Gynoecium diversity and systematics in basal monocots

Botanical Journal of the Linnean Society (2001), 136: 1–65. With 232 figures doi:10.1006/bojl.2000.0424, available online at http://www.idealibrary.com on

Gynoecium diversity and systematics in basal monocots ANTON IGERSHEIM, MATYAS BUZGO and PETER K. ENDRESS FLS∗ Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland Received October 1999; accepted for publication September 2000

Gynoecium and ovule structure was comparatively studied in representatives of the basal monocots, including Acorales (Acoraceae), Alismatales (Araceae, Alismataceae, Aponogetonaceae, Butomaceae, Hydrocharitaceae, Juncaginaceae, Limnocharitaceae, Potamogetonaceae, Scheuchzeriaceae, Tofieldiaceae), Dioscoreales (Dioscoreaceae, Taccaceae), and Triuridaceae as a family of uncertain position in monocots. In all taxa studied the carpels or gynoecia are closed at anthesis. This closure is attained in different ways: (1) by secretion without postgenital fusion (Araceae, Hydrocharitaceae); (2) by partly postgenitally fused periphery but with a completely unfused canal (Alismataceae, Aponogetonaceae, Butomaceae, Limnocharitaceae, Scheuchzeriaceae, Dioscoreaceae, Taccaceae); (3) by completely postgenitally fused periphery but with an unfused canal in the centre (Acoraceae, Tofieldiaceae); (4) by complete postgenital fusion and without an (unfused) canal (Juncaginaceae, Potamogetonaceae). In many Alismatales (but without Araceae) carpels have two lateral lobes. The stigmatic surface is restricted to the uppermost part of the ventral slit (if the carpel is plicate); it is never distinctly double-crested (Butomaceae?). Stigmas are commonly unicellular-papillate and secretory in most taxa. The locules are filled with a (often) mucilaginous secretion in a number of taxa. Superficial (probably intrusive) ethereal oil cells were found in the carpel wall of Acorus gramineus (as in Piperales!). Idioblasts in carpels are otherwise rare. A number of basal monocots has orthotropous ovules, which is perhaps the plesiomorphic condition in the group. The presence of almost tenuinucellar (pseudocrassinucellar) ovules is relatively common (Acoraceae, many Araceae, some Alismatales s.s.), whereas completely tenuinucellar ovules are rare and do not characterize larger groups. However, crassinucellar ovules occur in the largest number of families among the study group (basal Araceae, many Alismatales s.s.) The outer integument is always annular in orthotropous ovules. The inner integument is often lobed and it mostly forms the micropyle, whereas the outer integument is always unlobed. Gynoecium structure supports the isolated position of Acoraceae as sister to all other monocots. However, in an overall view, if compared with all other families, Acoraceae  2001 The Linnean Society of London clearly shows the greatest similarities with Araceae. ADDITIONAL KEYWORDS: Acorales – Alismatales – angiosperm systematics – angiospermy – carpels – Dioscoreales – flower evolution – ovules – Triuridales.

were not present or not prominent in the groups treated in our former contributions. Recent molecular systematic studies on one or several genes and also combined morphological and molecular analyses increasingly show that monocots are monophyletic and corroborate the hypothesis that Acorus (Acoraceae) is the basalmost clade among extant monocots, followed by Araceae and Alismatales as a clade or grade (e.g. Chase et al., 1993, 1995, 2000; Duvall et al., 1995; Nadot et al., 1995; Hahn, 1998; Doyle, 1998; Ka¨llersjo¨ et al., 1998; Kubitzki et al., 1998; Davis et al., 1999; Soltis et al., 2000). These taxa had also been recognized as a clade by Dahlgren, Clifford & Yeo (1985). Members of the paleoherbs, such as Nymphaeales, Aristolochiales or Piperales are most

INTRODUCTION This is the last of a series of five publications on the comparative morphology, anatomy and histology of gynoecia in all major groups of basal angiosperms (Endress & Igersheim, 1997, 1999; Igersheim & Endress, 1997, 1998). These five contributions are all structured in the same way in order to facilitate intergroup comparison. However, further aspects have been included here than in the first contributions. These include carpel vasculature and a few additional characters of carpel morphology and histology that

∗ Corresponding author. E-mail: [email protected] 0024–4074/01/050001+65 $35.00/0

1

 2001 The Linnean Society of London

2

A. IGERSHEIM ET AL.

favoured as putative sister groups of monocots (Dahlgren et al., 1985; Loconte & Stevenson, 1991; Chase et al., 1993; Qiu et al., 1993; Doyle, Donoghue & Zimmer, 1994). However, identification of the sister group of monocots has remained problematic due to poor resolution (Ka¨llersjo¨ et al., 1998; Soltis, Soltis & Chase, 1999; Chase et al., 2000). In addition, in some recent studies, Acorus does not appear as sister group to all other monocots, though still near the base of monocots (e.g. Qiu et al., 1999; Stevenson et al., 2000). In this study we include all families that have been discussed as basal monocots on structural and molecular grounds, in addition to Acoraceae also Alismatales (incl. Araceae), Dioscoreales and Triuridaceae. This allows discussion of character evolution on the basis of molecular systematic studies, as well as suggestions of systematic relationships on the basis of new structural traits. We present original results on these basal families and at the same time consider the literature as exhaustively as possible, which enables us to recognize the unbalanced coverage of the subgroups of the families in the published record. The arrangement of the orders and families follows the proposal by the Angiosperm Phylogeny Group (APG, 1998). In this treatment Araceae are included in Alismatales. In the discussion we use Alismatales s.s., if the group in its earlier circumscription is meant (i.e. without Araceae). For the circumscription of the families of Alismatales the family treatments in Kubitzki (1998b) are used. In larger families basal genera were studied as much as possible (for Araceae, see Mayo, Bogner & Boyce, 1997, for Hydrocharitaceae, see Tanaka, Setoguchi & Murata, 1997). Among Alismatales, families with only underwater-pollination or only water-surface-pollination were not studied because most likely their flowers are highly modified, and it can be expected that they show many advanced (reduced) features. These families are Cymodoceaceae, Najadaceae, Posidoniaceae, Ruppiaceae, Zannichelliaceae, and Zosteraceae (Kubitzki, 1998c). However, also for these families the literature was considered as exhaustively as possible.

MATERIAL AND METHODS Morphological and anatomical studies were carried out on the taxa and collections (preserved in FAA or ethanol) listed in Table 1. For serial microtome sections two techniques were applied. (1) Plant material was dehydrated in an ethanol and Histo-Clear II series and embedded in Paraplast, then sectioned with a rotary microtome. The 10
m thick sections were stained with Astrablue and safranin. (2) Plant material was embedded in Kulzer’s Technovit (2-hydroxyethyl methacrylate), as described

in Igersheim (1993) and Igersheim & Cichocki (1996), and sectioned with a Microm HM 355 rotary microtome and conventional microtome knife type C. For contrast enhancement of the mostly 6
m thick sections ruthenium red staining was post-stained with toluidine blue (Weber & Igersheim, 1994). Mucilaginous substances of pectic nature were localized with ruthenium red (Gerlach, 1984). The receptive stigmatic area in Tacca chantrieri was localized with KMnO4. The stained sections were enclosed in Histomount. Oxalate crystals and druses as well as starch grains were observed under crossed polarizing filters. For SEM studies the specimens were dehydrated in an ethanol series and acetone, and then critical-point dried. The dried specimens were mounted with nail polish on aluminum stubs and sputter-coated with gold. All LM-micrographs were prepared from sections of methacrylate embedded material and analysed using an Olympus BX 50 microscope and a PM10 ADS camera system on Agfapan 25. The films were developed with Agfa Rodinal at a mixing ratio of 1:50 at a temperature of 20° for 10 min. All vouchers and the permanent slides of the microtome sections are deposited at the Institute of Systematic Botany of the University of Zurich (Z). ABBREVIATIONS USED IN FIGURES

c f i n o ov st

carpel funicle inner integument nucellus outer integument ovule stigma

RESULTS The descriptions are based on our original results on the genera indicated in Table 1. For reports from the literature authors are cited, and genera are cited if the characters are not known to be common in the family. Carpel features in the family descriptions are taken from carpels at anthesis (mature carpels). Ovule features are taken from ovules at the time of embryo sac maturity (mature ovules), which in several taxa is a considerable time after anthesis. Sizes of carpels and ovules are artificially categorized in the same way as in previous publications of this series of studies on gynoecia in basal angiosperms to facilitiate large scale comparisons (see Endress & Igersheim, 1997, 1999; Igersheim & Endress, 1997, 1998). Carpels: very small (less than 1 mm long), small (1–3 mm long), medium (4–9 mm long), large (10–2 mm long), very large (more

GYNOECIUM IN BASAL MONOCOTS

3

Table 1. Collection data. (Abbreviations: BGZ=cultivated, Botanic Garden of the University of Zurich; E=P.K. Endress). In species with several collections respective figures are indicated Acorales Acoraceae Acorus calamus L., E 5180, BGZ (Fig. 228); E 7225, BGZ (Fig. 229); A. Igersheim s.n., coll. 11. v. 1999, BGZ (Figs 1–9, 232) Acorus gramineus Sol., A. Igersheim s.n., coll. 19.v.1999, BGZ Alismatales Araceae Gymnostachys anceps R.Br., M. Buzgo 814, New South Wales, Australia Orontium aquaticum L., E 4693, BGZ (Figs 20, 21, 27–29; A. Igersheim s.n., 5.vi.1999, BGZ (Figs 22, 23, 24–26, 232) Pothos longipes Schott, E 9097, Northern Queensland, Australia Alismataceae Alisma lanceolatum With., E 7696, BGZ Damasonium alisma Mill., E 99–44, BGZ Luronium natans Raf., E 99–37, BGZ (Figs 70, 71); E 99–42, BGZ (Figs 63–69, 72, 232) Aponogetonaceae Aponogeton distachyos L.f., E 98–148, BGZ Aponogeton ulvaceus Baker, E 6738, BGZ Butomaceae Butomus umbellatus L., E 4676, BGZ (Figs 85–95, 98, 229, 232); E 5196, BGZ (Fig. 228); A. Igersheim s.n., 9.vi.1999, BGZ (Fig. 84); A. Igersheim s.n., 10.vi.1999, BGZ (Figs 96, 97, 231) Hydrocharitaceae Elodea nuttallii H. St.John, E 99–38, BGZ Hydrocharis morsus-ranae L., E 9716, BGZ (Fig. 229); A. Igersheim s.n., 22.vii.1999, BGZ (Figs 115–117, 120, 228, 232); A. Igersheim s.n., 28.vii.1999, BGZ (Figs 113, 114, 118, 119) Stratiotes aloides L., E 4689, BGZ (Figs 121, 123–125); E 99–39, BGZ (Figs 122, 126–130, 232) Vallisneria americana Michx., C.D.K. Cook s.n., coll. 23.vii.1991, BGZ Juncaginaceae Triglochin maritima L., M. Buzgo 786, BGZ Limnocharitaceae Hydrocleys nymphoides Buchenau, E 7568, BGZ (Figs 150–154, 157, 230, 232); E 9719, BGZ (Figs 147–149, 155, 156), E 99–43, BGZ (Figs 228, 231) Potamogetonaceae Groenlandia densa Fourr., M. Buzgo 921, BGZ Potamogeton alpinus Balb., M. Buzgo 939, Switzerland Scheuchzeriaceae Scheuchzeria palustris L., E 6701, Switzerland Tofieldiaceae Tofieldia calyculata Wahlenb., E 6708, Switzerland incertae sedis in monocots Triuridaceae Sciaphila albescens Benth., de Granville et al. 5791, French Guiana (received from H. Maas) Dioscoreales Dioscoreaceae Tamus communis L., Igersheim 990504-2/1b, Crete Taccaceae Tacca chantrieri Andre´, E 9530, BGZ (Figs 228, 230); E 99–36, BGZ (Figs 217, 221–227, 232); A. Igersheim s.n., 30.vii. 1999, BGZ (Figs 218–220, 231)

than 20 mm long). In gynoecia with inferior ovaries, length was defined as extension from the base of ovarial cavity up to gynoecial tip. Ovules: very small (less than 0.1 mm long), small (0.1–0.2 mm long), medium

(0.3–0.5 mm long), large (0.6–1.0 mm long), very large (more than 1.0 mm long). Although almost all ovules are crassinucellar (or at least not completely tenuinucellar), the breadth of the nucellus is not uniform (as

4

A. IGERSHEIM ET AL.

measured at the broadest level in transverse direction): narrow (less than 0.1 mm broad), medium (0.1–0.2 mm broad), broad (more than 0.2 mm broad). Numbers of cell layers of integuments were determined at midlevel. ACORACEAE (ACORALES) (Figs 1–10, 228, 229, 232)

The flowers are bisexual (Buzgo, 1999). Carpels 3, small, whorled, syncarpous, synascidiate (c. threequarters of the length) and symplicate (c. one-quarter of the length), plicate only for a very short distance; ovary superior. The carpel apex is not extended into two lateral tips. The ovary locules are slightly bulged up. The septa are exceedingly thin. The ovules do not fill the locules but the micropyles are in close contact with the ovary wall. Septal nectaries are absent; however, there are non-secretory slits between the carpels in the symplicate and upper synascidiate zone (Buzgo, 1999; Buzgo & Endress, 2000). The stigma is minute, slightly immersed in the upper end of each ventral slit (Buzgo, 1999). It is unicellularpapillate and secretory. The gynoecium portion above the ovary is about the same length as the ovary; it is massive and not attenuated into a style. The inner surface of the carpel flanks above the ovary is not postgenitally fused except for a short distance just below the stigma (angiospermy type 3). Ovary locules and pollen tube transmitting tract are filled with secretion. Long hairs around the placentae produce the mucilaginous secretion in the locules (Dalmer, 1880; Rudall, Prychid & Jones, 1998). Pollen tube transmitting tissue is one-layered and well differentiated. A compitum is present in the symplicate zone. The carpel surface is glabrous. Stomata are present. Cells with oxalate crystals and druses and tanniferous cells are present in the ovary wall. Ethereal oil cells are present at the surface of the carpel wall (intrusive?) in A. gramineus (not found in A. calamus). Cells with oxalate raphides, sclereids, mucilage cells, and laticifers are lacking. Intercellular cavities are present. Ovules 2–6 per carpel (Eyde, Nicolson & Sherwin, 1967; Buzgo, 1999), with distinct funicle, large, pseudocrassinucellar (term after Davis, 1966; the cell layers surrounding the meiocyte are formed by periclinal division of the epidermis and not by division of the archesporial cell; Mu¨cke, 1908; Buell, 1938; Rudall & Furness, 1997); in addition, the nucellus becomes relatively thick by radial elongation of the subepidermal cells surrounding the embryo sac. The ovules are bitegmic, orthotropous (van Tieghem, 1907), pendant, apical; chalaza unextended; an aril is lacking. Placenta in the synascidiate zone, median and lateral, linear. Nucellus medium, with a single meiocyte (Mu¨cke, 1908; Rudall & Furness, 1997). The micropyle

is formed by the inner integument, which is considerably longer than the outer (van Tieghem, 1907; Ju¨ssen, 1928; Buell, 1938); the inner integument is not lignified (in contrast to van Tieghem, 1907); a micropylar cavity is lacking. A nucellar beak is lacking. The inner integument is lobed, and the lobes are papillate in Acorus calamus (Buzgo, 1999) (but see also French, 1987; Rudall & Furness, 1997); the papillae elongate into hairs in fruit development (Mu¨cke, 1908; Ju¨ssen, 1928). It is not lobed in A. gramineus. The outer integument is not lobed. Both integuments are annular. The inner integument is convoluted (only in A. calamus), but not the outer one. The outer integument is 3–4 cell layers thick in A. calamus (3 in A. gramineus), the inner is 2 layers thick. Tanniferous tissue occurs in the hypostase. Cells with oxalate crystals/druses/raphides, oil cells, and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza. ARACEAE (INCL. LEMNACEAE) (ALISMATALES) (Figs 11–40, 228, 229, 232)

The study is focused on the basal subfamilies of Araceae (Gymnostachydoideae, Orontioideae, Pothoideae) (cf. Mayo et al., 1997). Information on the remaining, more advanced groups (including Lemnaceae) is added from the literature. In the basal subfamilies the flowers are bisexual (Mayo et al., 1997). Carpels 1 (Gymnostachys, Orontium), 2–3 (Pothos), in most other genera 1 or 2, in Pedicellarum 3 (Mayo et al., 1997). In genera with a single carpel (Gymnostachys, Lysichitum, Orontium) the gynoecium has been interpreted as possibly pseudomonomerous (Engler, 1920; Eckardt, 1937; Eyde et al., 1967; Barabe´ & Labrecque, 1984), but this is still uncertain. The carpels are small, whorled, ascidiate or symplicate-synascidiate; ovary superior (partially inferior in species of Pothos; Eyde et al., 1967; and in Symplocarpus; Barabe´, Forget & Chre´tien, 1987b). The carpel apex is not extended into two lateral tips. The locules are bulged up dorsally in Pothos; the septa are exceedingly thin. The ovules commonly do not fill the locules (Gymnostachys is an exception); they are (Orontium) or are not (Pothos) in close contact with the ovary wall. Septal nectaries are absent (Daumann, 1970), only stigmatic nectaries (and perianth nectaries) are present in the family (Anthurium, Daumann, 1931b; Croat, 1980; Monstera, Ramı´rez & Go´mez, 1978). The stigma is small, around the orifice of the carpel or gynoecium, dry, smooth (Gymnostachys) or secretory, papillate (unicellular in Orontium, pluricellular-uniseriate in Pothos) (see also Buzgo, 1999). A style is absent. The inner space of the carpels is closed by secretion, postgenital fusion is lacking (angiospermy

GYNOECIUM IN BASAL MONOCOTS

5

Figures 1–9. Acorus calamus (Acoraceae), female stage of anthesis. Fig. 1. Gynoecium from above. Fig. 2. Part of Fig. 1, showing the unicellular-papillate, secretory stigma. Figs 3–6, 9. TS gynoecium at different levels. Fig. 3. Slightly immersed stigmatic region. Fig. 4. Below stigma (arrow-heads point to ventral slits). Fig. 5. Separate pollen tube transmitting tracts (arrow-heads). Fig. 6. Ovary with placentae (level indicated in Fig. 8 by arrow-head). Fig. 7. Ovules from the side (asterisks indicate secretion in locule). Fig. 8. LS ovary and ovules (arrow-head indicates level of Fig. 6). Fig. 9. TS ovules. Fig. 10. Acorus gramineus (Acoraceae), female stage of anthesis; TS gynoecium surface with oil cell. Scale bars: Figs 1, 6=0.5 mm; Figs 4, 5, 7–9=0.25 mm; Figs 2, 3, 10=0.1 mm.

type 1). Ovary locules are filled with secretion (only partially in Gymnostachys). Pollen tube transmitting tissue is one-layered and well differentiated. Long placental hairs are present (Orontium) or absent (Gymnostachys, Pothos) (absent also in Symplocarpus;

French, 1987). In a large comparative study French (1987) showed that there is a correlation between the presence of mucilage and placental hairs. Mucilage is produced by these hairs (Dalmer, 1880; Rudall et al., 1998), or, in other cases, by the entire wall of the locule

6

A. IGERSHEIM ET AL.

Figures 11–19. Gymnostachys anceps (Araceae), female stage of anthesis. Fig. 11. Gynoecium from the side. Fig. 12. Stigma from above. Fig. 13. LS upper part of carpel with unfused inner surface (arrow-heads indicate levels in Figs 14 and 15). Fig. 14. TS upper carpel region. Fig. 15. Above locule. Fig. 16. TS ovary and ovule. Fig. 17. Ovule from the side (single integument marked with star). Fig. 18. Ovule with exposed nucellar apex (single integument marked with star). Fig. 19. Median LS carpel and ovule (single integument marked with star). Scale bars: Figs 11, 13–16, 19= 0.25 mm; Figs 17, 18=0.1 mm; Fig. 12=0.05 mm.

(Eyde et al., 1967). The layered structure of the secreted material around the hairs indicates that it is secreted in pulses (Pothos; this study). A compitum is present in gynoecia with more than one carpel (Pothos). The carpel surface is glabrous. Stomata are present. Tanniferous cells are present (Orontium) or absent (Gymnostachys, Pothos). Cells with oxalate raphides are present (Gymnostachys, Orontium, Pothos) (also Anthurium; Manya-Chernej, 1978; Pothoidium; Eyde et al., 1967); cells with oxalate druses are present

(Pothos, Orontium) or absent (Gymnostachys); cells with simple oxalate crystals are present in Pothos. Sclereids, ethereal oil cells and mucilage cells are lacking. Intercellular cavities are present (Orontium) or absent (Gymnostachys, Pothos). Laticifers, although present in vegetative parts (Engler, 1920), are not known from the flowers of any Araceae (Eyde et al., 1967). Ovules 1 per carpel (Gymnostachys, Orontium, Pothos) and in most other basal Araceae, 1–2 in Lysichiton

GYNOECIUM IN BASAL MONOCOTS

7

Figures 20–29. Orontium aquaticum (Araceae), female stage of anthesis. Fig. 20. Gynoecium from above. Fig. 21. LS upper part of gynoecium with unfused inner surface (asterisks mark secretion). Fig. 22. Median LS ovule (arrow-head points to micropyle). Fig. 23. Part of Fig. 22, showing micropyle (arrow-head). Fig. 24. Ovule from the side (arrowhead points to micropyle). Fig. 25. Ovule with micropyle (arrow-head). Fig. 26. Part of Fig. 25, showing lobed inner integument. Figs 27–29. TS ovule at different levels. Fig. 27. Middle nucellar region. Fig. 28. Upper nucellar region. Fig. 29. Slightly below micropyle (arrow-head points to lobed inner integument). Scale bars: Figs 20, 22=0.5 mm; Figs 21, 23–25, 27–29=0.25 mm; Fig. 26=0.1 mm.

and Anthurium (Mayo et al., 1997) and Symplocarpus (Rosendahl, 1909); medium (Gymnostachys, Pothos) or large (Orontium), crassinucellar (Gymnostachys, Orontium) (also Lysichiton; Campbell, 1899, 1900; Symplocarpus; Gow, 1907; Rosendahl, 1909; Ju¨ssen, 1928;

probably Anthurium; Campbell, 1905), unitegmic (Gymnostachys) (Buzgo, 1999) or bitegmic (Orontium, Pothos) (the outer integument is only short in Lysichiton; Campbell, 1899, 1900; and Symplocarpus; Hofmeister, 1852; Rosendahl, 1909; Ju¨ssen, 1928),

8

A. IGERSHEIM ET AL.

Figures 30–40. Pothos longipes (Araceae), female stage of anthesis. Fig. 30. Gynoecium from the side. Fig. 31. Gynoecium from above. Fig. 32. Pluricellular-uniseriate, secretory stigma from above. Fig. 33. LS upper part of gynoecium with unfused inner surface (asterisk indicates secretion). Fig. 34. Part of Fig. 33 (arrow-heads indicate levels of Figs 35 and 36). Fig. 35. TS stigma (arrow-head points to unfused canal) (level indicated in Fig. 34). Fig. 36. TS pollen tube transmitting tract (level indicated in Fig. 34). Fig. 37. Placenta with ovules from above (asterisks indicate secretion in locule). Fig. 38. Ovule in oblique lateral view (arrow-head points to micropyle; asterisk indicates secretion). Fig. 39. Ovule, with micropylar region formed by outer integument (asterisk indicates secretion). Fig. 40. TS ovules (asterisk indicates secretion). Scale bars: Figs 30, 31=0.5 mm; Figs 33, 37=0.25 mm; Figs 32, 34–36, 38–40= 0.1 mm.

