulaceae; Endress, (7) Families potentially related with the study group 1967) Lepidobotryaceae are a small family, the systematic 18. Ovules one or two antitropous, collateral and position of which has changed extensively in the past. pendant, and obturator (also Chrysobalanaceae Lepidobotrys was originally placed with Linaceae s.l., Matthews & Endress, 2008; Euphorbiaceae (Engler, 1903). More recently, the family was placed s.l., Merino Sutter et al., 2006) as sister to Celastraceae plus Parnassiaceae in Celas- 19. Inner integument thicker than outer (common in trales (Savolainen et al., 2000b; Davis & Wurdack, the COM clade and malvids; Endress & Mat- 2004, Zhang & Simmons, 2006; Wurdack & Davis, thews, 2006b) 2009). Lepidobotryaceae share more unusual floral

© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 408 M. L. MATTHEWS and P. K. ENDRESS features with Linaceae and relatives than with centation (often misunderstood as free central placen- Celastraceae, as shown in the comparative study by tation) is a rare feature at the level of eudicots and Matthews & Endress (2005a), and even more in the best known otherwise from some Caryophyllaceae present study. The flowers are diplostemonous (vs. (e.g. Rohweder, 1967). haplostemonous), have carinal stigmas (vs. commis- Rhizophoraceae and Erythroxylaceae are well sup- sural), antitropous ovules (vs. syntropous), pro- ported as forming a clade by floral structure. Both nounced protruding obturators (vs. no obturators), Ctenolophonaceae and Linaceae–Irvingiaceae– vascular bundles in the outer integument (vs. lacking) Caryocaraceae, and among them especially Linaceae, and nectaries on the androecial tube (vs. disc around share features of interest at the systematic level of gynoecium). If the phylogenetic position of Lepidobot- the focus of this study with Rhizophoraceae and ryaceae in Celastrales is correct, it would imply that Erythroxylaceae. Ctenolophonaceae are of special Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 the shared features with Malpighiales could be ple- interest as potentially related family to Rhizophora- siomorphic for Celastrales and Malpighiales, and ceae and Erythroxylaceae, not by the number of deviating features in Celastrales derived. shared features, but by their general rarity. The most The families Goupiaceae, Humiriaceae, Ixonan- obvious diverging floral structures among the six thaceae and Lophopyxidaceae have similarities with families are in Caryocaraceae (androecium extremely the families studied here. It remains to be seen in polystemonous, ovules not supplied by derivatives of which exact position they will appear in future phy- synlateral vascular bundles, endothelium lacking) logenetic analyses of Malpighiales. and Irvingiaceae (staminal tube lacking, nectary disc present, conspicuous thickening of inner integument lacking). In sum: that Linaceae, Irvingiaceae and CONCLUSIONS Caryocaraceae form a clade is not well supported by The following features of the study group are of floral morphology. Other potentially related families, special interest because they are unusual at the level such as Goupiaceae, Humiriaceae, Ixonanthaceae and of Malpighiales and core eudicots in general: (1) Petal Lophopyxidaceae, or also additional families need to aestivation with unusual combination: basally be studied in comparison with those families in the valvate but contort above (Linaceae) or quincuncial future concomitant with the increase of the phyloge- above (Erythroxylaceae); (2) Presence of a zone of netic resolution of relationships between families postgenital fusion of petals above the base (some within Malpighiales. Rhizophoraceae, Ctenolophonaceae, some Linaceae). Such a zone is otherwise known from Oxalidales, ACKNOWLEDGEMENTS (Hartl, 1957; Matthews & Endress 2002), Celastrales Charles Davis, Kenneth Wurdack and Andreas (Stackhousia) (Matthews & Endress 2005a); and Worberg are thanked for providing unpublished Rutaceae, Hartl (1957), and from Gentianales, in molecular phylogenetic results and useful discussion which it is especially obvious in flowers with lateral during the project. We thank the herbaria Z, K, L and entrances; for example, Ceropegia, or flowers with MO, especially Reto Nyffler (Z), Peter Stevens (MO), fenestrate corolla tubes (Endress, 2010a). (3) Post- Gerard Thijsse (L) and Emma Tredwell (K) for assis- genital union of petals by hooking together, thus a tance in obtaining valuable floral material. Adrian postgenital connection at the morphological level! Juncosa (DAV) is thanked for material from his col- (Erythroxylum, Linaceae, Caryocaraceae). This is oth- lection of Rhizophoraceae and Luisa Kinoshita, Uni- erwise known from a few Oxalidales (Matthews & versity of Campinas, Brazil, for Caryocar brasiliense. Endress, 2002). (4) Antepetalous stamen filaments Thanks are given to Anita Lendel for many of the longer than antepetalous ones (many Rhizophoraceae, microtome sections and for additional assistance Erythroxylaceae, and Hugonia of Linaceae). This during the project. From the University of Zurich, feature, which is rare at the level of the core eudicots, Gery Barmettler and the Center for Microscopy and is also known from some Protium species of Burser- Image Analysis (ZMB), plus Christof Eichenberger aceae (Sapindales, Bachelier & Endress, 2009). (5) and Urs Jauch from the Institute of Plant Biology are Presence of an androecial corona (some Rhizophora- thanked for support with the SEM. We thank Maria ceae, Erythroxylaceae, Ctenolophonaceae, and von Balthazar and Peter Stevens for valuable com- Linaceae). 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