orthotropous (Gymnostachys) (also in Lysichiton; Campbell, 1899, 1900; Barabe´ & Labrecque, 1984, and Symplocarpus; French, 1986), hemianatropousanatropous (Orontium) (also Anthurium; Campbell,

1900, 1905; Gow, 1913) or anatropous (Pothos); pendant (apical: Gymnostachys; inserted at mid-height: Pothos) or ascendant, basal (Orontium); chalaza unextended (Orontium, Pothos) (somewhat extended in

GYNOECIUM IN BASAL MONOCOTS

Gymnostachys in compensation of the reduced integument/nucellus complex); an aril is lacking. Placenta median, in the (syn-)ascidiate zone. Nucellus medium (Gymnostachys, Orontium) or narrow (Pothos), with a single meiocyte (Campbell, 1905; Rosendahl, 1909; Gow, 1907, 1913). The embryo sac is inferior in Anthurium (Gow, 1913). The micropyle is formed by the inner integument (Orontium, Pothos) or is lacking (Gymnostachys) (according to Hofmeister, 1861, in Pothos pentaphylla by both integuments); a micropylar cavity is lacking. A nucellar beak is lacking. The outer integument is unlobed, the inner is lobed (Orontium) or unlobed (Pothos); the single integument of Gymnostachys is lobed. The outer integument is annular-semiannular (Orontium) or semiannular (Pothos). The single integument of Gymnostachys and the inner integument of the other genera is annular. The integuments are not convoluted. The outer integument is 8 cell layers thick in Pothos, and 22–26 in Orontium, the inner is 6 layers thick in Pothos, and 3(–4) in Orontium, the single integument in Gymnostachys is 4 cell layers thick; the outer integument in Lysichiton is also very thick (Campbell, 1900). van Tieghem (1907) mentions that the inner integument in Orontium has an especially differentiated inner epidermis with radially elongated cells (not present in Symplocarpus; Ju¨ssen, 1928). Tanniferous tissue, cells with oxalate druses/crystals/raphides, oil cells and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza and there may form a plate-like structure (Lysichiton, Orontium; French, 1986). The more advanced subfamilies of Araceae (True Araceae minus Pothoideae, sensu Mayo et al., 1997), also including Lemnaceae, are more diverse in gynoecium and ovule structures. The flowers are bisexual or unisexual. The gynoecium is commonly urn- or flaskshaped, (syn-)ascidiate or symplicate, without any apical lobes, as in the basal Araceae (e.g. Lehmann & Sattler, 1992; Scribailo & Tomlinson, 1992; Buzgo, 1994) (apically lobed only in a few genera, Mayo et al., 1997), but carpel (locule) number varies between 1 (all Areae and many other genera) and up to 47 (Philodendron; Mayo, 1989) (in several genera also possibly pseudomonomerous; Engler, 1920; Eckardt, 1937). The stigma is commonly small but may also be large in a few genera (Mayo et al., 1997). It is secretory or dry (Heslop-Harrison & Shivanna, 1977), secretory in Lemnaceae. Each carpel may have a separate stylar canal (Philodendron p.p.; Mayo, 1989) or the separate canals unite in the upper zone into a single one (e.g. Dracontium; Poisson & Barabe´, 1998; Philodendron p.p.; Mayo, 1989), or there is only one stylar canal. Commonly the ovary locule is bulged up peripherally so that its roof descends in the centre to form a collarlike protrusion surrounding the stylar canal, which

9

may contact the ovule(s). Long, unicellular or uniseriate-pluricellular (secretory) hairs are common around this roof and/or around the placenta (Capus, 1879; Dalmer, 1880; Rowlee, 1896; Gue´guen, 1901; French, 1987; Buzgo, 1994). In genera without placental hairs secretion in the locule is also lacking (Arisamea, Theriophonum, Typhonium; French, 1987). In the extreme case hairs may completely fill the locule (Lagenandra; Svedelius, 1910). The pollen tube transmitting tissue between stigma and ovary seems to be several-cell-layered (Capus, 1879). Ovule number per locule or per gynoecium (if it is unicarpellate) varies between 1 and many (up to 30 in Aridarum; Hotta, 1971; up to more than 35 in Pistia; Buzgo, 1994; up to 51 in Philodendron; Mayo, 1989; Mayo et al., 1997); in Lemnaceae it varies between 1 and 5 (Landolt, 1986). Placentae are diverse: basal, apical, axile or parietal, and linear, protruding-diffuse or basal-diffuse. Basal ovule position is especially common in the more advanced subfamilies; they are commonly ascendant, more rarely pendant or horizontal (in a few genera both apical/pendant and basal/ascendant in the same ovary; e.g. Dracunculus, Helicodiceros, Heteroaridarum and Theriophonum; Parameswaran, 1959; Mayo et al., 1997). Ovules have diverse expression of curvature between orthotropous, hemianatropous and anatropous forms; slightly campylotropous or amphitropous forms also occur. A number of tribes and even some genera (Philodendron, Steudnera) contain ovules with different curvature patterns (French, 1986). Orthotropous ovules occur in some Spathicarpeae, some Schismatoglottideae, some Peltandreae, most Colocasieae, all Arophyteae, and all Areae (French, 1986; Grayum, 1991; Mayo et al., 1997). Slightly campylotropous or amphitropous ovules have been reported in a few genera (French, 1986; Grayum, 1991). Also in Lemnaceae there is some variation: the ovules are almost anatropous in Spirodela (Maheshwari, 1958; Maheshwari & Maheshwari, 1963), hemianatropous in Lemna (Hofmeister, 1861; Hegelmaier, 1868, 1871; Caldwell, 1899; Lawalre´e, 1952; Shih, 1979), and orthotropous in the most reduced genus Wolffia (Gupta, 1935; Maheshwari, 1954). Many genera have ovules with a distinct funicle (Mayo et al., 1997). Two integuments are present; the outer one may be short at the time of embryo sac maturity (Lemna; Maheshwari & Kapil, 1963; Wolffia; Maheshwari, 1954); in Montrichardia there is only one integument, according to Goebel (1897). The micropyle is commonly formed by the inner integument (but by both integuments in Dieffenbachia; Nephthytis; Gow, 1908; Lagenandra; Panicker, 1965; Pistia; Kubin, 1878; Shadowsky, 1931; Spirodela; Maheshwari & Maheshwari; 1963; and Synandrospadix; Cocucci, 1966). In Calla the micropyle bears hairs, which make contact with the hairs at the lower end of the stylar canal

10

A. IGERSHEIM ET AL.

(Dalmer, 1880). Ovules are crassinucellar in a few genera (Calla; Ju¨ssen, 1928; Lemna; Hegelmaier, 1868; Jo¨nsson, 1881; Caldwell, 1899; Lawalre´e, 1952; Maheshwari & Kapil, 1963; Spirodela; Maheshwari, 1958; Maheshwari & Maheshwari, 1963; Lacor, 1970); Wolffia; Gupta, 1935; Maheshwari, 1954; probably also Peltandra; Goldberg, 1941); in most genera they are pseudocrassinucellar (Dieffenbachia, Campbell, 1900; Aglaonema; Campbell, 1912; Gow, 1908; Richardia; Gow, 1913; Michell, 1916; Arum, Homalomena, Spathiphyllum, Zantedeschia; Ju¨ssen, 1928; Typhonium; Banerji, 1947; Arisaema; Pickett, 1913; Maheshwari & Khanna, 1956; Theriophonum; Parameswaran, 1959; Lagenandra; Panicker, 1965; probably Nephthytis, Campbell, 1905); only in very few genera they are tenuinucellar (Pistia; Shadowsky, 1931; Synandrospadix; Cocucci, 1966). When the embryo sac is mature, commonly the lateral parts of the nucellus are degenerated and the embryo sac is directly adjacent to the inner integument; at the apex and base the nucellus remains (Ju¨ssen, 1928). This occurs even in crassinucellar ovules (Lemna; Caldwell, 1899; Peltandra; Goldberg, 1941; Spirodela; Maheshwari & Maheshwari, 1963). Concomitantly, the inner epidermis of the inner integument differentiates as an integumentary ‘tapetum’ with radially elongated cells (Pistia; Hofmeister, 1861; Kubin, 1878; Shadowsky, 1931; Mercado-Noriel & Mercado, 1978; Spathicarpa; Campbell, 1903; Richardia; Gow, 1913; Michell, 1916; Arum, Calla, Homalomena, Spathicarpa, Spathiphyllum, Xanthosoma; Ju¨ssen, 1928; Ambrosinia; Vignoli, 1939; Arisaema; Pickett, 1913, 1915; Maheshwari & Khanna, 1956; Lagenandra; Svedelius, 1910; Panicker, 1965; Synandrospadix; Cocucci, 1966; Theriophonum; Swamy & Krishnamurthy, 1970). Generally a single meiocyte is formed (Caldwell, 1899; Campbell, 1900, 1903, 1912; Gow, 1913; Ju¨ssen, 1928; Shadowsky, 1931; Gupta, 1935; Goldberg, 1941; Banerji, 1947; Lawalre´e, 1952; Maheshwari, 1954; Maheshwari & Khanna, 1956; Parameswaran, 1959; Maheshwari & Kapil, 1963; Maheshwari & Maheshwari, 1963; Panicker, 1965; Cocucci, 1966); several meiocytes were reported from Arisaema (Pickett, 1913). The embryo sac is commonly superior (but at least partially inferior, in cases where the nucellus is more reduced than the chalaza, such as in Homalomena, Philodendron; Gow, 1913; Lagenandra; Panicker, 1965; Lemna; Lawalre´e, 1952; Maheshwari & Kapil, 1963; Peltandra; Goldberg, 1941; Spirodela; Maheshwari & Maheshwari, 1963; Wolffia; Gupta, 1935; Maheshwari, 1954). A postament is formed in Arisaema (Pickett, 1913) and Peltandra (Goldberg, 1941). Integument thickness: Lagenandra; outer 2 cell layers, inner 2; Svedelius, 1910; Panicker, 1965; Lemna; outer 2, inner 2, Maheshwari & Kapil,

1963; Philodendron; outer 3, inner 2; Hofmeister, 1852; Spirodela; outer 3, inner 2–3; Maheshwari & Maheshwari, 1963; Synandrospadix; outer c. 7, inner 2–3; Cocucci, 1966). The vascular supply of ovules is diverse (French, 1986). In Arophyteae, Alocasia, Ariopsis, Peltandra, Pinellia, Typhonium and Typhonodorum the vascular bundle divides in the chalaza into several bundles (French, 1986).

ALISMATACEAE (ALISMATALES) (Figs 41–72, 228, 229, 232)

The flowers are bisexual or unisexual (Haynes, Les & Holm-Nielsen, 1998c). Carpels 3–20 (up to 660 in Sagittaria; Salisbury, 1926; Kaul, 1967a), small, whorled (in Alisma and other genera in more than one whorl; Singh & Sattler, 1973; Sattler & Singh, 1978; van Heel, 1983) or irregular if numerous (Leins & Stadler, 1973; Charlton, 1991; Wang et al., 1998), free (in Damasonium basally united via the undifferentiated floral centre), largely plicate but in early development pronouncedly ascidiate (Alisma, Caldesia, Echinodorus; Sprotte, 1940; Eckardt, 1957; Singh & Sattler, 1972; Sattler, 1973; van Heel, 1983; Wang & Chen, 1997); dorsally pronouncedly expanded so that the outlet of the ovarial cavity on the ventral side is restricted to a very short zone near the base of each carpel (Gre´goire, 1938; Eckardt, 1957); ovary superior. The carpel apex is not extended into two lateral tips. The ovule fills the locule. Septal nectaries are present (Schaffner, 1897; Daumann, 1931a, 1964, 1970; van Heel, 1988). The stigma extends only around the upper part of the ventral slit. It is unicellular-papillate, dry or weakly secretory (also Heslop-Harrison & Shivanna, 1977; for Echinodorus). A style is present. The ventral slit is postgenitally fused (see also Baum, 1948), but a thin unfused canal discharges into the stigmatic region (angiospermy type 2). The locule is not filled with secretion. Pollen tube transmitting tissue is onelayered and well differentiated. A compitum is lacking. The carpel surface is glabrous. Stomata are present (Alisma) or absent (Luronium, Damasonium). Tanniferous tissue, sclereids, cells with oxalate crystals/ druses/raphides, ethereal oil cells, and mucilage cells are absent in the carpel wall. Laticifers are present in the carpel wall (see also Tomlinson, 1982). Intercellular cavities are absent. Ovule 1 per carpel in most genera (in Damasonium mostly 2 to up to more than 10; Kaul, 1976), with distinct funicle, medium, pseudocrassinucellar to tenuinucellar (with the meiocyte subepidermal and some but not all epidermal cells around the meiocyte periclinally divided) (Alisma; Nitzschke, 1914; Dahlgren, 1928; Johri, 1936a; Kudryashov & Savich,

GYNOECIUM IN BASAL MONOCOTS

11

Figures 41–50. Alisma lanceolatum (Alismataceae), female stage of anthesis. Fig. 41. Gynoecium from above. Fig. 42. Gynoecium from the side. Figs 43, 44. TS carpels at different levels. Fig. 43. Stigma, unicellular-papillate. Fig. 44. Below stigma (arrow-heads point to ventral slits). Fig. 45. TS gynoecium, ovaries. Figs 46, 47. TS ovule. Fig. 46. Nucellar region. Fig. 47. Micropylar region (arrow-head points to pollen tube transmitting tissue). Fig. 48. Ovule from the side (arrow-head points to micropyle). Fig. 49. Micropylar region of ovule (arrow-head points to micropyle). Fig. 50. Median LS ovule (arrow-head points to micropyle). Scale bars: Figs 41, 42, 45, 48=0.5 mm; Fig. 50=0.25 mm; Figs 43, 44, 46, 47, 49=0.1 mm.

1963; Pogan, 1965; Frey, 1966; Damasonium; Maheshwari & Singh, 1943; Echinodorus; Nitzschke, 1914; Dahlgren, 1927, 1934; Limnophyton; Johri, 1933, 1935b; Sagittaria; Cook, 1907; Dahlgren, 1934; Johri,

1935d; Nikiticheva, 1990a), or tenuinucellar (Alisma; Fischer, 1880), bitegmic, at the time of fertilization anatropous, then becoming campylotropous (Alisma; Hofmeister, 1861; Fischer, 1880; Ward, 1880;

12

A. IGERSHEIM ET AL.

Figures 51–59. Damasonium alisma (Alismataceae), female stage of anthesis. Fig. 51. Gynoecium from the side. Fig. 52. Adaxial side of carpels (arrow-heads point to ventral slits). Fig. 53. Part of Fig. 52, showing the unicellular-papillate, secretory stigma. Figs 54–59. TS gynoecium at different levels. Fig. 54. Stigmas. Fig. 55. Below stigma (arrow-head points to thin, unfused secretory canal). Fig. 56. TS upper ovules in nucellar region (arrow-head points to pollen tube transmitting tissue). Fig. 57. TS upper ovules in micropylar region (at left). Fig. 58. Basally united carpels. Fig. 59. Below Fig. 58, with septal nectaries (arrow-heads). Scale bars: Fig. 58=1 mm; Figs 51, 52=0.5 mm; Figs 54–57, 59= 0.25 mm; Fig. 53=0.1 mm.

GYNOECIUM IN BASAL MONOCOTS

13

Figures 60–62. Damasonium alisma (Alismataceae), female stage of anthesis. Fig. 60. Median LS carpel and ovules (arrow-head points to septal nectary). Fig. 61. Part of Fig. 60, micropyle formed by inner integument. Fig. 62. Ovule from the side (arrow-head points to micropyle). Scale bars: Fig. 60=0.25 mm; Figs 61, 62=0.1 mm.

Dahlgren, 1928; Johri, 1936a; Kudryashov & Savich, 1963; Pogan, 1965; Frey, 1966; Swamy & Krishnamurthy; 1970; Damasonium, incl. Machaerocarpus; Maheshwari & Singh, 1943; Echinodorus, Dahlgren, 1934; Limnophyton; Johri, 1935b; Sagittaria; Schaffner, 1897; Johri, 1935d; Nikiticheva, 1990a), ascendant, basal; chalaza unextended; an aril is lacking. Placenta median in genera with a single ovule per carpel (see also Bessey, 1898; Eckardt, 1957; Charlton & Ahmed, 1973), in Damasonium the lowermost ovule median, others lateral, linear. The ovule of Luronium (as Elisma) is directed to the opposite side than that in other Alismataceae, although it has a median position (antitropous; Endress, 1994) (see also Buchenau, 1869, and Baillon, 1892). Nucellus narrow (in Damasonium medium), with a single meiocyte (Fischer, 1880; Schaffner, 1896; Bessey, 1898; Dahlgren, 1928, 1934; Johri, 1933, 1935b,c; Murthy, 1933; Maheshwari & Singh, 1943; Kudryashov & Savich, 1963; Pogan, 1965; Frey, 1966), exceptionally with more than one meiocyte (Johri, 1936a). The micropyle is formed by the inner integument (Ward, 1880; Schaffner, 1896; Dahlgren, 1928, 1934; Johri, 1935b, 1936a; Maheshwari & Singh, 1943; Frey, 1966; Serbanescu-Jitariu, 1974a; Nikiticheva, 1990a). A micropylar cavity is lacking. A nucellar beak is lacking. Both integuments are unlobed. The outer integument is semiannular, the inner is annular. Both integuments are not convoluted. Both integuments are 2 cell layers thick. Tanniferous tissue, cells with oxalate crystals/druses/raphides, oil cells and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza. APONOGETONACEAE (ALISMATALES) (Figs 73–83, 228, 229, 232)

The flowers are bisexual or unisexual (female) (van Bruggen, 1998). Carpels (2–)3(–9) (van Bruggen, 1985),

small, whorled, almost completely free or united at the base of the ovary for a short distance via the floral centre (see also Eber, 1934; Singh, 1965c), completely plicate (ovules in apocarpous zone in our material, but partly in the syncarpous zone in Eber, 1934); dorsally somewhat bulged up; ovary superior. The carpel apex is not extended into two lateral tips. The ovules do not fill the locule and are not in close contact with the ovary wall. Septal nectaries are present according to Daumann (1970). In our material of Aponogeton distachyos histologically weakly differentiated areas at the base of the gynoecium were present that may correspond to septal nectaries; however, in A. ulvaceus they were lacking. The stigma extends only around the upper part of the ventral slit. It is smooth and strongly secretory (unicellular-papillate and dry, according to HeslopHarrison & Shivanna, 1977). A style is present. The ventral slit of the carpels is postgenitally fused along the periphery but unfused and filled with secretion in the centre of the style (angiospermy type 2) (see also Gue´guen, 1901). The locule is not filled with secretion (A. ulvaceus) or partly filled with secretion (A. distachyos). Pollen tube transmitting tissue is onelayered, well differentiated, in the unfused canal of the ventral slit (in A. distachyos weakly differentiated). A compitum is lacking. The carpel surface is glabrous. Stomata are present. Cells with oxalate crystals are present (but without druses and raphides). Sclereids, tanniferous tissue, oil cells, and mucilage cells are absent. Intercellular cavities are present. Laticifers were found in A. ulvaceus but not in A. distachyos. Ovules 2–12 (4–6 in A. ulvaceus, 2–4 in A. distachyos) per carpel (van Bruggen, 1998), medium, crassinucellar (Sergue´eff, 1907; Afzelius, 1920; Saˆne´, 1939; Bouman, 1985), bitegmic (unitegmic in A. distachyos; Sergue´eff, 1907; transitions from bitegmy to (almost)

14

A. IGERSHEIM ET AL.

Figures 63–72. Luronium natans (Alismataceae), female stage of anthesis. Fig. 63. Upper part of gynoecium from the side. Fig. 64. Carpel from the side. Fig. 65. Carpel from ventral side (arrow-heads point to ventral slit). Figs 66–71. TS carpels (gynoecium) at different levels. Fig. 66. Below stigma (large arrow-head points to thin, unfused secretory canal; small arrow-head points to postgenitally fused ventral slit). Fig. 67. Ovary (arrow-head points to ventral slit). Fig. 68. Below Fig. 67 (arrow-head points to ventral slit). Fig. 69. Below placenta, carpel removed from centre of flower (arrow-head points to pollen tube transmitting tissue). Fig. 70. Gynoecium base (arrow-heads point to septal nectaries). Fig. 71. Part of Fig. 70 (arrow-heads point to septal nectaries). Fig. 72. Median LS ovule (arrow-head points to micropyle). Scale bars: Figs 63–65, 70=0.25 mm; Figs 66–69, 71, 72=0.1 mm.

GYNOECIUM IN BASAL MONOCOTS

15

Figures 73–83. Aponogeton ulvaceus (Aponogetonaceae), female stage of anthesis. Fig. 73. Gynoecium from above (arrow-heads point to ventral slits). Fig. 74. Carpel from the side. Fig. 75. Carpel from adaxial side (arrow-head points to ventral slit). Fig. 76. Stigma (asterisk indicates secretion). Figs 77–82. TS gynoecium at different levels. Fig. 77. Stigmatic region. Fig. 78. Below stigma (large arrow-head points to thin unfused secretory canal, small arrow-head to fused part of ventral slit). Fig. 79. Ovaries (arrow-heads point to ventral slits). Fig. 80. Part of Fig. 79, with TS ovules (arrow-heads point to pollen tube transmitting tissue). Fig. 81. Transition between apocarpous and syncarpous zone (arrow-head). Fig. 82. Syncarpous zone. Fig. 83. Median LS ovule (arrow-head points to micropyle). Scale bars: Figs 73–75=0.5 mm; Figs 77–83=0.25 mm; Fig. 76=0.1 mm.

unitegmy within the genus; Afzelius, 1920; Riede, 1921; Bouman, 1985), anatropous (to hemianatropous; Bouman, 1985), ascendant, almost basal (Planchon, 1844); chalaza unextended; an aril is lacking. Placenta in the plicate zone, lateral, linear (Singh & Sattler, 1977). Nucellus medium, commonly with a single meiocyte, exceptionally with more than one (Afzelius, 1920;

Saˆne´, 1939). The micropyle is formed by the inner integument (Afzelius, 1920; Saˆne´, 1939) or by the only integument (A. distachyos); a micropylar cavity is lacking. A nucellar beak is lacking. The outer integument is unlobed, the inner is lobed (the only integument in A. distachyos is also lobed). The outer integument is semiannular, the inner is annular (the

16

A. IGERSHEIM ET AL.

only integument in A. distachyos is annular-semiannular). The integuments are not convoluted. The outer integument is 4(–5) cell layers thick, the inner is 2 cell layers thick (the single integument in A. distachyos is (5–)6(–8) cell layers thick; see also Sergue´eff, 1907). Cells with oxalate crystals are present in integuments and nucellus in A. ulvaceus, but lacking in A. distachyos. Cells with oxalate druses and raphides, tanniferous tissue, oil cells and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza. BUTOMACEAE (ALISMATALES) (Figs 84–98, 228, 229, 231, 232)

The flowers are bisexual (Cook, 1998a). Carpels (4–)6 (Salisbury, 1926), large, whorled (developing in two successive alternating whorls; Singh & Sattler, 1974; van Heel, 1983), almost free (basally united at the periphery; Serbanescu-Jitariu, 1964), completely plicate (see also van Heel, 1983); ovary almost superior. The floral apex is not completely used up by carpel formation (Gre´goire, 1938). The carpel apex is somewhat extended into two lateral tips (Kaul, 1976). The ovary locule is not dorsally bulged up. The ovules do not fill the locule and are not in close contact with the ovary wall. Septal nectaries are present (Parlatore, 1854; Bo¨hmker, 1917; Daumann, 1970; van Heel, 1988). The stigma extends only around the upper part of the ventral slit. It is pluricellular-uniseriate, papillate, and weakly secretory (Singh, 1966b) (unicellular-papillate, according to Heslop-Harrison & Shivanna, 1977). A style is present. The ventral slit is postgenitally fused along its inner area but unfused along the centre and along the periphery (see also Singh & Sattler, 1974; Kaul, 1976); the carpel is also unfused apically but closed by secretion (angiospermy type 2). The ovarial cavity is not filled with secretion but secretion covers the placentae. Pollen grains were found inside the carpel (Johri & Bhatnagar, 1957). Pollen tube transmitting tissue is one-layered and well differentiated. A compitum is lacking. The carpel surface is glabrous. Stomata are present. Cells with oxalate crystals (but not with druses and raphides) are present. Tanniferous tissue, sclereids, ethereal oil cells, and mucilage cells are absent in the carpel walls (according to Bo¨hmker, 1917, the surface of the ovary is tanniferous). Intercellular cavities are present (Bo¨hmker 1917). Laticifers are absent. Ovules c. 150 per carpel, with distinct funicle, medium, weakly crassinucellar (Vesque, 1878; Ward, 1880; Holmgren, 1913; Nitzschke, 1914; Dahlgren, 1927; Roper, 1952; Krasnikov, 1990; Fernando & Cass, 1996, 1997; bitegmic, anatropous (one or a few orthotropous ovules in a carpel often present), ascendant,

along the length of the locule (Krasnikov, 1990); chalaza unextended; a pronounced funiculus is present; an aril is lacking. Placenta lateral, laminar-diffuse (Payer, 1857; Gre´goire, 1938; Eckardt, 1957; Leinfellner, 1973; van Heel, 1983); ovules lacking in the dorsal region; the ovules appear in acropetal sequence (Buchenau, 1857). Nucellus medium, with a single meiocyte (Roper, 1952; Krasnikov, 1990; Fernando & Cass, 1996, 1997; Holmgren, 1913, reports the occasional occurrence of ovules with several meiocytes). The micropyle is formed by the inner integument (Buchenau, 1857; Ward, 1880; Roper, 1952; Krasnikov, 1990); a micropylar cavity is lacking. A nucellar beak is lacking. The outer integument is unlobed, the inner is lobed. The outer integument is semiannular (annular in the unusual orthotropous ovules), the inner is annular. Both integuments are not convoluted. The outer integument is 2–3 cell layers thick, the inner is 2 cell layers thick. Tanniferous tissue, cells with oxalate crystals/druses/raphides, oil cells and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza. HYDROCHARITACEAE (ALISMATALES) (Figs 99–136, 228, 229, 232)

The flowers are bisexual or unisexual (Cook, 1998b). Rudiments of the opposite gender are present. Carpels commonly 3, often 6, in several genera with a range from 3 to more (Kaul, 1968; Cook, 1998b), 2 in Vallisneria caulescens (McConchie & Kadereit, 1987), up to 20 in Ottelia (Cook, Symoens & Urmi-Ko¨nig, 1984), medium (Hydrocharis) to very large (Elodea, Stratiotes, Vallisneria), whorled. The carpels have been interpreted as free but inserted on an elongated concave floral centre (Troll, 1931); in some genera which flower at the water surface, the upper part of this concave floral centre with the carpels is exceedingly elongated into a ‘neck’, which looks like a long pedicel (e.g. Elodea, Hydrilla), whereas Vallisneria has a normal pedicel. However, in Limnobium and Hydrocharis the carpels are clearly united, to a lesser extent perhaps also in some other genera (Jitariu, 1952; Kaul, 1968; Cook & Lu¨o¨nd, 1982b; Cook & Urmi-Ko¨nig, 1983; Scribailo & Posluszny, 1985). The carpels are either completely plicate (symplicate) (Elodea) or basally ascidiate (synascidiate) (Hydrocharis, Stratiotes). The ovules are commonly in the symplicate zone, more rarely in both the symplicate and synascidiate zone (Hydrocharis and Limnobium). The ovary is inferior. The carpel apex is transversely two-lobed in several genera (Elodea; Cook & Urmi-Ko¨nig, 1985; Enhalus; Troll, 1931; Kausik, 1940b; Hydrocharis; Rohrbach, 1873; this study; Limnobium; Cook & Urmi-Ko¨nig, 1983; Maidenia (McConchie, 1983); Nechamandra; Cook & Lu¨o¨nd, 1982a; Ottelia; Cook et al., 1984; Cook & Urmi-Ko¨nig, 1984b;

GYNOECIUM IN BASAL MONOCOTS

17

Figures 84–93. Butomus umbellatus (Butomaceae), female stage of anthesis. Fig. 84. Gynoecium from the side (arrowheads indicate levels of Figs 88–93). Fig. 85. Stigma and style from ventral side (arrow-head indicates level in Fig. 87). Fig. 86. Part of Fig. 85, showing weakly secretory stigma. Figs 87–93. TS gynoecium or carpel at different levels. Fig. 87. Stigma with uniseriate-pluricellular papillae (arrow-heads). Fig. 88. Below stigma. Fig. 89. Upper ovary region (arrow-heads point to pollen tube transmitting tissue). Fig. 90. Slightly above mid-height of ovary. Fig. 91. Somewhat below Fig. 90 (arrow-heads point to intercellular cavities). Fig. 92. Septal nectaries. Fig. 93. Carpels partly united at periphery. Scale bars: Figs 84, 90, 92=2 mm; Figs 85, 89, 91, 93=1 mm; Figs 86, 88=0.25 mm; Fig. 87=0.05 mm.

Stratiotes; this study; Thalassia; Tomlinson, 1969; Vallisneria; Wylie, 1917; Kausik, 1939; McConchie & Kadereit, 1987; this study). The inner space of each carpel is not dorsally bulged up. The ovules do not fill the

locule and are not in close contact with the ovary wall. Septal nectaries are absent but nectaries are present on staminodes (Daumann, 1931a,c, 1970; Kaul, 1968). The stigma extends only around the upper part of

18

A. IGERSHEIM ET AL.

Figures 94–98. Butomus umbellatus (Butomaceae), female stage of anthesis. Fig. 94. TS ovary with laminar-diffuse placenta. Fig. 95. Part of Fig. 94 with approximately median LS ovule. Fig. 96. One half of a carpel with laminardiffuse placenta. Fig. 97. Part of Fig. 96 with anatropous ovules and an orthotropous ovule. Fig. 98. Ovule from the side (arrow-head points to micropyle). Scale bars: Figs 94, 96=1 mm; Fig. 97=0.5 mm; Fig. 95=0.25 mm; Fig. 98= 0.1 mm.

the ventral slit (Stratiotes). It is unicellular-papillate (weakly secretory in Stratiotes; this study; and in Blyxa; Cook, Lu¨o¨nd & Nair, 1981; dry in Elodea, Hydrocharis, Vallisneria; this study; Thalassia; Heslop-Harrison & Shivanna, 1977; Cox & Tomlinson, 1988; Enhalus, Thalassia, Halophila; Pettitt, 1976, 1980; in the latter three genera not specified whether unicellular), multicellular-multiseriate-papillate in Limnobium (Heslop-Harrison & Shivanna, 1977). Upper ovules in ovary degenerate before maturity (Elodea) (Ernst-Schwarzenbach, 1951). A style is present. The carpels are not postgenitally fused but closed by secretion (angiospermy type 1). Pollen grains were found inside the carpels in Boottia and Ottelia (Islam, 1950; Johri & Bhatnagar, 1957). The locule is partly (Hydrocharis, Stratiotes, Elodea) or completely filled with secretion (Enhalus; Svedelius, 1904; Hydrocharis; Rohrbach, 1873; Scribailo & Posluszny, 1985; Ottelia; Montesantos, 1912; Thalassia; Tomlinson, 1969; Vallisneria; this study). Pollen tube transmitting tissue is one-cell-layered and well differentiated. In the ovary the entire carpel wall is secretory (Elodea, Enhalus, Halophila, Hydrocharis, Ottelia, Thalassia, Vallisneria

etc.; Rohrbach, 1873; Montesantos, 1912; Troll, 1931; Tomlinson, 1969) or there are discrete pads of secretory tissue between the ovules (Boottia; Kaul, 1969; Ottelia; Troll, 1931; Indra & Krishnamurthy, 1982, 1984; Apparao & Shah, 1989). A compitum is present. The carpel surface is glabrous. Stomata are lacking. Tanniferous cells are present in the carpel wall of Hydrocharis, Ottelia and Vallisneria. Cells with oxalate crystals are present in Elodea, Hydrocharis and Vallisneria but absent in Stratiotes. Cells with oxalate druses/raphides, sclereids, and oil cells are absent. Mucilage cells are present in Vallisneria among the four genera here studied. Intercellular cavities are present. Laticifers are lacking. Ovule number per carpel: 1 in Thalassia (Tomlinson, 1969); 1–3 in Egeria, Elodea and Hydrilla (Caspary, 1858b; Baillon, 1878; Kaul, 1968; Cook & Urmi-Ko¨nig, 1984a, 1985); 3 or more in Apalanthe (Cook, 1985); 5–7 in Stratiotes (this study); 45–50 in Hydrocharis (this study); c. 150 in Vallisneria (this study); c. 200 in Bootia (Kaul, 1969); up to 200 or more in Ottelia (Cook & Urmi-Ko¨nig, 1984b); with or without distinct funicle. The ovules are medium (Hydrocharis), large (Elodea,

GYNOECIUM IN BASAL MONOCOTS

19

Figures 99–112. Elodea nuttallii (Hydrocharitaceae), female flower at anthesis. Fig. 99. Flower from above. Figs 100–108. TS gynoecium at different levels. Fig. 100. Stigma, unicellular-papillate. Fig. 101. Apocarpous zone below stigma (level indicated in Fig. 109). Fig. 102. Upper syncarpous, inferior zone (level indicated in Fig. 109). Fig. 103. Region of ‘neck’ (small arrow-head) and spathe (large arrow-head); gynoecium and floral periphery are differentially fused (the three lacunae are unfused areas). Fig. 104. Part of Fig. 103, showing unfused secretory canal in the centre (arrow-head). Fig. 105. Above ovary, central canal enlarging before merging with the locule. Fig. 106. TS ovary and ovule. Fig. 107. TS ovary (arrow-heads point to pollen tube transmitting tissue). Fig. 108. Ovary base (arrow-heads point to pollen tube transmitting tissue). Fig. 109. LS upper part of gynoecium with unfused secretory canal (small arrow-heads); level of Figs 101 and 102 marked by large arrow-heads. Fig. 110. Ovules from the side (arrow-heads point to micropyles). Fig. 111. Ovules from above (arrow-heads point to micropyles). Fig. 112. LS ovules (arrow-head points to pollen tube transmitting tissue; asterisks indicates secretion). Scale bars: Fig. 99=1 mm; Figs 101–103, 107–112=0.25 mm; Figs 100, 104–106=0.1 mm.

20

A. IGERSHEIM ET AL.

Figures 113–120. Hydrocharis morsus-ranae (Hydrocharitaceae, female flower at anthesis. Fig. 113. Flower from above. Fig. 114. LS upper part of gynoecium (arrow-head indicates level in Fig. 115). Figs 115–117. TS gynoecium at different levels. Fig. 115. Upper inferior part (at level indicated by arrow-head in Fig. 114). Fig. 116. Mid-level of ovary. Fig. 117. Lower symplicate zone of ovary. Fig. 118. Laminar–diffuse placenta with orthotropous ovules. Fig. 119. Ovule (arrow-head points to micropyle). Fig. 120. LS ovule (arrow-head points to micropyle). Scale bars: Fig. 113=1 mm; Figs 114, 116, 117=0.5 mm; Figs 115, 118=0.25 mm; Figs 119, 120=0.1 mm.

GYNOECIUM IN BASAL MONOCOTS

21

Figures 121–130. Stratiotes aloides (Hydrocharitaceae), female flower at anthesis. Fig. 121. Upper (superior) part of gynoecium from the side (small arrow-heads point to two-lobed carpel apex; large arrow-head indicates level in Fig. 123). Fig. 122. Stigma, unicellular-papillate. Fig. 123. TS gynoecium (at level indicated in Fig. 121). Fig. 124. TS ovary. Fig. 125. Placenta with two ascendant ovules. Fig. 126. Ovule from the side (arrow-head points to micropyle). Fig. 127. Micropyle, formed by outer integument. Figs 128–130. TS ovule at different levels. Fig. 128. Nucellar region (arrowheads indicate inner integument). Fig. 129. Below micropylar region. Fig. 130. Micropylar region. Scale bars: Fig. 121=5 mm; Figs 123, 124=2.5 mm; Fig. 125=1 mm; Fig. 122=0.5 mm; Figs 126, 128–130=0.25 mm; Fig. 127=0.1 mm.

Vallisneria), or very large (Stratiotes); crassinucellar (Blyxa; Kausik, 1940a; Rangasamy, 1941; Govindappa & Naidu, 1956; Lakshmanan, 1961; Elodea; Fischer, 1880; Wylie, 1904; Halophila; Lakshmanan, 1963a;

Nechamandra, as Lagarosiphon; Padhye & Rao, 1960; Lakshmanan, 1963b); Ottelia, incl. Hydromistria; Tassi, 1900; Palm, 1915; Islam, 1950; Vallisneria; Rangasamy, 1934; Witmer, 1937) or tenuinucellar (Ottelia;

22

A. IGERSHEIM ET AL.

Figures 131–136. Vallisneria americana (Hydrocharitaceae), female flower at anthesis. Fig. 131. LS lower part of inferior ovary, locule filled with secretion. Fig. 132. LS upper part of inferior ovary (star indicates unfused secretory canal above the locule). Fig. 133. LS ovary. Fig. 134. TS ovary, with laminar–diffuse placenta. Fig. 135. TS ovule in micropylar region (arrow-head points to lobed inner integument). Fig. 136. LS orthotropous ovule (asterisk indicates secretion). Scale bars: Figs 131, 132=1 mm; Figs 133, 134=0.5 mm; Figs 135, 136=0.25 mm.

Narasimha Murthy, 1935); bitegmic (unitegmic in Thalassia; Tomlinson, 1969); anatropous in Bootia, Ottelia; Blyxa (Montesantos, 1912; Kausik, 1940a; Rangasamy, 1941; Islam, 1950; Govindappa & Naidu, 1956; Lakshmanan, 1961); Enhalus (Svedelius, 1904); Halophila (Lakshmanan, 1963a); Hydrilla (Maheshwari & Johri, 1950); Stratiotes (Baude; 1956), but orthotropous in Egeria (Cook & Urmi-Ko¨nig, 1984a), Elodea (Caspary, 1858b; Baillon, 1878; Fischer, 1880; Wylie, 1904; Cook & Urmi-Ko¨nig, 1985), Hydrocharis (Rohrbach, 1873), Lagarosiphon (Caspary, 1858a); Limnobium (incl. Hydromistria) (Tassi, 1900; Hunziker, 1982; Cook & Urmi-Ko¨nig, 1983), Nechamandra (Padhye & Rao, 1960; Lakshmanan, 1963b; Cook, 1998b), and Vallisneria (Chatin, 1855; Baillon, 1878; Rangasamy, 1934; Cook, 1998b); ascendant (Hydrocharis, Stratiotes, Elodea; Baillon, 1878; Wylie, 1904; this study) or irregularly directed (Vallisneria); more or less along the length of the ovary (Hydrocharis, Stratiotes, Vallisneria) or basal (Elodea; Baillon, 1878); chalaza unextended; an aril is lacking. The ovary is

commonly unilocular (Apalanthe; Cook, 1985); Egeria (Cook & Urmi-Ko¨nig, 1984a), with or without complete dissepiments (Cook, 1998b), both conditions (unilocular and plurilocular) present in Limnobium (Cook & Urmi-Ko¨nig, 1983). Placentae parietal, in Limnobium laminar-diffuse (Cook & Urmi-Ko¨nig, 1983), with ovules also on the dorsal side, laminar-diffuse also in Hydrocharis, Stratiotes, Vallisneria. Nucellus narrow (Hydrocharis), medium (Vallisneria), or broad (Elodea, Stratiotes); with a single meiocyte (Blyxa; Kausik, 1940a; Rangasamy, 1941; Govindappa & Naidu, 1956; Lakshmanan, 1961; Elodea; Fischer, 1880; Wylie, 1904; Halophila; Lakshmanan, 1963a; Hydrilla; Maheshwari, 1933; Limnobium (as Hydromistria); Tassi, 1900; Nechamandra; Lakshmanan, 1963b; Ottelia; Palm, 1915; Islam, 1950; Vallisneria; Burr, 1903; Rangasamy, 1934), but with 1–3 meiocytes in Hydrilla (Maheshwari, 1933). The micropyle is formed by both integuments (Blyxa; Govindappa & Naidu, 1956; Lakshmanan, 1961; Stratiotes; this study) or by the inner integument (Blyxa; Kausik, 1940a;

GYNOECIUM IN BASAL MONOCOTS

Elodea; this study; Enhalus; Svedelius, 1904; Hydrilla; Maheshwari & Johri, 1950; Hydrocharis; this study; Maidenia; McConchie, 1983; Nechamandra; Lakshmanan, 1963b; Vallisneria, with only short outer integument; Caspary, 1857; Mu¨ller, 1875, 1878; Rangasamy, 1934); in Vallisneria gigantea by the inner or by both integuments); a micropylar cavity is lacking. A nucellar beak is lacking, but in Stratiotes the nucellus apex has a nipple-shaped protuberance. The outer integument is unlobed, but the inner is lobed (Elodea, Hydrocharis, Stratiotes, Vallisneria). The outer integument is (annular-)semiannular (Stratiotes) or annular (Elodea, Hydrocharis, Vallisneria), the inner is annular. Both integuments are not convoluted. In Stratiotes the outer integument is 13–15 cell layers thick and the inner 2–3; in Blyxa 4–5 and 2–3, respectively (Kausik, 1940a; Govindappa & Naidu, 1956; Lakshmanan, 1961); in Elodea 4–5 and 2; in Halophila, Hydrocharis and Vallisneria both integuments 2 cell layers thick (Lakshmanan, 1963a; this study). Tanniferous tissue, cells with oxalate crystals/druses/raphides, oil cells and mucilage cells are lacking in the ovules (in Vallisneria oxalate crystals in integuments). The ovular vascular bundle ends in the chalaza. JUNCAGINACEAE (ALISMATALES) (Figs 137–146, 228, 229, 232)

The flowers are bisexual (in Lilaea bisexual and unisexual, in Tetroncium unisexual; Markgraf, 1936; Posluszny, Charlton & Jain, 1986; Haynes, Les & HolmNielsen, 1998d). In Triglochin carpels (3–)6(–8), small, in two whorls (Horn, 1875, 1876; Uhl, 1947; Eckardt, 1957; Singh, 1973) (in Triglochin palustris and T. striata only those of the inner whorl well developed and fertile, the outer ones solid and sterile; de Cordemoy, 1862; Hill, 1900; Eber, 1934; Uhl, 1947; Serbanescu-Jitariu, 1973a; Lieu, 1979). Tetroncium and Maundia have 4 carpels, Lilaea 1 carpel (Haynes et al., 1998d). In Triglochin the carpels originate as separate organs, but they are ‘united’ via the large-celled, undifferentiated floral centre (Eber, 1934; Singh, 1973; Lieu, 1979). Thus they may be seen as apocarpous (and largely plicate) with extremely oblique bases or as syncarpous of an unspecialized type (and largely synascidiate). In young stages they are pronouncedly ascidiate (Eckardt, 1957). In Lilaea the carpel is ascidiate (Posluszny et al., 1986). The ovary is superior. The carpel apex is not extended into two lateral tips. The locule is not dorsally bulged up. The ovule does not fill the locule but is laterally in contact with the ovary wall. Septal nectaries are lacking (see also Daumann, 1970). The stigma extends completely around the ventral slit. It is unicellular-papillate and dry (see also HeslopHarrison & Shivanna, 1977). A style is absent. The

23

ventral slit and the short canal in the uppermost ascidiate zone are postgenitally fused (angiospermy type 4). Pollen tube transmitting tissue is well differentiated and 1-layered. Secretion in the locules was not found. A compitum is lacking. However, since the stigmatic hairs are contiguous between carpels, pollen tubes may be able to grow here from one carpel to another. The carpel surface is glabrous. Stomata are present. Cells with oxalate druses/crystals/raphides, tanniferous tissue, sclereids, ethereal oil cells, and mucilage cells are all absent from the carpel wall. Intercellular cavities are present. Laticifers are present in Triglochin (also at least in the vegetative organs of Lilaea; Tomlinson, 1982). Ovule 1 per carpel, large, crassinucellar (Vesque, 1879; Fischer, 1880; Campbell, 1898; Agrawal, 1952; Tomlinson, 1982; Nikiticheva & Proskurina, 1990), bitegmic, anatropous (Hofmeister, 1861; de Cordemoy, 1862; Campbell, 1898; Hill, 1900; Eber, 1934; Agrawal, 1952; Nikiticheva & Proskurina, 1990) (but orthotropous in Maundia, Tomlinson, 1982), ascendant, basal (Campbell, 1898; Singh, 1965d, 1973) (but apical and pendant in Maundia, Aston, 1973); chalaza unextended; an aril is lacking. Placenta in the (syn) ascidiate zone, median. Nucellus medium, with a single meiocyte (Campbell, 1898; Agrawal, 1952; Nikiticheva & Proskurina, 1990) (an ovule with two collateral embryo sacs for Triglochin figured by Fischer, 1880). The micropyle is formed by the inner integument (Nikiticheva & Proskurina, 1990). A micropylar cavity is lacking. A nucellar beak is lacking. Both integuments are unlobed. The outer integument is semiannular, the inner is annular. Both integuments are not convoluted. The outer integument is (3–)4–5 cell layers thick, the inner is 2 cell layers thick. Cells with oxalate druses/ crystals/raphides, tanniferous tissue, oil cells and mucilage cells are lacking in the ovules. As a special feature the outer integument has intercellular cavities. The ovular vascular bundle ends in the chalaza.

LIMNOCHARITACEAE (ALISMATALES) (Figs 147–157, 228, 230–232)

The flowers are bisexual (Haynes, Les & Holm-Nielsen, 1998e). Carpels 3–20 (Haynes et al., 1998e), in Hydrocleys medium, whorled, largely free, largely plicate (basally ascidiate and synascidiate); in Limnocharis free, plicate (if interpreted as obliquely inserted; cf. Troll, 1932; Kaul, 1967b) or syncarpous, synascidiate (if not interpreted as obliquely inserted); ovary superior. The carpel apex is somewhat extended into two lateral tips (Juhnke & Winkler, 1938; Kaul, 1976). The locule is not dorsally bulged up. The ovules do not fill the locule and are not in close contact with the

24

A. IGERSHEIM ET AL.

Figures 137–146. Triglochin maritima (Juncaginaceae), female stage of anthesis. Fig. 137. Gynoecium from the side. Fig. 138. Carpel surface with stomata. Figs 139–142. TS carpel at different levels. Fig. 139. Stigma. Fig. 140. Lower end of stigma with postgenitally fused ventral slit (arrow-head). Fig. 141. Ascidiate part of style with postgenitally fused ventral slit (arrow-head). Fig. 142. Upper part of ovary (arrow-head points to pollen tube transmitting tissue). Fig. 143. TS gynoecium at level of ovary. Fig. 144. Ovule from the side (arrow-head points to micropyle). Fig. 145. Micropyle and placental hairs (arrow-heads). Fig. 146. Median LS ovule (arrow-head points to micropyle). Scale bars: Figs 137, 143=1 mm; Figs 139–142=0.25 mm; Figs 138, 144–146=0.1 mm.

ovary wall. Septal nectaries are present (at the base) (see also Daumann, 1970). The stigma extends only around the upper part of the ventral slit. It is unicellular papillate and weakly secretory. A style is present. The carpel is postgenitally fused along the periphery of the ventral slit but unfused along the centre and apically closed by secretion (angiospermy type 2). The locule is not filled with secretion. Pollen grains were reported inside carpels in Butomopsis and Limnocharis (Johri, 1935a, 1936b;

Sahni & Johri, 1936; Johri & Bhatnagar, 1957). Pollen tube transmitting tissue is one-layered and well differentiated. A compitum is lacking. The carpel surface is glabrous. Stomata are present. Cells with oxalate crystals are present in the carpel wall. Cells with oxalate druses/raphides, tanniferous tissue, sclereids, ethereal oil cells, and mucilage cells are lacking. Intercellular cavities are present. Laticifers are present (see also Nayar & Sworupanandan, 1978). Ovules in Hydrocleys c. 110–130 per carpel (in Lim-

GYNOECIUM IN BASAL MONOCOTS

25

Figures 147–157. Hydrocleys nymphoides (Limnocharitaceae), female stage of anthesis. Fig. 147. Gynoecium from the side. Fig. 148. Stigmatic region (arrow-heads point to secretion). Fig. 149. Basal adaxial side of carpels (arrowhead points to ventral slit). Figs 150–154. TS carpel and gynoecium at different levels. Fig. 150. Stigma, unicellularpapillate (arrow-head points to secretion). Fig. 151. Style (arrow-heads point to laticifers). Fig. 152. Upper ovary region (arrow-heads point to intercellular cavities). Fig. 153. Transition between plicate and ascidiate zone (arrow-heads). Fig. 154. Septal nectary (arrow-head). Fig. 155. Laminar diffuse placenta with ovules. Fig. 156. Ovule from the side. Fig. 157. Median LS ovule (small arrow-heads indicate inner integument; large arrow-head points to micropyle). Scale bars: Fig. 147=2.5 mm; Fig. 148=1 mm; Fig. 149=0.5 mm; Figs 150–155=0.25 mm; Figs 156, 157=0.1 mm.

26

A. IGERSHEIM ET AL.

nocharis more than 60, according to a figure in Nayar & Sworupanandan, 1978), with distinct funicle, medium, pseudocrassinucellar (by periclinal division of all or part of the epidermal cells above the meiocyte) or tenuinucellar (Hall, 1902; Nitzschke, 1914; Johri, 1936b, 1938a,b); bitegmic, anatropous to (slightly) campylotropous; ascendant (see also Sattler & Singh, 1973; Serbanescu-Jitariu, 1973b), along the length of the locule in the plicate zone; chalaza unextended; an aril is lacking. Placenta lateral, laminar-diffuse (Troll, 1932; Nayar & Sworupanandan, 1978); ovules lacking in the dorsal region. Nucellus narrow, with a single meiocyte (Hall, 1902; Suessenguth, 1921; Johri, 1936b, 1938a,b). The micropyle is formed by the inner integument (Hall, 1902); a micropylar cavity is absent. A nucellar beak is lacking. Both integuments are unlobed. The outer integument is semiannular, the inner is annular. Both integuments are not convoluted. Both integuments are 2 cell layers thick (see also Hall, 1902; Johri, 1938a, for Limnocharis; Johri, 1938b, for Hydrocleys; Johri, 1936b, for Butomopsis). Tanniferous tissue, cells with oxalate crystals/druses/raphides, oil cells, and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza.

cells, and mucilage cells are lacking. Intercellular cavities are present. Laticifers are absent. Ovule 1 per carpel, medium, crassinucellar (Wiegand, 1898, 1900; Holferty, 1901; Gupta, 1934; Takaso & Bouman, 1984; Kamelina, 1990), bitegmic (also Lakshmanan, 1968), at first orthotropous, at anthesis campylotropous (Hofmeister, 1861; Cook, 1908; Gupta, 1934; Serbanescu-Jitariu, 1972b; Takaso & Bouman, 1984; Teryokhin, Chubarov & Romanova, 1997), pendant, more or less apical; chalaza unextended; an aril is lacking. Placenta in the ascidiate zone, median. Nucellus broad (P. alpinus) or medium (Groenlandia), with a single meiocyte (Holferty, 1901; Gupta, 1934; Takaso & Bouman, 1984). The micropyle is formed by the inner integument (Gupta, 1934; Takaso & Bouman, 1984; Teryokhin et al., 1997). A micropylar cavity is lacking. A nucellar beak is lacking. The outer integument is unlobed, the inner is lobed. Both integuments are annular. Both integuments are not convoluted. The outer integument is (2–)3(–4) cell layers thick (Groenlandia) or only 2 cell layers (P. alpinus; this study; P. crispus; Gupta, 1934), the inner integument is 2 cell layers thick. Cells with oxalate crystals/druses/raphides, tanniferous tissue, oil cells, and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza.

POTAMOGETONACEAE (ALISMATALES) (Figs 158–176, 228, 230, 232)

SCHEUCHZERIACEAE (ALISMATALES)

The flowers are bisexual (Haynes, Les & Holm-Nielsen, 1998f). Carpels 4 (in Potamogeton trichoides and P. zosteriformis 1 terminal carpel; Helm, 1934; Posluszny, 1981; in P. compressus often 1–2; in P. lucens 4–6; in some species variable according to the position in the inflorescence; Charlton & Posluszny, 1991), small, whorled, free, almost completely ascidiate (see also Hegelmaier, 1870; Sprotte, 1940; Posluszny & Sattler, 1973, 1974a; Takaso & Bouman, 1984); locule dorsally somewhat bulged up; ovary superior. The carpel apex is slightly extended into two lateral tips (see also Posluszny & Sattler, 1974a). The ovule fills the locule. Septal nectaries are lacking. The stigma extends completely around the ventral slit. It is unicellular-papillate and seemingly strongly secretory (Potamogeton alpinus) or smooth and dry or weakly secretory (Groenlandia) (according to HeslopHarrison & Shivanna, 1977, also Potamogeton). A style is present (Groenlandia) or absent (P. alpinus). The (very short) ventral slit is partly unfused, but the long, thin canal in the ascidiate zone is postgenitally fused (angiospermy type 4). In the locule secretion was not found. Pollen tube transmitting tissue is one-layered and only weakly differentiated. A compitum is lacking. The carpel surface is glabrous. Stomata are absent. Tanniferous tissue is present in the ovary wall. Cells with oxalate crystals/druses/raphides, sclereids, oil

The flowers are bisexual (Haynes, Les & Holm-Nielsen, 1998g). Carpels 3–4(–6) (Haynes et al., 1998g), small, whorled, largely free (if viewed as obliquely inserted), basally for a short distance united via the flanks (Eames, 1931; Eber, 1934; Serbanescu-Jitariu, 1966), completely plicate; ovary superior. The carpel apex is slightly extended into two lateral tips (see also Posluszny, 1983). The locule is not dorsally bulged up. The ovules do not fill the locule and are not in close contact with the ovary wall. Septal nectaries seem to be absent; although the carpel flanks form narrow slits at the ovary base, the epidermis is not differentiated as otherwise in septal nectaries. The stigma extends around the upper part of the ventral slit and above the ventral slit and far down the median dorsal line. It is unicellular-papillate and weakly secretory (dry after Heslop-Harrison & Shivanna, 1977). A style is not present. The inner surface of the carpels is postgenitally fused along the periphery, but an unfused canal, lined with papillae and filled with secretion, discharges into the stigmatic area (angiospermy type 2). The locule is not filled with secretion. Pollen tube transmitting tissue is one-layered and clearly differentiated. A compitum is lacking. The carpel surface is glabrous. Stomata are present. Cells with oxalate crystals are present in the ovary

(Figs 177–186, 228, 230, 232)

GYNOECIUM IN BASAL MONOCOTS

27

Figures 158–166. Groenlandia densa (Potamogetonaceae), female stage of anthesis. Fig. 158. Carpel from the side (adaxial side at right). Fig. 159. Carpel from above (adaxial side at right). Figs 160–164. TS gynoecium and carpels at different levels. Fig. 160. Stigma and below (arrow-head points to secretion). Fig. 161. Ascidiate styles (arrow-heads point to postgenitally fused ventral slits). Fig. 162. Ascidiate style in higher magnification (arrow-head points to postgenitally fused ventral slit). Fig. 163. Ovaries. Fig. 164. TS ovary with TS ovule at nucellar level (arrow-heads indicate inner integument). Fig. 165. Median LS ovule (arrow-head points to micropyle). Fig. 166. Micropylar region of ovule with lobed inner integument. Scale bars: Figs 158, 163=0.5 mm; Figs 160, 161, 164=0.25 mm; Figs 159, 162, 165=0.1 mm; Fig. 166=0.05 mm.

wall. Cells with oxalate druses/raphides, tanniferous tissue, sclereids, ethereal oil cells and mucilage cells are lacking. Intercellular cavities are lacking. Laticifers are lacking. Ovules 2 per carpel (mostly only 1 developing into seed; Serbanescu-Jitariu, 1966), medium, crassinucellar (Stenar, 1935; Nikiticheva, 1990b; Nikiticheva & Proskurina, 1992), bitegmic, anatropous, horizontal or slightly ascendant, in the lower part of the locule; chalaza unextended; an aril is lacking. Placenta in the plicate zone, lateral, linear. Nucellus narrow, number of meiocytes not recorded. The micropyle is formed by the inner integument (Stenar,

1935; Nikiticheva, 1990b; Nikiticheva & Proskurina, 1992); a micropylar cavity is lacking. A nucellar beak is lacking. The outer integument is unlobed, the inner is lobed. The outer integument is semiannular, the inner is annular. Both integuments are not convoluted. The outer integument is 5–6 cell layers thick, the inner is 4 cell layers thick. Tanniferous tissue, cells with oxalate crystals/druses/raphides, ethereal oil cells, and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza (according to Nikiticheva, 1990b, and Nikiticheva & Proskurina, 1992, a strand extends into the base of the outer integument after anthesis).

28

A. IGERSHEIM ET AL.

Figures 167–176. Potamogeton alpinus (Potamogetonaceae), female stage of anthesis. Fig. 167. Gynoecium from above (arrow-head points to ventral slit). Fig. 168. Carpel from the side (adaxial side at right). Fig. 169. Carpel from adaxial side (arrow-head points to ventral slit). Fig. 170. Part of Fig. 169, showing unicellular-papillate stigma. Figs 171–173. TS gynoecium or carpel at different levels. Fig. 171. Stigmas (arrow-heads point to ventral slits). Fig. 172. Ascidiate style (arrow-head points to postgenitally fused ventral slit). Fig. 173. Ovaries. Fig. 174. Ovule from the side (arrowhead points to micropyle). Fig. 175. Median LS ovule (arrow-head points to micropyle). Fig. 176. Micropylar region of ovule with lobed inner integument. Scale bars: Figs 167–169=0.5 mm; Figs 171, 173=0.25 mm; Figs 170, 172, 174–176=0.1 mm.

TOFIELDIACEAE (ALISMATALES) (Figs 187–196, 228, 230–232)

The flowers are bisexual (Tamura, 1998). Carpels 3, small to medium, syncarpous at the base (along a very short length), and partially postgenitally united in the apocarpous zone (Baum, 1948; El-Hamidi, 1952; Leinfellner, 1962, 1969; Eie, 1972; Utech, 1978), stipitate, largely plicate (ascidiate below the placenta)

(Leinfellner, 1969), (ovules on plicate part); ovary superior. The carpel apex is not extended into two lateral tips. The locule is not dorsally bulged up. The ovules do not fill the locule and are not in close contact with the ovary wall. Nectaries are present at the base of the carpels in the same position as septal nectaries in taxa with syncarpous gynoecia (see also SchniewindThies, 1897; Daumann, 1970; Sterling, 1979; van Heel, 1988).

GYNOECIUM IN BASAL MONOCOTS

29

Figures 177–186. Scheuchzeria palustris (Scheuchzeriaceae), female stage of anthesis. Fig. 177. Gynoecium from the side. Fig. 178. Gynoecium from above (arrow-heads point to ventral slits). Fig. 179. Stigma. Figs 180–183. TS Carpel and gynoecium at different levels. Fig. 180. Stigma, unicellular-papillate. Fig. 181. Ovary above placentae (arrow-head points to pollen tube transmitting tissue). Fig. 182. Ovary in placental region. Fig. 183. Placenta with approximate median LS ovule (arrow-head points to united carpels). Fig. 184. Ovules (arrow-heads point to pollen tube transmitting tissue). Fig. 185. Ovule from the side. Fig. 186. Micropylar region of ovule. Scale bars: Figs 177, 182=1 mm; Fig. 178= 0.5 mm; Figs 179–181, 183, 184=0.25 mm; Figs 185, 186=0.1 mm.

The stigma extends around the upper part of and above the ventral slit. It is unicellular-papillate and weakly secretory. A style is present. The ventral slit is postgenitally fused at the periphery but unfused

and forming a canal in the centre, which contains secretion; the canal is fused for a short zone at the apex (angiospermy type 3). In Tofieldia pusilla the zone where the three carpels are postgenitally united,

30

A. IGERSHEIM ET AL.

Figures 187–196. Tofieldia calyculata (Tofieldiaceae), female stage of anthesis. Fig. 187. Gynoecium from the side. Fig. 188. Gynoecium from above. Fig. 189. Stigma, unicellular-papillate (arrow-head points to ventral slit). Fig. 190. LS style and stigma at right angle to median plane (arrow-head indicates level in Fig. 191). Figs 191–196. TS carpel and gynoecium at different levels. Fig. 191. Lower part of stigma. Fig. 192. Style (arrow-head points to unfused secretory canal). Fig. 193. Ovary with anatropous ovules. Fig. 194. Ovary (arrow-head points to postgenitally fused ventral slits and postgenitally united flanks of adjacent carpels). Fig. 195. Ascidiate zone of carpels below placentae. Fig. 196. Ovary base and septal nectaries (arrow-heads). Scale bars: Fig. 187=1 mm; Figs 188, 192–196=0.25 mm; Figs 189–191=0.1 mm.

GYNOECIUM IN BASAL MONOCOTS

i.e. the ovary, the ventral slits are widely gaping (Eie, 1972), whereas in T. calyculata the ventral slits are postgenitally fused also in the ovary. The locule is not filled with secretion. Pollen tube transmitting tissue is one-layered and well differentiated. A compitum may be present in the postgenitally united zone of the gynoecium. The carpel surface is glabrous. Stomata were not found. Cells with oxalate druses and crystals are present in the carpel wall (cf. also Sterling, 1979). Cells with oxalate raphides, tanniferous tissue, sclereids, ethereal oil cells and mucilage cells are lacking. Intercellular cavities are present. Laticifers are lacking. Ovules c. 20–24 per carpel, medium, weakly crassinucellar (Seelieb, 1924; Sokolowska-Kulczycka, 1980, describes it as tenuinucellar, but her figures are not clear), bitegmic (two of 16 species studied from herbarium material unitegmic, according to Sterling, 1979), anatropous (campylotropous in some species; Sterling, 1979), horizontal, along the length of the locule; chalaza unextended (extended into a hook in a few species; Sterling, 1979); an aril is lacking. Placenta in the plicate zone, lateral, linear. Nucellus narrow, with a single meiocyte (Seelieb, 1924). The micropyle is formed by both integuments (see also Seelieb, 1924); a micropylar cavity is lacking. A nucellar beak is lacking. The outer integument is unlobed, the inner is lobed. The outer integument is semiannular, the inner is annular. Both integuments are not convoluted. Both integuments are 2 cell layers thick (see also Seelieb, 1924). Tanniferous tissue, cells with oxalate crystals/ druses/raphides, ethereal oil cells, and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza.

FAMILIES OF ALISMATALES WITH ONLY OR PREDOMINANTLY UNDERWATER FLOWERS AND UNDERWATER POLLINATION (CYMODOCEACEAE,

NAJADACEAE, POSIDONIACEAE, RUPPIACEAE, ZANNICHELLIACEAE, ZOSTERACEAE)

The flowers are unisexual in Cymodoceaceae (Kuo & McComb, 1998a), Najadaceae (Haynes, Holm-Nielsen & Les, 1998a), Zannichelliaceae (Haynes, Les & HolmNielsen, 1998h), and Zosteraceae (Kuo & McComb, 1998c; but Zostera interpreted as having bisexual flowers by Markgraf, 1936); bisexual only in Posidoniaceae (Kuo & McComb, 1998b) and Ruppiaceae (Haynes, Holm-Nielsen & Les, 1998b). Carpel number per flower is 1 (but 1–8 in Zannichelliaceae; 2 in Cymnodoceaceae; (2–)4(–16) in Ruppiaceae). In gynoecia with more than one carpel, the carpels are free. It has also been suggested that in genera with more than one carpel, each carpel represents a separate flower (e.g. Campbell, 1897). This question of flower delimitation is unsettled (Posluszny & Tomlinson,

31

1977). The carpels are strongly ascidiate (Najas; our own observations; Ruppia; Graves, 1908; Posluszny & Sattler, 1974b; Kaul, 1993; Lacroix & Kemp, 1997; Phyllospadix; Soros-Pottruff & Posluszny, 1994; Zannichelliaceae; Posluszny & Sattler, 1976a; Posluszny & Tomlinson, 1977; Zostera; de Lanessan, 1875). Septal nectaries are lacking. In several groups the stigma has two lateral lobes, sometimes three lobes (Cymodocea; Bornet, 1864; Heterozostera; Soros-Pottruff & Posluszny, 1995; Najas; Magnus, 1870; Campbell, 1897; Swamy & Lakshmanan, 1962; Phyllospadix; Soros-Pottruff & Posluszny, 1994; Syringodium; Tomlinson & Posluszny, 1978; Cox, Elmqvist & Tomlinson, 1990; Zostera; De Cock, 1980; Posidonia (whether lateral?); McConchie & Knox, 1989); Thalassodendron (Kuo & Kirkman, 1987); (see also Markgraf, 1936); the stigma has several branches in Amphibolis (Ducker & Knox, 1976; McConchie, Ducker & Knox, 1982; Pettitt et al., 1983). Gue´guen (1901) describes the three branches of Najas as u-shaped in transverse section, which could indicate the presence of three carpels. The stigma is not branched but funnel-shaped in Ruppia (Lacroix & Kemp, 1997) and commonly in Zannichelliaceae (Posluszny & Tomlinson, 1977). Ruppia has a collar around the stigma (‘indusiate stigma’) (Hofmeister, 1852; Murbeck, 1902; Gamerro, 1968; Posluszny & Sattler, 1974b; Cox & Knox, 1989); the collar is thought to prevent water contact of the stigma in this water surface-pollinated plant (Cox & Knox, 1989). The stigma is papillate in Najas (Swamy & Lakshmanan, 1962) and Lepilaena (Posluszny & Tomlinson, 1977); feathery but non-papillate in Phyllospadix (Soros-Pottruff & Posluszny, 1994); it is non-papillate in Syringodium (Cox et al., 1990), Thalassodendron (Pettitt, 1976; Heslop-Harrison & Shivanna, 1977; Cox, 1991), Posidonia (Pettitt, 1984; McConchie & Knox, 1989), Amphibolis (Ducker & Knox, 1976; Heslop-Harrison & Shivanna, 1977; Ducker, Pettitt & Knox, 1978; Pettitt, Ducker & Knox, 1981; Pettitt et al., 1980, 1983), Heterozostera (Pettitt et al., 1983), Zostera (De Cock, 1980; Pettitt et al., 1983). A style is commonly present. Intracarpellary fusion in these families has not been reported in the literature. In Najas the stylar canal seems not to be fused (Gue´guen, 1901). There are only a few reports on the structure of the pollen tube transmitting tract. In Najas papillae or hairs are present on the placenta and inner orifice of the stylar canal (Campbell, 1897; Guignard, 1901; Swamy & Lakshmanan, 1962; Singh 1965b), which fill the entire locule with mucilage by holocrine secretion (Vijayaraghavan & Kapoor, 1980). As the gynoecia are consistently apocarpous, a compitum is lacking. The carpel surface is glabrous. The ovary wall is only two cell layers thick in Najas (Campbell, 1897; Guignard, 1901; Swamy & Lakshmanan, 1962),

32

A. IGERSHEIM ET AL.

whereas the wall of the style is more cell layers thick (Campbell, 1897). Laticifers have not been reported. Each carpel has only one ovule in all six families. The ovule is apical, pendant (Althenia; Prillieux, 1864; our own observations; Cymodocea; Bornet, 1864; Ruppia; Gamerro, 1968; Kamelina & Teryokhin, 1990a; Syringodium; Tomlinson & Posluszny, 1978; Zannichellia; Campbell, 1897; Serbanescu-Jitariu, 1972a; Vijayaraghavan & Kumari, 1974; Kamelina & Teryokhin, 1990b), or basal, ascendant (Najas; Magnus, 1870; Guignard, 1901; Swamy & Lakshmanan, 1962; Singh, 1965b; Serbanesu-Jitariu, 1986; Zostera; Dahlgren, 1939). The ovules are orthotropous in Althenia (Prillieux, 1864; Teryokhin & Chubarov, 1991), Cymodocea; Bornet, 1864; Ruppia (slightly campylotropous at embryo sac maturity or later; Hofmeister, 1852, 1861; Murbeck, 1902; Graves, 1908; Gamerro, 1968; Kamelina & Teryokhin, 1990a), Zannichellia (Campbell, 1897; Vijayaraghavan & Kumari, 1974, erroneously stated as anatropous in the text by the latter authors; Kamelina & Teryokhin, 1990b), and Zostera (Hofmeister, 1852; de Lanessan, 1875; Dahlgren, 1939; Serbanescu-Jitariu, 1974b); the ovules are anatropous in Najas (Hofmeister, 1861; Magnus, 1870; Campbell, 1897; Guignard, 1901; Swamy & Lakshmanan, 1962; Posluszny & Sattler, 1976b; Serbanescu-Jitariu, 1986) and Syringodium (Lakshmanan & Rajeshwari, 1979). The ovules are bitegmic (Althenia; Prillieux, 1864; Teryokhin & Chubarov, 1991; Cymodocea; Bornet, 1864; Najas; Campbell, 1897; Guignard, 1901; Swamy & Lakshmanan, 1962; Ruppia; Murbeck, 1902; Graves, 1908; Posluszny & Sattler, 1974b, 1976b; Serbanescu-Jitariu, 1974b; Kamelina & Teryokhin, 1990a; Syringodium; Lakshmanan & Rajeshwari, 1979; Zannichellia; Campbell, 1897; Serbanescu-Jitariu, 1972a; Vijayaraghavan & Kumari, 1974; Posluszny & Sattler, 1976a; Kamelina & Teryokhin, 1990b; Zostera; de Lanessan, 1875; Serbanescu-Jitariu, 1974b). The ovules are weakly crassinucellar in Ruppia (Murbeck, 1902; Graves, 1908; Kamelina & Teryokhin, 1990a), Najas (Campbell, 1897; Swamy & Lakshmanan, 1962), Syringodium (whether weakly?) (Lakshmanan & Rajeshwari, 1979), and Zannichellia (Campbell, 1897; Vijayaraghavan & Kumari, 1974; Kamelina & Teryokhin, 1990b), but pseudocrassinucellar in Zostera (Rosenberg, 1901; Dahlgren, 1939). A single meiocyte is formed in Najas (Campbell, 1897; Swamy & Lakshmanan, 1962) and Ruppia (Murbeck, 1902; Graves, 1908; but occasionally two meiocytes were found; Murbeck, 1902; Graves, 1908). The micropyle is formed by the inner integument (Althenia; Teryokhin & Chubarov, 1991; Cymodocea; Bornet, 1864; Najas; Campbell, 1897; Swamy & Lakshmanan, 1962; Syringodium; Lakshmanan & Rajeshwari, 1979; Zannichellia; Campbell, 1897; Zostera; Hofmeister, 1852; de Lanessan, 1875; Dahlgren, 1939;

Serbanescu-Jitariu, 1974b); or by both integuments (Ruppia; Murbeck, 1902; Serbanescu-Jitariu, 1974b). The chalaza is thick in Zostera (Hofmeister, 1852; Dahlgren, 1939). The embryo sac touches the inner integument at maturity in Zostera (Hofmeister, 1852). A postament was reported from Zostera (Hofmeister, 1852; Dahlgren, 1939). Integument thickness in cell layers: outer 2, inner 2 (Ruppia; Murbeck, 1902; Zannichellia; Campbell, 1897; Vijayaraghavan & Kumari, 1974); outer 3, inner 2 (Najas, Swamy & Lakshmanan, 1962); outer c. 7, inner 2 (Zostera; Dahlgren, 1939). The ovular vascular bundle ends in the chalaza (Zannichellia; Campbell, 1897). TRIURIDACEAE (INCL. LACANDONIACEAE) (INCERTAE SEDIS IN MONOCOTS) (Figs 197–199, 228, 230)

The flowers are bisexual or unisexual (Maas-van de Kamer & Weustenfeld, 1998), rudiments of the opposite gender may be present (Wirz, 1910). Carpels 6–50 (Ru¨bsamen-Weustenfeld, 1991), 60–80 in Lacandonia (Martı´nez & Ramos, 1989), small, whorled or irregular if numerous (Ru¨bsamen-Weustenfeld, 1991), free, largely plicate (clearly ascidiate in early development); dorsally pronouncedly bulged up so that the outlet of the locule on the ventral side is restricted to a very short zone near the base of the carpel (Poulsen, 1906; Ru¨bsamen-Weustenfeld, 1991); ovary superior. The carpel apex is not extended into two lateral tips. The ovule fills the locule. Septal nectaries are lacking (but tepal nectaries are present) (Ru¨bsamen-Weustenfeld, 1991; Endress, 1995). The stigma is minute, at least in some taxa papillate (Poulsen, 1906; Ru¨bsamen-Weustenfeld, 1991), dry(?). The style is thin and solid, terete, without a ventral slit. In the slightly preanthetic flowers at our disposal the carpel flanks in the outlet area are contiguous but apparently not postgenitally fused. It is not known which angiospermy type is present at anthesis. The locule is not filled with secretion in the preanthetic stage available. A distinct pollen tube transmitting tract is not differentiated before anthesis in our material and seems to be lacking also at anthesis (Ru¨bsamen-Weustenfeld, 1991). The carpel surface is glabrous. Stomata are lacking. Cells with oxalate crystals/druses/raphides, tanniferous tissue, sclereids, oil cells and mucilage cells, and laticifers are lacking. Intercellular cavities are present. Ovule 1 per carpel, small to medium (Ru¨bsamenWeustenfeld, 1991), tenuinucellar, bitegmic, anatropous (Poulsen, 1906; Wirz, 1910; Ma´rquez-Guzma´n et al., 1989; Ru¨bsamen-Weustenfeld, 1991; Va´zquezSantana et al., 1998), ascendant, basal; chalaza unextended; an aril is lacking. Placentation median. Nucellus narrow, with a single meiocyte (Poulsen, 1906;

GYNOECIUM IN BASAL MONOCOTS

33

Figures 197–199. Sciaphila albescens (Triuridaceae), female flower. Fig. 197. Preanthetic flower, gynoecium from the side. Fig. 198. Anthetic flower, carpels from above. Fig. 199. Postanthetic flower, carpel from the side. Scale bars: Figs 197, 199=0.25 mm; Fig. 198=0.1 mm.

Wirz, 1910; Ru¨bsamen-Weustenfeld, 1991; Va´zquezSantana et al., 1998). The micropyle is formed by the inner integument (Wirz, 1910; Ma´rquez-Guzma´n et al., 1989; Ru¨bsamen-Weustenfeld, 1991). A micropylar cavity is absent. A nucellar beak is lacking. Both integuments are unlobed. The outer integument is semiannular, the inner is annular. Both integuments are not convoluted. Both integuments are two celllayers thick (Ru¨bsamen-Weustenfeld, 1991). Tanniferous tissue, cells with oxalate crystals/druses/raphides, oil cells and mucilage cells are lacking in the ovule. The ovular vascular bundle ends in the chalaza. DIOSCOREACEAE (DIOSCOREALES) (Figs 200–216, 228, 230, 232)

The flowers are commonly unisexual, but bisexual in Stenomeris (Burkill, 1960; Huber, 1998a). Carpels 3, medium, whorled, syncarpous (in the superior part only postgenitally united), plicate and symplicate (synascidiate zone extremely short); ovary inferior. The carpel apex is extended into two lateral tips (see also Al-Shehbaz & Schubert, 1989; Huber, 1998a). The locules are not dorsally bulged up. The ovules do not completely fill the locule but they are in contact with the ovary wall. Septal nectaries are present (see also Daumann, 1970). The stigma extends only around the upper part of the ventral slit. It is smooth and strongly secretory (also Heslop-Harrison & Shivanna, 1977). A style is present. In the apocarpous part the ventral slits are postgenitally fused at the periphery, but there is a completely unfused canal filled with secretion (angiospermy type 2); downwards follows a region where the carpels are postgenitally united, but intracarpellary fusion is completely lacking; in the inferior part the carpels become again postgenitally fused along the ovuliferous region. The gynoecium is not postgenitally fused along the ventral slits of the carpels but closed by secretion. The ovarial cavity is filled

with secretion. Pollen tube transmitting tissue is onelayered and well differentiated. A compitum is present. The carpel surface is glabrous. Stomata are lacking. Cells with oxalate crystals and raphides and mucilage cells are present. Cells with oxalate druses, sclereids, tanniferous tissue, oil cells, and laticifers are lacking. Intercellular cavities are lacking in the carpel walls. Ovules 2 per carpel (numerous in Stenomeris; Burkill, 1960; Huber, 1998a), large, crassinucellar, bitegmic, anatropous (see also Rao, 1953; Takeuchi & Kimura, 1968; Takeuchi, 1971, 1972), pendant (or one of the two ascendant; Takeuchi, 1972), one above the other (Takeuchi & Kimura, 1968; Takeuchi, 1971, 1972); chalaza unextended; an aril is lacking. Placenta in the symplicate zone, lateral, linear. Nucellus medium, with a single meiocyte (Rao, 1953; Takeuchi & Kimura, 1968; Takeuchi, 1971, 1972). The micropyle is formed by both integuments (see also Takeuchi & Kimura, 1968); a micropylar cavity is lacking. A nucellar beak is lacking. The outer integument is unlobed, the inner is lobed. The outer integument is (annular to) semiannular, the inner is annular. The integuments are not convoluted. The outer integument is 4–5 cell layers thick, the inner is 2 cell layers thick. Cells with oxalate crystals/druses/raphides, tanniferous tissue, oil cells and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza. TACCACEAE (DIOSCOREALES) (Figs 217–228, 230–232)

The flowers are bisexual (Kubitzki, 1998a). Carpels 3, large, syncarpous, completely (sym-)plicate (without a synascidiate base); ovary inferior. The carpel apex is extended into two lateral tips. The inner surface of each carpel is not dorsally bulged up. The ovules do not fill the locule and are not in close contact with the locule wall. Septal nectaries seem to be lacking (see also Daumann, 1970; according to Daumann, Brown (1938) erroneously adscribed septal nectaries to Tacca).

34

A. IGERSHEIM ET AL.

Figures 200–212. Tamus communis (Dioscoreaceae), female flower at anthesis. Fig. 200. Flower from above. Fig. 201. Upper (superior) part of gynoecium from the side (arrow-heads point to stigmatic secretion). Figs 202–212. TS gynoecium at different levels. Fig. 202. Free carpels; since the carpel tips are recurved, each carpel appears twice on the figure. Fig. 203. Postgenitally united superior part of gynoecium (arrow-head points to unfused secretory canal). Fig. 204. Slightly lower section, with septal nectaries (arrow-heads). Fig. 205. Pollen tube transmitting tract above upper placentae. Fig. 206. Placental region of upper ovules. Fig. 207. Micropylar region of upper ovules (arrow-heads indicate secretion in locules). Fig. 208. Ovary with upper ovules (arrow-heads indicate levels in Figs 213 and 215). Fig. 209. Nucellar region of ovules (arrow-heads point to pollen tube transmitting tissue). Fig. 210. Ovary with lower ovules. Fig. 211. Ovary above transition between symplicate and synascidiate zone. Fig. 212. Transition between symplicate and synascidiate zone. Scale bars: Fig. 200=1 mm; Figs 201, 208, 211=0.5 mm; Figs 202–207, 209, 210, 212=0.25 mm.

GYNOECIUM IN BASAL MONOCOTS

35

Figures 213–216. Tamus communis (Dioscoreaceae), female flower at anthesis. Fig. 213. LS gynoecium at level indicated in Fig. 208. Fig. 214. Part of Fig. 213 (arrow-head indicates micropyle of the lower ovule). Fig. 215. LS gynoecium at level indicated in Fig. 208 (arrow-head points to septal nectary). Fig. 216. Part of Fig. 215 (arrow-head indiates micropyle of lower ovule). Scale bars: Figs 213, 215=0.5 mm; Figs 214, 216=0.25 mm.

However, a secretory zone with flask-shaped papillae is present on the flanks of the free upper part of the carpels; it is possibly an osmophore. The stigma extends only around the upper part of the ventral slit. It is strongly secretory, unicellularpapillate (dry, after Heslop-Harrison & Shivanna, 1977). A style is present. The ventral slits are postgenitally fused at the periphery but a continuous secretory canal discharges into the stigmatic region (angiospermy type 2). The pollen tube transmitting tissue is one-layered and well differentiated. The ovarial cavity is partly lined with secretion along the placentae. A compitum is present. The carpel surface is glabrous. Stomata are lacking. Cells with oxalate crystals and raphides are present in the carpel wall. Cells with oxalate druses, tanniferous tissue, sclereids, oil cells, mucilage cells, and laticifers are absent. Intercellular cavities are absent. Ovules c. 42–46 per carpel (in Tacca chantrieri ), with distinct funicle, large, weakly crassinucellar (Hakansson, 1921; Paetow, 1931), bitegmic (Suessenguth, 1921), anatropous, irregularly directed (horizontal, ascendant and pendant in the same gynoecium), along the length of the ovary; chalaza unextended; an aril is lacking; however, the raphe is thick and resembles that in some Aristolochiaceae at anthesis. Placenta lateral, linear (parietal) (Rao, 1969). Nucellus broad (by strong enlargement of the subepidermal cell layer), with a single meiocyte, occasionally with more than one (Hakansson, 1921; Suessenguth, 1921; Paetow, 1931). The micropyle is formed by the inner integument (Hakansson, 1921); a micropylar cavity is lacking. A nucellar beak is lacking. The outer integument is unlobed, the inner is lobed. The outer integument is semiannular, the inner is annular. Both integuments

are not convoluted. Both integuments are 2 cell layers thick. Tanniferous tissue is lacking in the integuments but present in the hypostase. Cells with oxalate crystals/druses/raphides, oil cells and mucilage cells are lacking in the ovules. The ovular vascular bundle ends in the chalaza.

DISCUSSION CARPEL MORPHOLOGY AND POLLEN TUBE TRANSMITTING TRACT

Uhl (1947) considers the flower of Triglochin, Scheuchzeria, Potamogeton, and perhaps Aponogeton, to be a pseudanthium, i.e. a condensed partial inflorescence, in contrast to Alismataceae where each flower is a real flower. For Potamogeton pseudanthial nature of the flowers was suggested earlier by Kunth (1841) and Miki (1937). According to Eames (1961) only Triglochin and related genera, but not Scheuchzeria and Potamogeton, have pseudanthia. Pseudanthial nature of the flowers of at least part of the Alismatales s.s. was also discussed by Burger (1977), and somewhat differently by Posluszny & Charlton (1993) and Posluszny, Charlton & Les (1998). In view of the recently better substantiated phylogeny of the basal angiosperms a pseudanthial nature of the bisexual flowers in Alismatales is unlikely. This is not the place to develop this issue in detail, but the following discussion is based on an euanthial interpretation. Flowers are bisexual in most families. In some families both bisexual and unisexual flowers occur (Araceae, Alismataceae, Aponogetonaceae, Hydrocharitaceae, Juncaginaceae, Triuridaceae, Dioscoreaceae). A few families of the underwater flowering Alismatales only

36

A. IGERSHEIM ET AL.

Figures 217–224. Tacca chantrieri (Taccaceae), female stage of anthesis. Fig. 217. Gynoecium from above. Fig. 218. LM-micrograph of upper (superior) part of gynoecium removed from lower part and viewed from below (arrow-heads point to stigmatic regions, which are dark after treatment with KMnO4; in contrast, the apical carpel lobes are genuinely dark and are not stigmatic). Fig. 219. SEM-micrograph of stigmatic region (arrow-head). Fig. 220. Stigma, unicellular-papillate. Figs 221–224. TS gynoecium at different levels. Fig. 221. Stigmatic region (arrow-head points to secretory zone with flask-shaped epidermal cells, different from stigma; perhaps osmophore). Fig. 222. Detail of this secretory zone. Fig. 223. Stylar region with unfused secretory canal. Fig. 224. Ovary with anatropous ovules on parietal placentae. Scale bars: Figs 217–219=1 mm; Figs 221, 224=0.5 mm; Fig. 223=0.25 mm; Figs 220, 222=0.1 mm.

GYNOECIUM IN BASAL MONOCOTS

37

Figures 225–227. Tacca chantrieri (Taccaceae), female stage of anthesis. Fig. 225. Ovule from the side. Fig. 226. Median LS ovule. Fig. 227. TS ovule (arrow-heads indicate inner integument). Scale bars: Figs 225–227=0.25 mm.

contain taxa with unisexual flowers (Cymodoceaceae, Najadaceae, Zannichelliaceae, Zosteraceae). Carpel number is often 3, 6 or 1; in some families one or a few genera show a secondary increase in carpel number to 20 or more (Araceae, Alismataceae, Hydrocharitaceae, Limnocharitaceae, Triuridaceae), up to 660 in Sagittaria (Alismataceae) (Salisbury, 1926; Kaul, 1967a). It has been disputed whether unilocular gynoecia in Araceae were pseudomonomerous or monomerous (Eckardt, 1937; Barabe´ & Labrecque, 1984; Barabe´, Chre´tien & Forget, 1987a; Grayum, 1990). The basic form of the gynoecium in Araceae seems to be a tubular structure, which can be unilocular or partially or completely divided into two or more locules (e.g. Lehmann & Sattler, 1992; Scribailo & Tomlinson, 1992; Barabe´ & Bertrand, 1996; Boubes & Barabe´, 1996, 1997). Is this basic form a single ascidiate carpel, which may be secondarily subdivided? Or is it a pseudomonomerous gynoecium, derived from a syncarpous gynoecium of more than one carpel? This should be tackled in a broad comparative developmental study. That secondary increase in locule number does occur, is clearly shown by Philodendron with up to 47 locules (Mayo, 1989). Carpels vary between small (0.8 mm long in Luronium, Alismataceae) and very large (35 mm long in Elodea, Hydrocharitaceae). They are commonly small, but medium in Limnocharitaceae, some Tofieldiaceae, and Dioscoreaceae, large in Butomaceae, Taccaceae, medium to very large in Hydrocharitaceae. Carpels are whorled, in several taxa in more than one whorl (Salisbury, 1926; Sattler & Singh, 1978), but if numerous, they are irregularly arranged (Leins & Stadler, 1973; Charlton, 1991; Ru¨bsamen-Weustenfeld, 1991; Wang et al., 1998). At the end of an inflorescence peloria-like structures occur in some groups, such as Acoraceae (Buzgo, 1999; Buzgo & Endress, 2000), and Potamogetonaceae (Charlton & Posluszny, 1991),

where carpels may appear in a spiral arrangement. However, such a peloria-like structure cannot be regarded as a normal flower but rather as a pseudanthium of several highly reduced flowers. Gynoecia with free carpels are predominant. However, they are pronouncedly united in Acoraceae, Araceae, Hydrocharitaceae, Juncaginaceae, Dioscoreaceae, and Taccaceae. In some additional families they are only basally united. Carpel form is diverse. Pronouncedly ascidiate carpels are present in Acoraceae, some Araceae, and Potamogetonaceae. In many families with underwater flowers the carpels are completely ascidiate. In Najas (Najadaceae) the ovary wall is only two cell layers thick in its entire circumference (Campbell, 1897; Guignard, 1901; Swamy & Lakshmanan, 1962) (see below). Such a thin wall would probably be architecturally more problematical for angiospermy if the carpel were plicate! However, carpel margins may be very thin and may have only two cell layers also in carpels that are at least partly plicate of some Alismatales s.s., such as Butomus (Butomaceae) and Hydrocleys, Enhalus, and Ottelia (Hydrocharitaceae). In the extreme case, margins even have only a single cell layer (Vallisneria, Hydrocharitaceae; Leinfellner, 1940), but here they are inside a syncarpous structure and not postgenitally fused, so that an architectural constraint for a certain firmness is lacking. In Alismataceae and Triuridaceae the carpels begin development as ascidiate structures but at anthesis they are largely plicate. In syncarpous gynoecia the carpels may be largely or completely (sym-)plicate (Araceae p.p., Hydrocharitaceae, Dioscoreaceae, Taccaceae). The interpretation of carpel form is problematic in some families. In Limnocharis (Limnocharitaceae) the gynoecium is in some way similar to that in Nymphaeaceae (Troll, 1932, 1933; Kaul, 1967b): the carpels are free, plicate, if interpreted as obliquely inserted, but united, synascidiate, if in-

38

A. IGERSHEIM ET AL.

Figure 228. Schematic median LS carpels (or entire syncarpous gynoecia) at anthesis; ventral side at right; outer and inner surfaces of carpels indicated; solid parts of carpel walls and ovules drawn with uninterrupted lines, outline of postgenitally fused parts drawn with interrupted lines, outline of free parts outside the median plane drawn with dotted lines. Scale bar=1 mm. A, Acorus calamus (Acoraceae). B, Gymnostachys anceps (Araceae). C, Pothos longipes (Araceae). D, Alisma lanceolatum (Alismataceae). E, Aponogeton ulvaceus (Aponogetonaceae). F, Butomus umbellatus (Butomaceae). G, Hydrocharis morsus-ranae (Hydrocharitaceae). H, Triglochin maritima (Juncaginaceae). I, Hydrocleys nymphoides (Limnocharitaceae). J, Potamogeton alpinus (Potamogetonaceae). K, Scheuchzeria palustris (Scheuchzeriaceae). L, Tofieldia calyculata (Tofieldiaceae). M, Sciaphila albescens (Triuridaceae) (preanthetic, simplified after Ru¨bsamen-Weustenfeld, 1991, plate 12 f). N, Tamus communis (Dioscoreaceae). O, Tacca chantrieri (Taccaceae).

terpreted as horizontally inserted. The same problem arises in Triglochin (Juncaginaceae) and Aponogeton (Aponogetonaceae) (see also Eber, 1934). The ovary is commonly superior, but it is partly inferior in some Araceae (sunken in the spadix), Butomaceae, and completely inferior in Hydrocharitaceae, and in Dioscoreales. The carpel apex is more or less prominently laterally two-lobed in a number of Alismatales s.s. (references see above), such as in the majority of Hydrocharitaceae (especially those with aerial flowers), very pronounced in various families with underwater flowers, weakly so in Butomaceae, Limnocharitaceae, Potamogetonaceae, Scheuchzeriaceae, among Dioscoreales in Dioscoreaceae, Taccaceae.

Carpels with dorsally bulged up locules are especially pronounced in Alismataceae and Triuridaceae, and also present but less pronounced in Acoraceae, Araceae, Aponogetonaceae and Potamogetonaceae. The ovary locule is filled by the ovule(s) in a few Araceae, in Alismataceae, Potamogetonaceae and Triuridaceae. Septal nectaries are present in Alismataceae, Aponogetonaceae, Butomaceae, Limnocharitaceae, Dioscoreaceae, and Taccaceae (Daumann, 1970). Stigmatic secretion serving as nectar is present in some Araceae, such as Monstera (Ramı´rez & Go´mez, 1978), and Anthurium (Daumann, 1931b; Croat, 1980). In some Hydrocharitaceae nectar is secreted at the base of staminodes (Daumann, 1970), in Alismataceae a com-

GYNOECIUM IN BASAL MONOCOTS

39

Figure 229. Schematic TS carpels (or entire syncarpous gynoecia) at anthesis; ventral side up for single carpels; outer and inner surfaces of carpels drawn with normal lines, postgenitally fused areas drawn with interrupted lines, vascular bundles drawn with thinner lines; each figure with one to three sections above the ovary and one to four sections of the ovary. Scale bar=1 mm. A, Acorus calamus (Acoraceae). B, Gymnostachys anceps (Araceae). C, Pothos longipes (Araceae). D, Damasonium alisma (Alismataceae). E, Aponogeton ulvaceus (Aponogetonaceae). F, Butomus umbellatus (Butomaceae). G, Hydrocharis morsus-ranae (Hydrocharitaceae). H, Elodea nuttallii (Hydrocharitaceae). I, Triglochin maritima (Juncaginaceae).

40

A. IGERSHEIM ET AL.

Figure 230. Schematic TS carpels (or entire syncarpous gynoecia) at anthesis; ventral side up for single carpels; outer and inner surfaces of carpels drawn with normal lines (outer surface of the inferior ovary part not drawn in the last Figure of G), postgenitally fused areas drawn with interrupted lines, vascular bundles drawn with thinner lines; each figure with one to three sections above the ovary and one to four sections of the ovary. Scale bar=1 mm. A, Hydrocleys nymphoides (Limnocharitaceae). B, Potamogeton alpinus (Potamogetonaceae). C, Scheuchzeria palustris (Scheuchzeriaceae). D, Tofieldia calyculata (Tofieldiaceae). E, Sciaphila albescens (Triuridaceae). F, Tamus communis (Dioscoreaceae). G, Tacca chantrieri (Taccaceae).

GYNOECIUM IN BASAL MONOCOTS

41

Figure 231. Forms of pluriovulate placentae, at anthesis. Scale bar=5 mm. A, Butomus umbellatus (Butomaceae), laminar–diffuse. B, Hydrocleys nymphoides (Limnocharitaceae), laminar–diffuse. C, Tofieldia calyculata (Tofieldiaceae), more or less linear. D, Tacca chantrieri (Taccaceae), parietal, protruding–diffuse.

bination of staminodial and septal nectaries occurs (Daumann, 1970; Smets et al., 2000). This suggests that these two types may be related: the nectariferous area may have evolutionarily expanded and shifted from the androecial to the gynoecial region and/or vice versa. In Acorus pronounced slits are present between the carpels without being secretory (Buzgo, 1999; Buzgo & Endress, 2000). This is reminiscent of nonsecretory slits in the same position in basal angiosperms, such as Saruma (Aristolochiaceae) and Nymphaea (Nymphaeaceae) (Igersheim & Endress, 1998). Stigmas are various, small or large, with large stigmas especially occurring in wind-pollinated groups (Juncaginaceae, Potamogetonaceae, Scheuchzeriaceae) and in water-pollinated groups. They are mostly unicellular-papillate or non-papillate, in Butomaceae uniseriate-pluricellular-papillate, in Limnobium (Hydrocharitaceae) pluriseriate-pluricellular-papillate (Heslop-Harrison & Shivanna, 1977); they are commonly weakly secretory or dry, but strongly secretory in Acoraceae and most Araceae. A style is absent in Acoraceae, most Araceae, and part of Alismatales s.s., especially in the wind-pollinated families. All four types of angiospermy (Endress & Igersheim, 2000) occur in basal monocots. Type 1 is present in Araceae and Hydrocharitaceae, type 2 in Alismataceae, Aponogetonaceae, Butomaceae, Limnocharitaceae, Scheuchzeriaceae, Dioscoreaceae, Taccaceae, type 3 in Acoraceae and Tofieldiaceae, type 4 in Juncaginaceae and Potamogetonaceae. Although Acoraceae and Araceae fall into different categories, the pollen tube transmitting tracts are similar: narrow canals lined with

upwards directed papillae. These papillate epidermal cells are fused over a short distance in Acoraceae, but apparently unfused in the Araceae studied. This apparent discrepancy needs critical comparative study in more Araceae taxa. In some families with unfused canals throughout the carpels (type 1 and 2), pollen grains were found inside carpels, such as in Butomus (Butomaceae) (Johri & Bhatnagar, 1957), in Butomopsis and Limnocharis (Limnocharitaceae) (Johri 1935a, 1936b; Sahni & Johri, 1936; Johri & Bhatnagar, 1957), and in Boottia and Ottelia (Hydrocharitaceae) (Islam, 1950; Johri & Bhatnagar, 1957). The ovary locules are commonly filled with secretion in some families (especially Acoraceae, Araceae, Hydrocharitaceae, Najadaceae, Dioscoreaceae). In some of these the secretion is a thick mucilage (Acoraceae, some Araceae, Hydrocharitaceae, Najadaceae). This mucilage is not easily penetrable by fixing liquids or solvents, and ovules enclosed by it are therefore difficult to preserve properly (e.g. Acorus; Buzgo, 1999; Enhalus, Hydrocharitaceae; Svedelius, 1904). The secretion originates from secretory hairs around the placenta (Acoraceae, Araceae; Gue´guen, 1901; French, 1987; Buzgo, 1994; Najadaceae; Vijayaraghavan & Kapoor, 1980) or from papillate pads between the ovules (Hydrocharitaceae p.p.; Troll, 1931; Kaul, 1969; Indra & Krishnamurthy, 1982, 1984; Apparao & Shah, 1989) or from the entire surface of the locule (Hydrocharitaceae p.p.). There is a correlation between strong secretion within carpels and on stigmas, and life in the water or in wet habitats (e.g. Acoraceae, many Araceae, incl. Lemnaceae; Endress, 1990, 1995; Rudall et al., 1998).

Figure 232. Median LS ovules, at anthesis. Scale bar=0.5 mm. A, Acorus calamus (Acoraceae). B, Acorus gramineus (Acoraceae). C, Gymnostachys anceps (Araceae). D, Orontium aquaticum (Araceae). E, Pothos longipes (Araceae). F, Alisma lanceolatum (Alismataceae). G, Damasonium alisma (Alismataceae). H, Luronium natans (Alismataceae). I, Aponogeton distachyos (Aponogetonaceae). J, Aponogeton ulvaceus (Aponogetonaceae). K, Butomus umbellatus (Butomaceae). L, Elodea nuttallii (Hydrocharitaceae). M, Hydrocharis morsus-ranae (Hydrocharitaceae). N, Stratiotes aloides (Hydrocharitaceae). O, Vallisneria americana (Hydrocharitaceae). P, Triglochin maritima (Juncaginaceae). Q, Hydrocleys nymphoides (Limnocharitaceae). R, Groenlandia densa (Potamogetonaceae). S, Potamogeton alpinus (Potamogetonaceae). T, Scheuchzeria palustris (Scheuchzeriaceae). U, Tofieldia calyculata (Tofieldiaceae). V, Tamus communis (Dioscoreaceae). W, Tacca chantrieri (Taccaceae).

42 A. IGERSHEIM ET AL.

GYNOECIUM IN BASAL MONOCOTS

In addition, strong secretion in carpels also often goes hand in hand with carpels that are completely or largely unfused (but closed by secretion). Pollen tube transmitting tissue is 1-layered and well differentiated throughout. A compitum is present in Acoraceae, many Araceae, Hydrocharitaceae, Tofieldiaceae and in Dioscoreales.

CARPEL ANATOMY

In Acoraceae carpel vasculature is simple. A dorsal vascular bundle is lacking. Above the placenta each carpel has two weak lateral bundles. In the placental zone the laterals of adjacent carpels unite in the centre of the septa to form synlaterals; the ovules are served by offshoots of these synlaterals (see also van Tieghem, 1871; Saunders, 1937/1939; Eyde et al., 1967; Buzgo, 1999; Buzgo & Endress, 2000). In Araceae vasculature is diverse. In some genera a dorsal bundle for each carpel and a synlateral between the carpels are present; the ovules are provided by bundles branching off from the synlaterals or from common bundles from the floral base, such as in Pothos p.p. (Eyde et al., 1967), Alocasia (Koschewnikoff, 1877) Richardia (van Tieghem, 1867, 1871), Spathiphyllum (Barabe´ & Chre´ tien, 1986), and Zamioculcas (Barabe´ & Forget, 1988b). In other genera a dorsal and two or more laterals are present in each carpel, such as in Pothos longipes (Buzgo, 1999), Lysichiton (Barabe´ & Labrecque, 1984), Anchomanes (Barabe´ et al., 1986), Homalomena (Eyde et al., 1967), Spathiphyllum (Eyde et al., 1967), and Symplocarpus (Barabe´ , 1982). In some genera a dorsal bundle is reduced or lacking at least in part of the species, such as in Spathicarpa (Barabe´ & Chre´ tien, 1985; Barabe´ et al., 1987a), Anthurium (Koschewnikoff, 1877; Barahona Carvajal, 1978; Manya-Chernej, 1978; Barabe´ et al., 1984), and Schismatoglottis (Hotta, 1971). As an extreme pattern an irregular number of vascular bundles without a distinctive dorsal and lateral ones serve the carpels. This may not be surprising for pronouncedly ascidiate carpels or flask-shaped syncarpous gynoecia with an evenly developing wall, such as in Orontium (Eyde et al., 1967; Barabe´ & Labrecque, 1985), Aglaonema (Barabe´ & Forget, 1988a), Arum (Eckardt, 1937), Calla (Barabe´ & Labrecque, 1983), Culcasia (Barabe´ & Forget, 1993), Lasia, Peltandra, and Xanthosoma (Eyde et al., 1967). In Gymnostachys (the basalmost genus in Araceae), Buzgo (1999) found that discrete vascular bundles are not present but rather xylem and phloem elements that are not strictly associated with each other. In Alismataceae each carpel has a dorsal and two lateral vascular bundles; additional bundles may be in between. At the base of the carpel the two laterals merge into a ventral median, which also serves the

43

ovule, (see also Saunders, 1929; Singh, 1966a; Kaul, 1976). In Alisma the dorsal bundle ‘splits’ into two parts by a laticifer in the middle (see also Singh, 1966a). The dorsal and the ventral bundle may merge in the floral basis and form a single trace (Singh, 1966a; Kaul, 1967a). In Aponogetonaceae each carpel has a dorsal and two (in Aponogeton distachyos two to six) lateral vascular bundles; in the floral base the lateral bundles of each carpel flank merge into one bundle (Saunders, 1929; Singh, 1965c). The ovules are served by the lateral bundles. In Butomaceae the dorsal bundle is accompanied by a variable number of lateral bundles. The dorsal and the laterals are connected by several oblique secondary bundles. The laminar–diffuse ovules are served by the laterals and the connecting secondary bundles (Kaul, 1976; according to Zazhurilo & Kusnetsova, 1939, only by the laterals). In Hydrocharitaceae, with its diversity in floral structure, also carpel vasculature is diverse (Saunders, 1929; Eber, 1934; Jitariu, 1952; Singh, 1967a; Kaul, 1968; Tomlinson, 1969). A dorsal bundle and a variable number of lateral bundles and synlaterals are present in those with large flowers (synlaterals in the outer wall in Bootia, in the inner part of each septum in Hydrocharis and Limnobium; Kaul, 1968). In Elodea in which the underwater ovary has only a very thin wall, dorsal bundles are present only in the apocarpous region of the gynoecium, whereas in the inferior ovary there is only one bundle in each placental radius, where the ovary wall is thicker, thus serving all floral organs (see also Caspary, 1858b; Jitariu, 1952); this is similar in Blyxa p.p. (Kaul, 1968) and Hydrilla (Singh, 1967b). In taxa with numerous ovules per carpel, the ovules are served by smaller secondary bundles between the dorsal and main lateral bundles (Suessenguth, 1921; Kaul, 1968). In Juncaginaceae, carpels of Triglochin have a dorsal bundle that branches somewhat in the stigmatic region. The median ovule is served by a ventral bundle that may continue above the placenta as a ventral or two lateral bundles (see also Saunders, 1929; Eber, 1934; Uhl, 1947; Eckardt, 1957; Serbanescu-Jitariu, 1973a; Lieu, 1979). Lilaea has a dorsal and two lateral bundles, which unite in the base into a ventral bundle, which also serves the ovule (Arber, 1940; Agrawal, 1952; Singh, 1965d). In Limnocharitaceae, carpels of Limnocharis have a dorsal and two closely associated lateral bundles as well as a ventral bundle; in addition, there are secondary connections between these bundles, from which the laminar-diffuse ovules are served (Kaul, 1976; Nayar & Sworupanandan, 1978). Carpels of Hydrocleys lack the two distinct lateral bundles but have many thin lateral bundles that serve the ovules (Kaul, 1976);

44

A. IGERSHEIM ET AL.

in the ascidiate zone a ventral bundle complex is present. The main bundles tend to branch in the stigmatic region (Kaul, 1976). In Potamogetonaceae carpels have a dorsal and a ventral vascular bundle; the ventral bundle serves the ovule and does not extend beyond the placenta. Dorsal and ventral bundle unite in the floral base before they join the other floral bundles (Saunders, 1929, 1937/ 1939; Singh, 1965a; Serbanescu-Jitariu, 1972b). In Scheuchzeriaceae carpels have a dorsal and two lateral bundles; the latter serve the ovules. In the floral base the laterals unite into synlaterals before they join the dorsals (Saunders, 1929; Eames, 1931; Eber, 1934; Uhl, 1947; Serbanescu-Jitariu, 1966). In Tofieldiaceae carpels have a dorsal and two lateral bundles (often synlateral at the base) (Gatin, 1920; Saunders, 1928, 1937/1939; Eames, 1931; El-Hamidi, 1952; Leinfellner, 1969; Eie, 1972; Utech, 1978; Sterling, 1979). Underwater Alismatales s.s., with their reduced flowers, commonly have simple carpel vasculature. As an extreme case, in the style and in the only 2-celllayered ovary wall of Najas there is no vascular bundle, except for a rudimentary dorsal bundle, which is restricted to the area below the ovary; the ovule is served by a ventral bundle (Gue´ guen, 1901; Uhl, 1947; Singh, 1965b). This is similar, but with the dorsal bundle extending into the ovary wall for some distance, in Althenia (Teryokhin & Chubarov, 1991), Cymodocea (Bornet, 1864), Phyllospadix (Saunders, 1937/1939), Ruppia (Saunders, 1937/1939; Gamerro, 1968; Serbanescu-Jitariu, 1974b), Syringodium (Tomlinson & Posluszny, 1978), and Zannichellia (Campbell, 1897; Saunders, 1937/1939; Serbanescu-Jitariu, 1972a; Vijayaraghavan & Kumari, 1974). In Amphibolis the dorsal bundle extends up to the stigma, and the ovule seems to be served by several bundles of the ventral side of the carpel (McConchie et al., 1982). In Zostera carpel vasculature is lacking except for the ovule supply (Saunders, 1937/1939; Serbanescu-Jitariu, 1974b). In Triuridaceae each carpel has a dorsal bundle, which is only present in the ovary but not in the style. The ovule is served by a ventral bundle, which does not extend beyond the ovule (Ru¨ bsamen-Weustenfeld, 1991). In Dioscoreaceae each carpel has a dorsal bundle, which goes up to the stigmatic region, where it ends with ample tracheoids. In the inferior ovary there are two lateral bundles, which serve the ovules and the septal nectaries (Saunders, 1937/1939). The same vascular pattern is found in Trichopus (Trichopodaceae) (Kale & Pai, 1979). In Taccaceae each carpel has a dorsal bundle, which extends up to the stigmatic region. In the inferior ovary two main lateral bundles serve the ovules; secondary, additional bundles are also present, which form a

network with the primary bundles (Saunders, 1931; Rao, 1969). CARPEL HISTOLOGY

The carpel surface is glabrous throughout. Stomata are present in part of the families (Acoraceae, Araceae, part of Alismataceae, Aponogetonaceae, Butomacae, Juncaginaceae, Limnocharitaceae, Scheuchzeriaceae). Oxalate crystals are present in the majority of families, whereas oxalate druses are lacking in most families (present in Acoraceae, some basal Araceae, Tofieldiaceae). Oxalate raphides are present in basal Araceae (not in Acorus!) and in Dioscoreales. Tanniferous cells are only present in Acorus, Orontium (basal Araceae), Hydrocharitaceae, and Potamogetonaceae. Ethereal oil cells were only found in Acorus gramineus (not in A. calamus), they are superficial (probably intrusive). Mucilage cells were found in Vallisneria (Hydrocharitaceae) and Tamus (Dioscoreaceae). Sclereids are absent throughout. Laticifers were found in Alismataceae, Aponogetonaceae, Juncaginaceae, and Limnocharitaceae. Intercellular cavities are present in most families, especially in water plants (among basal Araceae, e.g. in Orontium, but not in Gymnostachys and Pothos; lacking also in Alismataceae, Scheuchzeriaceae, and Dioscoreales). OVULE MORPHOLOGY

Ovule number per carpel is commonly low. In Acoraceae it is 2–6. In several families it is 1 (almost all basal Araceae, many True Araceae, most Alismataceae, Juncaginaceae, Potamogetonaceae, all underwaterpollinated families of Alismatales s.s., Triuridaceae). An increase in ovule number has occurred several times in basal monocots: in some Araceae, Aponogetonaceae, Butomaceae, Hydrocharitaceae (up to more than 200), Limnocharitaceae, some Dioscoreaceae, and Taccaceae. Ovule size varies between medium (0.3 mm long in Tofieldia, Tofieldiaceae) and large (1.1 mm long in Orontium, Araceae). It tends to be medium in Alismatales s.s. (large in Hydrocharitaceae and Juncaginaceae) and large in Dioscoreales. Placentation is laminar-diffuse in Butomaceae, some Hydrocharitaceae, and in Limnocharitaceae; in Butomaceae and Limnocharitaceae (but not in Hydrocharitaceae) ovules are lacking in the dorsal region of each carpel. In Acoraceae and rarely in Araceae (Mangonia; Mayo et al., 1997) several ovules are arranged in a horizontal line. In some true Araceae the placenta is axile or parietal and protruding-diffuse or basal-diffuse. Otherwise the placenta is axile or parietal and linear. More than in any other basal angiosperm groups, the ovules tend to have a distinct funicle (Acoraceae,

GYNOECIUM IN BASAL MONOCOTS

many advanced Araceae, Alismataceae, Butomaceae, Limnocharitaceae, Hydrocharitaceae p.p.). Ovules are apical/pendant in Acoraceae, a number of Araceae, Potamogetonaceae, some underwater Alismatales s.s. (and Dioscoreales) but basal or at midheight/ascendant in most Alismatales s.s. and part of Araceae. They are median in Acoraceae, Araceae, Alismataceae, Juncaginaceae, Limnocharitaceae, Potamogetonaceae and Triuridaceae, lateral in the other families. Almost all taxa have bitegmic ovules. Transitions from bitegmy to (almost) unitegmy are present in Aponogeton (Aponogetonaceae) (Afzelius, 1920), and in Tofieldia (Tofieldiaceae) (Sterling, 1979), similar as in Ranunculaceae and Menispermaceae (Endress & Igersheim, 1999). Erratic genera with unitegmic ovules are Gymnostachys (Buzgo, 1999) and Montrichardia (Goebel, 1897) (both Araceae), and Thalassia (Tomlinson, 1969) (Hydrocharitaceae). Reduction to a single integument seems to be correlated with an extended chalaza. Although anatropous ovules appear to be predominant in the assemblage treated here, relatively many basal monocots have orthotropous ovules, notably Acoraceae, many Araceae, some Hydrocharitaceae, Potamogetonaceae, and some families with underwater flowers. In some families ovules are at first orthotropous or anatropous but become campylotropous in later development (Alismataceae, Limnocharitaceae, Potamogetonaceae, Tofieldiaceae, Ruppiaceae). Slightly campylotropous or amphitropous ovules are also reported from a few Araceae (French, 1986; Grayum, 1991). In Alismataceae and Potamogetonaceae the single ovule fills the locule, and the campylotropous form seems to be architecturally correlated with the dorsally bulging out of the locule. Campylotropous ovules may originate in different ways, as discussed, e.g. by Bouman & Boesewinkel (1991). This is nicely shown by Alismataceae/Limnocharitaceae and Potamogetonaceae. Their mature ovules have a similar shape at first sight, but a closer look shows that in Alismataceae/Limnocharitaceae the outer integument is absent on the concave side (semiannular), whereas it is present in Potamogetonaceae (annular). This difference is due to an anatropous stage in earlier development in the former, and an orthotropous stage in the latter. Anatropous ovules are syntropous (curved in the same direction as the carpel; for terminology see Endress, 1994) in uniovulate carpels, except for Luronium (Alismataceae), where they are antitropous (curved in the opposite direction than the carpel). An aril is lacking throughout; a nucellar beak is also lacking. The micropyle is almost always formed by the inner integument, only rarely by both integuments (some

45

Araceae, some Hydrocharitaceae, some underwater Alismatales s.s., Tofieldiaceae, Dioscoreaceae). In the unitegmic Gymnostachys (Araceae) a micropyle is not formed. A micropylar cavity is lacking throughout. The outer integument is always unlobed. The inner is lobed or unlobed. It is lobed in Acoraceae p.p., some Araceae, Aponogetonaceae, Butomaceae, Hydrocharitaceae, Potamogetonaceae, Tofieldiaceae, Scheuchzeriaceae, and Dioscoreales. The inner integument is always annular. The outer is semiannular or annular. As in other basal angiosperms studied it is strictly annular in orthotropous ovules but commonly semiannular in anatropous ovules, probably depending on how early in development the curvature of the ovule begins, i.e. the more likely it becomes semiannular, the earlier curvature begins to develop. Integuments are not convoluted. The only exception found is the inner integument in Acorus calamus (Acoraceae). This is especially interesting, because this rare feature is also present in some Piperales (Igersheim & Endress, 1998).

OVULE ANATOMY

In almost all groups studied the vascular bundle of the ovule ends in the chalaza. Only in some true Araceae it branches in the chalaza into several strands, which may continue into the base of the outer integument (Arophyteae; French, 1986). This branching is more prominent in orthotropous than in anatropous ovules. In Scheuchzeriaceae a vascular strand extends into the outer integument after anthesis (Nikiticheva, 1990b; Nikiticheva & Proskurina, 1992).

OVULE HISTOLOGY

A single meiocyte develops in the nucellus. Rarely some ovules in a species have several meiocytes; this was reported from Alisma (Alismataceae) (Johri, 1936a), Aponogeton (Aponogetonaceae) (Afzelius, 1920; Saˆ ne´ , 1939), Butomus (Butomaceae) (Holmgren, 1913), Hydrilla (Hydrocharitaceae) (Maheshwari, 1933), Ruppia (Ruppiaceae) (Murbeck, 1902; Graves, 1908), Tacca (Taccaceae) (Hakansson, 1921; Suessenguth, 1921; Paetow, 1931); in Arisaema triphyllum (Araceae) several meiocytes were found to be common (Pickett, 1913). Some taxa have crassinucellar ovules (basal Araceae, Lemnaceae, Peltandra of true Araceae, Aponogetonaceae, Hydrocharitaceae p.p., Juncaginaceae, Potamogetonaceae, Dioscoreaceae). In several groups the ovules have only two to three cell layers above the meiocyte, thus they are almost tenuinucellar. These cell layers develop either by periclinal divisions of the epidermis (pseudocrassinucellar; term after Davis,

46

A. IGERSHEIM ET AL.

1966) or of the archesporial cell (weakly crassinucellar). Pseudocrassinucellar ovules are not distinguished from tenuinucellar ones by some authors (Rudall, 1997). However, since these patterns seem to be rather constant within families, we feel a distinction to be useful. Thus ovules are pseudocrassinucellar in Acoraceae, most true Araceae, and Zosteraceae; weakly crassinucellar in Butomaceae, Najadaceae, Ruppiaceae, Tofieldiaceae, Zannichelliaceae and Taccaceae. Tenuinucellar ovules occur in a few true Araceae, Hydrocharitaceae p.p., and Triuridaceae, and rarely in Alismataceae. Alismataceae and Limnocharitaceae commonly have ovules intermediate between pseudocrassinucellar and tenuinucellar, because some but not all epidermal cells around the meiocyte undergo periclinal divisions. In Araceae pseudocrassinucellar and tenuinucellar ovules are accompanied by an integumentary tapetum. An integumentary tapetum is also present in the crassinucellar ovules of Orontium (van Tieghem, 1907). Also in weakly crassinucellar or pseudocrassinucellar ovules the nucellus may become relatively thick (broad) by radial elongation of the subepidermal cells (Acorus, Tacca, and other monocots; cf. Rudall, 1997). This kind of differentiation is less common in eudicots. Nucellus breadth varies between narrow (0.03 mm in Pothos, Araceae) and broad (more than 0.3 mm in Stratiotes, Hydrocharitaceae, and Tacca, Taccaceae). Also within a family there may be considerable variation. Although many monocots have both integuments only two cell layers thick, thus implying dermal origin in development (Bouman, 1984), a number of basal monocots have thicker integuments, especially the outer integuments, comparable with magnoliids (Endress & Igersheim, 1997; Igersheim & Endress, 1997, 1998). An extreme group are basal Araceae with the outer integument 8–26-layered, the inner 3–6-layered. In Hydrocharitaceae the outer integument has up to 15 cell layers. In Acoraceae the outer is 3–4-layered, the inner 2-layered. The inner integument is 2-layered in most families but more than 2-layered in Araceae p.p., Hydrocharitaceae p.p., and Scheuchzeriaceae. Nevertheless, also a number of basal monocot families have both integuments only two cell layers thick (Araceae p.p., Alismataceae, Butomaceae, Hydrocharitaceae p.p., Limnocharitaceae, Potamogetonaceae p.p., Tofieldiaceae, some underwater Alismatales s.s., Triuridaceae, Taccaceae). This is of interest in view of a relationship with Piperales (incl. Aristolochiales), where this feature is predominant. Idioblasts are rare in the ovules. Tanniferous tissue was only found in the ovules of Acoraceae and in Taccaceae. Cells with oxalate crystals were found in Aponogetonaceae p.p. and Hydrocharitaceae p.p. Cells with oxalate druses/raphides, ethereal oil cells, and mucilage cells are lacking throughout.

EVOLUTIONARY ASPECTS OF CARPELS AND OVULES

Postgenitally fused carpels occur in Acoraceae but fusion is lacking (at least along the centre of the carpels) in many Alismatales. Since postgenital fusion is also predominant in Piperales (incl. Aristolochiales), the potential sister group of monocots (see below), postgenitally fused carpels are probably primitive at the level of monocots. Non-fused carpels may have evolved in concert with strong secretion in the internal space of the carpels in many Alismatales and Dioscoreales. However, other scenarios have to be considered as well, e.g. with Austrobaileyales or Ceratophyllum as sister groups (see below). In these cases, carpels closed by secretion could be possibly basal in monocots. In some families more than one type of ovules is present. Ovules are crassinucellar, pseudocrassinucellar and tenuinucellar in Araceae, crassinucellar and tenuinucellar in Hydrocharitaceae, pseudocrassinucellar to tenuinucellar in Alismataceae and Limnocharitaceae. This indicates an evolutionary lability of this nucellus character at a relatively low systematic level in basal monocots, whereas it is much more stable in (basal) eudicots. The considerable number of taxa with orthotropous ovules in basal monocots is obvious. Are they primitive in monocots? The presence in the probably basalmost family, Acoraceae, and in the potential sister group, Piperales, are strong arguments for this view. On the other hand, there is a strong functional correlation between orthotropous ovules and massive secretion in the ovary locules. The pollen tubes grow through the secretion directly into the micropyle (Buzgo, 1994), whereas in gynoecia without massive secretion the anatropy of the ovules helps to direct the micropyle immediately to the placenta from where the pollen tubes are taken up. Acoraceae, many Araceae and many Hydrocharitaceae have both orthotropous ovules and massive secretion in the ovaries. Plants with massive secretion occur predominantly in moist or wet habitats where there is no shortage of water (Endress, 1990; Rudall et al., 1998). Therefore, another hypothesis would be that orthotropous ovules tend to evolve secondarily in water plants. Also a number of Alismatales s.s. with underwater flowers and Potamogetonaceae have orthotropous ovules. In those the carpels are uniovulate and thus the ovule needs not to be anatropous for a direct contact with the locule surface. In such cases orthotropy may be derived. In magnoliids (and basal eudicots) a correlation was found between orthotropous ovules and a thin outer integument (Endress & Igersheim, 1997, 1999; Igersheim & Endress, 1998). This is less obvious in basal monocots. Although some underwater flowering Alismatales s.s. show this combination, it is not present in Acoraceae and some Araceae. At any rate, it will be

GYNOECIUM IN BASAL MONOCOTS

important to further follow this general correlation in basal angiosperms also in the framework of molecular developmental genetics of ovules (e.g. Gasser, Broadhvest & Hauser, 1998; Schneitz, 1999).

SPECIAL FEATURES OF CARPELS AND OVULES RELATIVE TO FRUITS AND SEEDS

The mucilage in the ovaries that functions in pollen tube transmission persists in the fruits and may play a role in seed dispersal, although this has not been studied in detail. In Hydrocharitaceae the fruit of Ottelia opens like a banana and the seeds are retained by the mucilage in the centre and are eaten by fish; in Vallisneria the fruit wall disintegrates and the seeds are also held together by the mucilage (C. D. K. Cook, pers. comm.). In Anthurium (Araceae) mucilage from the ovary or from seed tissues may help in the dispersal of epiphytic species by making the seeds sticky (Mayo et al., 1997). Vijayaraghavan & Kapoor (1980) hypothesize that the mucilage (of Najas, Najadaceae) may protect the developing seed from the aquatic environment. The apical part of the inner (or both) integument(s), which form(s) the micropyle is thickened and in some groups differentiates as an operculum in the mature seed (by expansion or periclinal division of the epidermis), which opens at germination. This is the case in Araceae (incl. Lemnaceae) (Grayum, 1991; Buzgo, 1994), and Zosteraceae (Shamrov, 1998).

FOSSIL RECORD

Fossil pollen comparable to those of some monocots in having a special graded reticulum are known from many Early Cretaceous palynofloras and mesofloras (Doyle, 1973; Doyle, Van Campo & Lugardon, 1975; Doyle et al., 1977; Walker & Walker, 1985; Friis, Crane & Pedersen, 1997; Friis, Pedersen & Crane, 1999). In addition, a tricarpellate flower from the Late Santonian Allon flora with Liliacidites pollen (Herendeen et al., 1999) supports its monocot nature. Well preserved fossils of clear affinity to Acorales, Alismatales and Dioscoreales appear only in the Upper Cretaceous and Tertiary fossil record (Daghlian, 1981; Herendeen & Crane, 1995; Gandolfo & Daghlian, 1999). The oldest, well-preserved probable monocot fossil flowers are male and have six united tepals and 3 stamens with monosulcate pollen. They were described from the Turonian of New Jersey and interpreted as Triuridaceae (Gandolfo et al., 1998; Gandolfo, Nixon & Crepet, 2000). Similar flower forms also occur in extant Dioscoreaceae (cf. e.g. Al-Shehbaz & Schubert, 1989). Cretovarium are other monocot flower fossils, probably melanthioid, from the Upper Cretaceous of Japan (Stopes & Fujii, 1910; Ohsawa, 1998). Organically

47

preserved potential monocot leaf remains were described from the Albian–Cenomanian of Australia (Pole, 1999). In a study considering the fossil record combined with differential molecular clock data, Bremer (2000) estimated the split of Acoraceae from the other monocots to be more than 134 million years old, and the split between Alismatales and the remaining monocots not much younger. SYSTEMATIC RELATIONSHIPS Basal monocots

Generally, monocots appear as a monophyletic group in molecular systematic studies. In almost all analyses based on one or several genes, Acorus appears as sister to all other monocots (Chase et al., 1993, 1995, 1998, 2000; Duvall et al., 1993a,b, 1995; Qiu et al., 1993; Nadot et al., 1995; Soltis et al., 1997; Davis et al., 1998a; Hahn, 1998; Ka¨ llersjo¨ et al., 1998; Kubitzki et al., 1998; Soltis et al., 2000), or Acorus forms a clade with Gymnostachys (Araceae) (French & Kressler, 1989; Davis, 1995) or with Alismatales (Davis et al., 1998b; Stevenson et al., 2000). Araceae and Alismatales s.s. are identified as the next higher basal monocots after Acorus in molecular analyses mentioned above. Additional support for these three groups as basal monocots comes from the finding that the fourth intron in the mitochondrial gene nad1 is cis-spliced in Acoraceae, Araceae and most Alismatales s.s. (as most dicots and gymnosperms), whereas Najas, Syringodium (both in underwater families of Alismatales s.s.), Dioscoreales and the rest of the monocots have the trans-spliced intron (Qiu & Palmer, 1998). Araceae are either sister to Alismatales s.s. (Chase et al., 1993, 1995; Duvall et al., 1993a; Hahn, 1998; Ka¨ llersjo¨ et al., 1998; Kubitzki et al., 1998) or Acorus, Araceae and Alismatales s.s. form a grade (Duvall et al., 1995; Nadot et al., 1995; Stevenson et al., 2000). Distinctiveness of Acorus

Acorus was traditionally included in Araceae because of their similar inflorescences and flowers. However, it was removed from Araceae as a separate family even before the molecular era by Grayum (1987) based on structural features. Earlier reports of major differences from Araceae were by van Tieghem (1867) based on vegetative anatomy, by Ju¨ ssen (1928) based on ovule development, and by Tillich (1985) based on seedling morphology. Delpino (1903) placed Acorus not in Araceae but with Tofieldia (Tofieldiaceae), because both have equitant leaves. Grayum (1987) listed 16 mainly structural features distinguishing Acorus from Araceae; Mayo, Bogner & Boyce (1995) listed 13 characters. To this list can be added, based on the present

48

A. IGERSHEIM ET AL.

studies: upper part of pollen tube transmitting tract postgenitally fused (angiospermy type 3 vs. unfused type 1 in Araceae); presence of (superficial) ethereal oil cells in the carpel wall (in Acorus gramineus) (vs. absence in Araceae); absence of raphides not only in the vegetative parts but also in the carpels (vs. presence in Araceae). In addition, floral development is unidirectional in Acorus (vs. regular in Araceae), and the ovary elongates only shortly before anthesis (vs. more continuously in Araceae) (Buzgo, 1999).

Similarities between Acorus and Araceae

In spite of the differences between Acorus and Araceae, which have been emphasized in the past 15 years, as discussed above, they share many special structural traits. Structurally the closest family to Acoraceae is still Araceae, as seen from the present study and from earlier studies. Spadices with densely arranged flowers with five trimerous whorls, apparently without subtending bracts, occur in Acorus and Araceae p.p. (Buzgo, 1999). The gynoecium of Acorus is similar to that of, e.g. Pothos: it is pronouncedly syncarpous with a compitum, it has a punctiform stigma, which often secretes considerable liquid. The pollen tube transmitting tract is lined by upwards directed papillae. The locules are dorsally bulged up and are full of mucilage, which is produced by hairs around the placenta. The ovary septa are exceedingly thin. Acorus and some Araceae have no dorsal vascular bundles in the carpels (Eyde et al., 1967). The ovules are orthotropous, apical, pendant in Acorus and some Araceae. Present in Acorus and Araceae p.p. (but rare in other Alismatales) are: oxalate druses in the carpel (oxalate druses are common in dicots but relatively rare in monocots, except for some basal groups; Prychid & Rudall, 1999); in addition, according to Prychid & Rudall (1999), Acorus and Araceae are the only monocots where the combined presence of calcium oxalate druses and styloids has been recorded. A septal nectary is absent. Further special similarities include: form-P2c plastids in Acorus and part of Araceae (incl. Lemnaceae) (Behnke, 1995), monosulcate, psilate and foveolate pollen in Acorus and basal Araceae (Grayum, 1992), and a basic chromosome number of x=12 in Acorus, Gymnostachys and Pothoideae (Mayo et al., 1997).

Similarities between Acorus, Araceae and Alismatales s.s.

External similarities between Acoraceae, some basal Araceae and those families of Alismatales s.s. with spicate inflorescences, especially Potamogetonaceae and Juncaginaceae, are striking (although they may partly be based on convergences) but there are also

some special anatomical and histological common features (Engler, 1892; Mayo et al., 1995; Buzgo, 1999). Mayo et al. (1995) listed 19 shared characters between Araceae and Alismatales s.s. They share more or less spadix-like inflorescences with small greenish flowers with the perianth in two trimerous or dimerous whorls of tepals, and protogynous flowers (Acorus; Buzgo, 1999; Araceae; Koschewnikoff, 1877; Campbell, 1900; Daumann, 1931b; Croat, 1980; Pellmyr & Patt, 1986; Triglochin, Juncaginaceae; Endress, 1995; Potamogeton; Daumann, 1963; Teryokhin et al., 1997; Groenlandia; Guo & Cook, 1990; both Potamogetonaceae; Tofieldia, Tofieldiaceae; Loew & Kirchner, 1934; and Zostera, Zosteraceae; De Cock, 1981; SorosPottruff & Posluszny, 1995). However, petaliferous Alismatales s.s. tend to be protandrous (Baldellia californica, Alismataceae; Vuille, 1987; Butomus, Butomaceae; Pohl, 1935; Cook, 1998a; Ottelia, Hydrocharitaceae; Islam, 1950; also Posidonia, Posidoniaceae, without a perianth; McConchie & Knox, 1989). Secretory hairs around the placentae occur in various monocots (Rudall et al., 1998), especially in basal monocots: apart from Acoraceae and many Araceae, they are also present in some Alismatales s.s. (Juncaginaceae; this study; Najadaceae; Vijayaraghavan & Kapoor, 1980). Various forms of diffuse placentae, pseudocrassinucellar ovules with distinct funicles, and intercellular cavities in the carpel wall are common. Other shared features are also noteworthy. Laticifers are present in vegetative organs in part of the Araceae (Engler, 1884; Mayo et al., 1997) and Alismatales s.s. (Alismataceae, Limnocharitaceae, Aponogetonaceae, Juncaginaceae, but not in Butomaceae, Hydrocharitaceae, Scheuchzeriaceae, Juncaginaceae, Potamogetonaceae, Posidoniaceae, Najadaceae, Triuridaceae (Ancibor, 1979; Tomlinson, 1982); laticifers occur otherwise very scattered in monocots and are not reported from Acoraceae (Dahlgren et al., 1985). Oxalate raphides, otherwise common in monocots, are absent in Alismatales s.s. and Acoraceae (Prychid & Rudall, 1999). Postament formation (i.e. columnar tissue differentiation in the nucellus base around which the base of the mature embryo sac forms a collarlike extension) has been reported from the nucelli of Acoraceae (Mu¨ cke, 1908; Buell, 1938; Dahlgren, 1940), Arisaema (Araceae) (Pickett, 1913) and Zostera (Zosteraceae) (Dahlgren, 1939, 1940). Successive microsporogenesis is present in Acoraceae and many Alismatales (Furness & Rudall, 1999, 2000).

Relationships within Alismatales s.s.

Based on rbcL analysis, Alismatales s.s. consist of two clades: (1) (Alismataceae, with Limnocharitaceae nested in it)+(Butomaceae+Hydrocharitaceae, with

GYNOECIUM IN BASAL MONOCOTS

Najadaceae nested in the latter), and (2) (Scheuchzeriaceae (Aponogetonaceae (Juncaginaceae (subaquatic families (Zosteraceae+Potamogetonaceae, with Zannichelliaceae nested in the latter)))) (Les, Cleland & Waycott, 1997). There is support for this topology from gynoecium structure. The first clade is characterized by angiospermy type 2 and, for the syncarpous Hydrocharitaceae, angiospermy type 1. In the second clade, the basal families have also type 2 but the more derived families studied here (Juncaginaceae and Potamogetonaceae) have type 4. Alismataceae and Limnocharitaceae are especially similar. They share septal nectaries, angiospermy type 2, laticifers in the ovary wall, pseudocrassinucellar to tenuinucellar, and campylotropous ovules with a distinct funicle, and both integuments only two cell layers thick. The close relationship of Najadaceae with Hydrocharitaceae as suggested by seed structure (ShafferFehre, 1991), and molecular studies (Les, Garwin & Wimpee, 1993; Les & Haynes, 1995; Tanaka et al., 1997) may also be supported by gynoecium structure (very thin ovary wall, strong secretion in the locule).

49

wall is greatly bulged out on the dorsal side so that it covers the single, basal, median ovule like a helmet and the ventral carpel side remains very short. The carpels are largely plicate at anthesis, but they are clearly ascidiate in early development (Eckardt, 1957; Ru¨ bsamen-Weustenfeld, 1991). Both families share the tendency to form numerous small carpels and reach the highest numbers in basal monocots (3–660 in Alismataceae; 6–80 in Triuridaceae), and if numerous they tend to be irregularly arranged. Lacandonia (Triuridaceae) has flowers with a reversed position of androecium and gynoecium. For this unique trait it has been put in a family of its own, Lacandoniaceae (Ma´ rquez-Guzma´ n et al., 1989; Mart´ınez & Ramos, 1989; Va´ zquez-Santana et al., 1998), and the developmental mechanism of these inside-out flowers is under study (Vergara et al., 1999). The fact that in Echinodorus (Alismataceae), flowers have been also found with stamens occurring within the gynoecium (Sattler & Singh, 1978) may further support the close relationship between Triuridaceae and Alismataceae and suggest a shared peculiar floral developmental mechanism in these families with a tendency to give up the otherwise strict sequence stamens-carpels.

Tofieldiaceae and Alismatales s.s.

Tofieldia (incl. Pleea), traditionally included in Liliales (e.g. Cronquist, 1988), appears in Alismatales in Chase et al. (1993, 1995), and this is supported by Kubitzki et al. (1998), Chase et al. (2000), and Fuse & Tamura (2000). A basal position of Tofieldia (or Melanthiaceae where Tofieldia was classified earlier; Dahlgren et al., 1985) in monocots was also assumed by Walker (1986) and Thorne (1992). A special feature in floral structure supporting this view is frequent double position of stamens (Leinfellner, 1962; Utech, 1978) as in Butomaceae and Alismataceae but unlike other Liliiflorae or monocots in general. The carpels are free (only postgenitally united), which is common in Alismatales s.s. but not in other monocots. The endosperm is helobial as in Alismatales s.s. but less so in Liliiflorae (Seelieb, 1924; Ono, 1929). Triuridaceae and Alismatales s.s.

A position of Triuridaceae in Alismatales s.s. was suggested by Engler (1892). However, more recent authors emphasized their isolated position between Alismatales s.s. and Liliiflorae (e.g. Tomlinson, 1982; Dahlgren et al., 1985; Cronquist, 1988; Ru¨ bsamenWeustenfeld, 1991; Thorne, 1992; Takhtajan, 1997). Because of their achlorophyllous habit, molecular systematic studies are inconclusive as yet. A single gene study (18S) places Triuridaceae with Pandanales (Chase et al., 2000). Carpels are reminiscent of Alismataceae. The ovary

Monocots and basal angiosperms

As mentioned above, molecular analyses support monocots as a monophyletic group. However, the branching region of the monocots from basal angiosperms is poorly resolved. This is also reflected by various premolecular hypotheses, which identified different groups of magnoliids as potential precursor clades of monocots, interestingly all from the paleoherbs, a group named by Donoghue & Doyle (1989a,b), comprising Nymphaeales, Piperales, Aristolochiales, and monocots. Dahlgren et al. (1985) also emphasized the close relationships between Nymphaeales and Piperales. At present, paleoherbs are recognized to be polyphyletic and to consist of two clades (monocots not considered): Nymphaeales and Piperales (incl. Aristolochiales) (APG, 1998). Other potential sister groups of monocots are Chloranthaceae (Mathews & Donoghue, 1999; Soltis et al., 2000) (which also show some structural similarities with Piperales), Austrobaileyales (Barkman et al., 2000), and Ceratophyllaceae (Qiu et al., 1999, Graham & Olmstead, 2000). Features that tie paleoherbs and monocots together, as emphasized by earlier authors, are: (1) a single (sometimes adaxial) prophyll instead of two lateral ones (Piperales incl. Aristolochiales, many monocots); (2) presence of ethereal oil cells in Piperales and Acorus; (3) double position of stamens (Saururaceae, Aristolochiaceae, Nymphaeaceae, some Alismatales

50

A. IGERSHEIM ET AL.

s.s.); (4) helobial endosperm (some Nymphaeaceae, many monocots); (5) monosulcate pollen (some Nymphaeaceae, Piperales, incl. Aristolochiales, many monocots); (6) successive pollen meiosis (Aristolochiaceae, many monocots). The different groups of paleoherbs should be discussed separately, especially, as paleoherbs are not monophyletic. Different apparent connections between paleoherbs and monocots seem to be based on convergence due to similar biological syndromes (Chase et al., 1995; Endress, 1995). They have led some earlier authors to the assumption that monocots are polyphyletic (Lotsy, 1911; Suessenguth, 1921; Huber, 1969). Alismatales s.s. were thought to be most closely related with Nymphaeales, and phylogenetically derived from them, since Delpino (1880, 1896) and Hallier (1905) (see also Cronquist, 1988), with Butomaceae, Alismataceae or Hydrocharitaceae basal. Nymphaeales are sister to Alismatales in a morphological analysis by Loconte & Stevenson (1991), in a combined rRNA and morphological analysis by Doyle et al., 1994), and in a morphological analysis by Doyle & Endress (2000). Monosulcate pollen occurs in Butomaceae (Chanda, Nilsson & Blackmore, 1988), as in some Nymphaeaceae (Walker, 1976). Special gynoecial features present in both orders are: (1) laminar-diffuse placenta; (2) strong secretion in the locules (concomitant with aquatic habit); (3) slits between carpels in syncarpous gynoecia (Troll, 1931); (4) uniseriatemulticellular stigmatic papillae (Igersheim & Endress, 1998); (5) helobial endosperm (Schnarf, 1925); formation of an operculum in seeds (Boesewinkel & Bouman, 1984). However, in most recent molecular analyses, Nymphaeales are not sister to monocots (e.g. Les & Schneider, 1995; Qiu et al., 1999; Chase et al., 2000; Duvall, 2000). Aristolochiales were also hypothesized to be the closest relatives of monocots, especially Dioscoreales (Dahlgren & Clifford, 1982; Dahlgren & Bremer, 1985; Dahlgren et al., 1985; Stevenson & Loconte, 1995; Loconte, 1996), or also Alismatales s.s. (Erbar & Leins, 1994). In a combined analysis based on rbcL and nonmolecular features Aristolochiales and monocots came out as sister groups (Nandi, Chase & Endress, 1998). Trichopus (Trichopodaceae, Dioscoreales) was originally classified in Aristolochiaceae (Lindley, 1832) because of striking superficial similarity in habit and floral structure. However, Trichopodaceae seem to be relatively specialized among Dioscoreales (Huber, 1998b). Special features that Aristolochiales have in common with monocots are: type P2c sieve tube plastids (only known from basal Aristolochiaceae outside of monocots (Behnke, 1981, 1991, 2000); with regard to gynoecium structure: (1) septal slits are

present in the syncarpous ovary of Saruma (Aristolochiaceae) (Igersheim & Endress, 1998), as in some Hydrocharitaceae; (2) uniseriate-pluricellular stigmatic hairs are present in some Aristolochiaceae (Igersheim & Endress, 1998), as in Butomus; (3) ovules have thin outer integuments (only two cell layers thick) in Aristolochiaceae (Igersheim & Endress, 1998), as in many monocots (Bouman, 1984). It seems that if any particular extant clade of basal angiosperms were especially close to monocots, it would be Saururaceae and Piperaceae (Piperales s.s.), based on structural features (see Tucker & Douglas, 1996). This is in part also reflected in molecular analyses. In Bharathan & Zimmer (1995), based on partial 18s rDNA, Acorus is linked with Piperales s.s. (either nested within or sister to them). In Duvall (2000), based on a four gene analysis from all three genomes, Piperales (incl. Aristolochiales) is sister to monocots, though weakly supported. The same result was obtained in a combined morphological and molecular analysis (based on the three gene analysis by Soltis et al., 2000) by Doyle & Endress (2000). The great superficial similarity of inflorescences and flowers was already mentioned above. Piperaceae were seen as most closely related to monocots due to seedling structure (Hill, 1906). Lotsy (1911) supposed two origins of monocots, one from Piperales s.s. to Araceae (and some other groups), and one from Proranales (i.e. ancestors of magnoliids) to Alismatales s.s. (and the bulk of the monocots). The claim of earlier authors that in basal monocots (incl. Acorus) vessels are present only in roots has been shown to be incorrect; they have vessels with scalariform perforations in the shoot (Carlquist & Schneider, 1997, 1998; Schneider & Carlquist, 1997; 1998). Carlquist, Dauer & Nishimura (1995) recorded for Saururaceae also primitive vessels with scalariform perforations in the shoot and reduced cambial activity (though still present). They also emphasized sympodial growth in Piperales and basal monocots. Double stamen position is present in Saururaceae (Tucker & Douglas, 1996) and some Alismatales s.s. Monosulcate pollen occurs in Saururaceae, Piperaceae and Saruma (Aristolochiaceae) as well as in Acorus and basal Araceae (Walker, 1976; Grayum, 1992). Protogynous flowers are present in practically all basal angiosperms (magnoliids), but also in Acorus, Araceae and those Alismatales s.s. with spicate inflorescences (see above). Leaf sheaths with ligules are present in Piperales and Araceae (Roth, 1949; Weberling, 1970). The relationships between near exhaustion of the vegetative apex with the formation of each leaf and distichous phyllotaxis, as it is present in Piperales and many monocots should be further explored (e.g. Hagemann, 1960; Schu¨ epp, 1966). In gynoecium structure there are also especially

GYNOECIUM IN BASAL MONOCOTS

many features in common between Piperales and basal monocots; (1) in Piperales and Acorus the carpels are postgenitally fused (angiospermy type 3 or 4) (Igersheim & Endress, 1998); (2) it has long been known that Acorus has ethereal oil cells in vegetative organs, as many basal angiosperms (von Schantz, 1958); ethereal oils are also known from rhizomes of a few Araceae but not in special oil cells (Mayo et al., 1997); a striking finding of this study is the occurrence of oil cells at the surface of carpel walls, probably intrusive, in Acorus gramineus, a feature that we have found to be so prominent in Piperales but otherwise rare in basal angiosperms; it also occurs in Illiciales, Trimeniaceae and Chloranthaceae (Endress & Igersheim, 1997, 2000; Igersheim & Endress, 1997, 1998); (3) orthotropous ovules are characteristic for Piperales s.s., Acorus, and many Araceae; (4) integuments are convoluted in Acorus as in some Piperales and Chloranthaceae (Endress & Igersheim, 1997; Igersheim & Endress, 1998); (5) thin (only two cell-layered) outer integuments occur in many monocots (Bouman, 1984) and are common in Piperales (Igersheim & Endress, 1998); (6) nearly tenuinucellar (pseudocrassinucellar and weakly crassinucellar) ovules are common in basal monocots and do also occur in Saururaceae (Igersheim & Endress, 1998); (7) endosperm is cellular in many Piperaceae and in Acorus and Araceae (Huber, 1977); (8) a perisperm is present in Acorus (Mu¨ cke, 1908; Buell, 1938; Visayenskaya, 1985), but also in Piperales; it was, however, noted that the perisperm is not homologous in the two groups, because in Acorus starch is restricted to the epidermis, whereas it is subepidermal in other taxa (Rudall & Furness, 1997); this is open for discussion. Although convergent evolutionary trends may account for part of the similarities between Piperales and basal monocots (e.g. Dahlgren & Clifford, 1981), they may have arisen from a common ancestor, which had a disposition to develop these similarities in the two lineages. At any rate, there are many common features in Acorus and Piperales so that this relationship has to be further explored.

ACKNOWLEDGEMENTS We thank C. D. K. Cook and H. Maas for providing valuable plant material, and B. P. M. Hyland for support in the field in North Queensland. J. A. Doyle, C. D. K. Cook, and Y.-L. Qiu provided information in many discussions, for which we are grateful. We thank E. M. Friis for critically reading the manuscript. We are indebted to R. Siegrist for skillful microtome work and U. Jauch for support with the SEM. This study is part of a project of P.K.E. financed by the Swiss National Foundation (Nr. 3100-040327.94).

51

REFERENCES Afzelius K. 1920. Einige Beobachtungen u¨ ber die Samenentwicklung der Aponogetonaceae. Svensk Botanisk Tidskrift 14: 168–175. Agrawal JS. 1952. The embryology of Lilaea subulata H.B.K. with a discussion on its systematic position. Phytomorphology 2: 15–29. Al-Shehbaz IA, Schubert BG. 1989. The Dioscoreaceae in the Southeastern United States. Journal of the Arnold Arboretum 70: 57–95. Ancibor H. 1979. Systematic anatomy of vegetative organs of the Hydrocharitaceae. Botanical Journal of the Linnean Society 78: 237–266. APG (The Angiosperm Phylogeny Group) 1998. An ordinal classification for the families of flowering plants. Annals of the Missouri Botanical Garden 85: 531–553. Apparao BJ, Shah CK. 1989. Intracarpellary secretory cells and their role in Ottelia alismoides. Journal of the Indian Botanical Society 68: 25–28. Arber A. 1940. Studies in flower structure: VI. On the residual vascular tissue in the apices of reproductive shoots, with special reference to Lilaea and Amherstia. Annals of Botany 2: 617–627. Aston H. 1973. Aquatic plants of Australia. Melbourne: Melbourne University Press. Baillon H. 1878. Traite´ du de´ veloppement de la fleur et du fruit (suite). XI. Hydrocharide´ es. XII. Garryace´ es. XIII. Loranthe´ es. Adansonia 12: 255–282. Baillon H. 1892. Sur la direction des ovules des Alisma. Bulletin Mensuel de la Socie´ te´ Linne´ enne de Paris 132: 1050–1051. Banerji I. 1947. Life history of Typhonium trilobatum. Proceedings of the National Institute of Science of India B 13: 207–230. Barabe´ D. 1982. Vascularisation de la fleur de Symplocarpus foetidus (Araceae). Canadian Journal of Botany 60: 1536– 1544. Barabe´ D, Bertrand C. 1996. Organoge´ nie florale des genres Culcasia et Cercestis (Araceae). Canadian Journal of Botany 74: 898–908. Barabe´ D, Chre´ tien L. 1985. Anatomie florale de Spathicarpa sagittifolia (Araceae). Beitra¨ ge zur Biologie der Pflanzen 60: 403–412. Barabe´ D, Chre´ tien L. 1986. Vascularisation de la fleur de Spathiphyllum wallisii. Canadian Journal of Botany 64: 1397–1401. Barabe´ D, Chre´ tien L, Forget S. 1986. Vascularisation de la fleur pistille´ e d’Anchomanes difformis Engl. Feddes Repertorium 97: 831–835. Barabe´ D, Chre´ tien L, Forget S. 1987a. On the pseudomonomerous gynoecia of the Araceae. Phytomorphology 37: 139–143. Barabe´ D, Forget S. 1988a. Anatomie florale de l’Aglaonema pictum (Araceae). Beitra¨ ge zur Biologie der Pflanzen 63: 453–462. Barabe´ D, Forget S. 1988b. Anatomie des fleurs fertiles et steriles de Zamioculcas (Araceae). Bulletin du Muse´ um National d’Histoire Naturelle, B, Adansonia 10: 411–419.

52

A. IGERSHEIM ET AL.

Barabe´ D, Forget S. 1993. Anatomie florale des Culcasia (Araceae). Bulletin du Muse´ um National d’Histoire Naturelle, Paris, Se´ r. 4, B, Adansonia 14: 263–278. Barabe´ D, Forget S, Chre´ tien L. 1987b. Organoge´ ne`se de la fleur de Symplocarpus foetidus (Araceae). Canadian Journal of Botany 65: 446–455. Barabe´ D, Labrecque M. 1983. Vascularisation de la fleur de Calla palustris (Araceae). Canadian Journal of Botany 61: 1718–1726. Barabe´ D, Labrecque M. 1984. Vascularisation de la fleur de Lysichitum camtschatcense (Araceae). Canadian Journal of Botany 62: 1971–1983. Barabe´ D, Labrecque M. 1985. Vascularisation de la fleur d’Orontium aquaticum L. (Arace´ es). Bulletin de la Socie´ te´ Botanique de France, Lettres Botaniques 132: 133–145. Barabe´ D, Labrecque M, Chre´ tien L. 1984. Vascularisation de la fleur d’Anthurium lhotzkyanum (Araceae). Comptes Rendus de l’Acade´ mie des Sciences Paris, Se´ r. III 299: 651–656. Barahona Carvajal ME. 1978. Estudio morfolo´ gico comparativo de las inflorescencias de dos especies de Araceae: Anthurium denudatum Engler y Philodendron radiatum Schott. Revista de Biologia Tropical 25: 301–333. Barkman TJ, Chenery G, McNeal JR, Lyons-Weiler J, dePamphilis CW. 2000. Independent and combined analysis of sequences from all three genomic compartments converge on the root of flowering plant phylogeny. Proceedings of the National Academy of Sciences USA 97: 13166–13171. Baude E. 1956. Die Embryoentwicklung von Stratiotes aloides L. Planta 46: 649–671. ¨ ber die postgenitale Verwachsung in KarBaum H. 1948. U ¨ sterreichische Botanische Zeitschrift 95: 86–94. pellen. O Behnke H-D. 1981. Siebelement-Plastiden, Phloem-Protein und Evolution der Blu¨ tenpflanzen: II. Monokotyledonen. Berichte der Deutschen Botanischen Gesellschaft 94: 647– 662. Behnke H-D. 1991. Distribution and evolution of forms and types of sieve-element plastids in the dicotyledons. Aliso 13: 167–182. Behnke H-D. 1995. P-type sieve-element plastids and the systematics of the Arales (sensu Cronquist 1988) – with Stype plastids in Pistia. Plant Systematics and Evolution 195: 87–119. Behnke H-D. 2000. Forms and sizes of sieve-element plastids and evolution of the monocotyledons. In: Wilson KL, Morrison DA, eds. Monocots: systematics and evolution. Collingwood, Victoria: CSIRO Publishing, 163–188. Bessey EA. 1898. The comparative morphology of the pistils of the Ranunculaceae, Alismaceae and Rosaceae. Botanical Gazette 26: 297–314. Bharathan G, Zimmer EA. 1995. Early branching events in monocotyledons, partial 18S ribosomal DNA sequence analysis. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ, eds. Monocotyledons: systematics and evolution 1. Kew, Royal Botanic Gardens, 81–107. Boesewinkel FD, Bouman F. 1984. The seed: structure. In: Johri BM, ed. Embryology of angiosperms. Berlin: Springer, 567–610.

Bo¨ hmker H. 1917. Beitra¨ ge zur Kenntnis der floralen und extrafloralen Nektarien. Beihefte zum Botanischen Centralblatt, Sect. 1 33: 169–247. Bornet E. 1864. Recherches sur le Phycagrostis major Cavol. Annales des Sciences Naturelles, Botanique, Se´ rie 5 1: 5–51. Boubes C, Barabe´ D. 1996. De´ veloppement de l’inflorescence et des fleurs du Philodendron acutatum Schott (Araceae). Canadian Journal of Botany 74: 909–918. Boubes C, Barabe´ D. 1997. Flower and inflorescence development in Montrichardia arborescens (Araceae). International Journal of Plant Sciences 158: 408–417. Bouman F. 1984. The ovule. In: Johri BM, ed. Embryology of angiosperms. Heidelberg: Springer, 123–157. Bouman F. 1985. Embryology. In: van Bruggen HWE, ed. Monograph of the genus Aponogeton (Aponogetonaceae). Bibliotheca Botanica 137: 4–9. Bouman F, Boesewinkel FD. 1991. The campylotropous ovules and seeds, their structure and functions. Botanische Jahrbu¨ cher fu¨ r Systematik 113: 255–270. Bremer K. 2000. Early Cretaceous lineages of monocot flowering plants. Proceedings of the National Academy of Sciences USA 97: 4707–4711. Brown WH. 1938. The bearing of nectaries on the phylogeny of flowering plants. Proceedings of the American Philosophical Society 79: 549–594. ¨ ber die Blu¨ thenentwicklung von AlBuchenau F. 1857. U isma und Butomus. Flora 40: 241–256. ¨ ber die Richtung der Samenknospe bei Buchenau F. 1869. U den Alismaceen. Jahrbu¨ cher fu¨ r Wissenschaftliche Botanik 7: 19–33. Buell MF. 1938. Embryogeny of Acorus calamus. Botanical Gazette 99: 556–568. Burger WC. 1977. The Piperales and the monocots. Alternative hypotheses for the origin of monocotyledonous flowers. Botanical Review 43: 345–393. Burkill IH. 1960. The organography and the evolution of Dioscoreaceae. Botanical Journal of the Linnean Society 56: 319–412. Burr HG. 1903. The embryology of Vallisneria spiralis. Ohio Naturalist 3: 439–443. Buzgo M. 1994. Inflorescence development of Pistia stratiotes (Araceae). Botanische Jahrbu¨ cher fu¨ r Systematik 115: 557– 570. Buzgo M. 1999. Flower structure and development of Acoraceae and basal Araceae and their systematic position among basal monocotyledons. Unpublished D. Phil. Thesis, University of Zurich. Buzgo M, Endress PK. 2000. Floral structure and development of Acoraceae and its systematic relationships with basal angiosperms. International Journal of Plant Sciences 161: 23–41. Caldwell OW. 1899. The life-history of Lemna minor. Botanical Gazette 27: 37–66. Campbell DH. 1897. A morphological study of Najas and Zannichellia. Proceedings of the California Academy of Sciences, Ser. 3, Bot 1: 1–66. Campbell DH. 1898. Development of the flower and embryo of Lilaea subulata H.B.K. Annals of Botany 12: 1–12.

GYNOECIUM IN BASAL MONOCOTS Campbell DH. 1899. Notes on the structure of the embryo sac in Sparganium and Lysichiton. Botanical Gazette 27: 153–166. Campbell DH. 1900. Studies on the Araceae. Annals of Botany 14: 1–25. Campbell DH. 1903. Studies on the Araceae 2. The embryo sac and embryo of Aglaonema and Spathicarpa. Annals of Botany 17: 665–687. Campbell DH. 1905. Studies on the Araceae 3. Annals of Botany 19: 329–349. Campbell DH. 1912. The embryo sac of Aglaonema. Scottish Botanical Review 1: 100–115. Capus G. 1879. Anatomie du tissu conducteur. Annales des Sciences Naturelles, Botanique, Se´ r. 6 7: 209–291. Carlquist S, Schneider EL. 1997. Origins and nature of vessels in monocotyledons. I. Acorus. International Journal of Plant Sciences 158: 51–56. Carlquist S, Schneider EL. 1998. Origin and nature of vessels in monocotyledons. 5. Araceae subfamily Colocasioideae. Botanical Journal of the Linnean Society 128: 71–86. Carlquist S, Dauer K, Nishimura SY. 1995. Wood and stem anatomy of Saururaceae with reference to ecology, phylogeny, and origin of the monocotyledons. IAWA Journal 16: 133–150. Caspary R. 1857. Sur l’ovule du Vallisneria spiralis. Bulletin de la Socie´ te´ Botanique de France 4: 904–907. Caspary R. 1858a. Die Hydrilleen (Anacharideen Endl.). Jahrbu¨ cher fu¨ r Wissenschaftliche Botanik 1: 377–513. Caspary R. 1858b. Die Blu¨ the von Elodea canadensis Rich. Botanische Zeitung 42: 313–317. Chanda S, Nilsson S, Blackmore S. 1988. Phylogenetic trends in the Alismatales with reference to pollen grains. Grana 27: 257–272. Charlton WA. 1991. Studies in the Alismataceae. IX. Development of the flower in Ranalisma humile. Canadian Journal of Botany 69: 2790–2796. Charlton WA, Ahmed A. 1973. Studies in the Alismataceae. III. Floral anatomy of Ranalisma humile. Canadian Journal of Botany 51: 891–897. Charlton WA, Posluszny U. 1991. Meristic variation in Potamogeton flowers. Botanical Journal of the Linnean Society 106: 265–293. Chase MW, de Bruijn A, Fay MF, Sullivan S, Rudall PJ, Soltis DE, Soltis PS, Hahn WJ. 1998. A combined analysis of multiple datasets and a new phylogenetic classification of the monocotyledons. Monocots II. Second International Conference on the Comparative Biology of the Monocotyledons. University of New South Wales, Sydney. Abstracts, 14. Chase MW, Soltis DS, Soltis PS, Rudall PJ, Fay MF, Hahn WH, Sullivan S, Molvray M, Kores PJ, Joseph J, Givnish T, Sytsma KJ, Pires JC. 2000. Higher-level systematics of the monocotyledons: an assessment of current knowledge and a new classification. In: Wilson KL, Morrison DA, eds. Monocots: systematics and evolution. Collingwood, Victoria: CSIRO Publishing, 3–16. Chase MW et al. 1993. Phylogenetics of seed plants: an

53

analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 528–580. Chase MW, Stevenson DW, Wilkin P, Rudall PJ. 1995. Monocot systematics: a combined analysis. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ, eds. Monocotyledons: systematics and evolution 2. Kew: Royal Botanic Gardens, 685–730. Chatin GA. 1855. Me´ moire sur le Vallisneria spiralis L., conside´ re´ dans son organographie, sa ve´ ge´ tation, son organoge´ nie, son anatomie, sa te´ ratologie et sa physiologie. Paris: Mallet-Bachelier. Cocucci AE. 1966. Embryology of Synandrospadix vermitoxicus (Araceae). Kurtziana 3: 157–181. Cook CDK. 1985. A revision of the genus Apalanthe. Aquatic Botany 21: 157–164. Cook CDK. 1998a. Butomaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 100–102. Cook CDK. 1998b. Hydrocharitaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 234–248. Cook CDK, Lu ¨ o¨ nd R. 1982a. A revision of the genus Nechamandra (Hydrocharitaceae). Aquatic Botany 13: 505–513. ¨ o¨ nd R. 1982b. A revision of the genus HydroCook CDK, Lu charis (Hydrocharitaceae). Aquatic Botany 14: 177–204. Cook CDK, Lu ¨ o¨ nd R, Nair B. 1981. Floral biology of Blyxa octandra (Roxb.) Planchon ex Thwaites (Hydrocharitaceae). Aquatic Botany 10: 61–68. Cook CDK, Symoens J-J, Urmi-Ko¨ nig K. 1984. A revision of the genus Ottelia (Hydrocharitaceae). I. Generic considerations. Aquatic Botany 18: 263–274. Cook CDK, Urmi-Ko¨ nig K. 1983. A revision of the genus Limnobium including Hydromistria (Hydrocharitaceae). Aquatic Botany 17: 1–27. Cook CDK, Urmi-Ko¨ nig K. 1984a. A revision of the genus Egeria (Hydrocharitaceae). Aquatic Botany 19: 73–96. Cook CDK, Urmi-Ko¨ nig K. 1984b. A revision of the genus Ottelia (Hydrocharitaceae). 2. The species of Eurasia, Australasia and America. Aquatic Botany 20: 131–177. Cook CDK, Urmi-Ko¨ nig K. 1985. A revision of the genus Elodea (Hydrocharitaceae). Aquatic Botany 21: 111–156. Cook MT. 1907. The embryology of Sagittaria lancifolia L. Ohio Naturalist 7: 97–101. Cook MT. 1908. The development of the embryo-sac and embryo of Potamogeton lucens. Bulletin of the Torrey Botanical Club 35: 209–218. Cox PA. 1991. Hydrophilous pollination of a dioecious seagrass, Thalassodendron ciliatum (Cymodoceaceae) in Kenya. Biotropica 23: 159–165. Cox PA, Elmqvist T, Tomlinson PB. 1990. Submarine pollination and reproductive morphology in Syringodium filiforme (Cymodoceaceae). Biotropica 22: 259–265. Cox PA, Knox RB. 1989. Two-dimensional pollination in hydrophilous plants: convergent evolution in the genera Halodule (Cymodoceaceae), Halophila (Hydrocharitaceae), Ruppia (Ruppiaceae), and Lepilaena (Zannichelliaceae). American Journal of Botany 76: 164–175.

54

A. IGERSHEIM ET AL.

Cox PA, Tomlinson PB. 1988. Pollination ecology of a seagrass, Thalassia testudinum (Hydrocharitaceae), in St. Croix. American Journal of Botany 75: 958–965. Croat TB. 1980. Flowering behavior of the neotropical genus Anthurium (Araceae). American Journal of Botany 67: 888–904. Cronquist A. 1988. The evolution and classification of flowering plants, ed. 2. Bronx: New York Botanical Garden. Daghlian CP. 1981. A review of the fossil record of monocotyledons. Botanical Review 47: 517–555. Dahlgren KVO. 1927. Die Morphologie des Nuzellus mit besonderer Beru¨ cksichtigung der deckzellosen Typen. Jahrbu¨ cher fu¨ r Wissenschaftliche Botanik 67: 347–426. Dahlgren KVO. 1928. Die Embryologie einiger Alismatazeen. Svensk Botanisk Tidskrift 22: 1–17. Dahlgren KVO. 1934. Die Embryosackentwicklung von Echinodorus macrophyllus und Sagittaria sagittifolia. Planta 6: 602–612. Dahlgren KVO. 1939. Endosperm- und Embryobildung bei Zostera marina. Botaniska Notiser 4: 607–615. Dahlgren KVO. 1940. Postamentbildungen in den Embryosa¨ cken der Angiospermen. Botaniska Notiser 5: 347– 369. Dahlgren RMT, Bremer K. 1985. Major clades of the angiosperms. Cladistics 1: 349–368. Dahlgren RMT, Clifford HT. 1981. Some conclusions from a comparative study of the monocotyledons and related dicotyledonous orders. Berichte der Deutschen Botanischen Gesellschaft 94: 203–227. Dahlgren RMT, Clifford HT. 1982. The monocotyledons: a comparative study. London: Academic Press. Dahlgren RMT, Clifford HT, Yeo PF 1985. The families of the monocotyledons. Berlin: Springer. Dahlgren RMT, Rasmussen FN. 1983. Monocotyledon evolution: characters and phylogenetic estimation. Evolutionary Biology 16: 255–395. ¨ ber die Leitung der Pollenschla¨ uche bei Dalmer M. 1880. U den Angiospermen. Jenaische Zeitschrift fu¨ r Naturwissenschaften, n.F 7: 530–566. Daumann E. 1931a. Zur Phylogenie der Diskusbildungen. Beitra¨ ge zur Kenntnis der Nektarien II (Hydrocharis, Sagittaria, Sagina). Beihefte zum Botanischen Centralblatt, Sect. I 48: 183–208. Daumann E. 1931b. Nektarabscheidung in der Blu¨ tenregion einiger Araceen. Zugleich ein Hinweis auf die Bargersche Methode. Planta 12: 38–52. ¨ kologie der Daumann E. 1931c. Zur Morphologie und O Blu¨ te von Stratiotes aloides L. Planta 14: 766–776. Daumann E. 1963. Zur Frage nach dem Ursprung der Hydrogamie. Zugleich ein Beitrag zur Blu¨ teno¨ kologie von Potamogeton. Preslia 35: 23–30. Daumann E. 1964. Zur Morphologie der Blu¨ te von Alisma plantago-aquatica L. Preslia 36: 226–239. Daumann E. 1970. Das Blu¨ tennektarium der Monocotyledonen unter besonderer Beru¨ cksichtigung seiner systematischen und phylogenetischen Bedeutung. Feddes Repertorium 80: 463–590. Davis GL. 1966. Systematic embryology of the angiosperms. New York: Wiley.

Davis JI. 1995. A phylogenetic structure for the monocotyledons, as inferred from chloroplast DNA restriction site variation, and a comparison of measures of clade support. Systematic Botany 20: 503–527. Davis JI, Simmons MP, Stevenson DW, Wendel JF. 1998a. Data decisiveness, data quality, and incongruence in phylogenetic analysis: an example from the monocotyledons using mitochondrial atpA sequences. Systematic Biology 47: 282–310. Davis JI, Stevenson DW, Freudenstein JV, Hardy CR, Simmons MW, Specht CD. 1999. Phylogenetics of the monocotyledons. XVI International Botanical Congress, St. Louis, USA, Abstr., 118. Davis JI, Stevenson DW, Specht CD, Freudenstein JV, DeSalle R. 1998b. A phylogenetic analysis of the monocotyledons, based on morphological and molecular character sets. Monocots II. Second International Conference on the Comparative Biology of the Monocotyledons. University of New South Wales, Sydney. Abstracts, 18. De Cock AWAM. 1980. Flowering, pollination and fruiting in Zostera marina L. Aquatic Botany 9: 201–220. De Cock AWAM. 1981. Development of the flowering shoot of Zostera marina L. under controlled conditions in comparison to the development in two different natural habitats in the Netherlands. Aquatic Botany 10: 99–113. de Cordemoy CJ. 1862. Organoge´ nie des Triglochin. Adansonia 3: 12–15. de Lanessan J-L. 1875. Organoge´ nie de la fleur et du fruit des Zostera marina L. et Z. nana Roth. Rapports des Zostera avec les Gramine´ es. Comptes rendus de la Session de l’Association Franc¸ aise pour l’Avancement des Sciences, Nantes 1875: 690–707. Delpino F. 1880. Contribuzioni alla storia dello sviluppo del regno vegetale. I. Smilacee. Genova: Istituto Sordo-Muti. Delpino F. 1896. Applicazione di nuovi criterii per la classificazione delle piante. Sesta memoria. Memorie della Reale Accademia di Scienze dell’Istituto di Bologna, Serie V 6: 83–116. Delpino F. 1903. Aggiunte alla teoria della classificazione delle Monocotiledoni. Memorie della Reale Accademia di Scienze dell’Instituto di Bologna, Seria V 10: 569–584. Donoghue MJ, Doyle JA. 1989a. Phylogenetic studies of seed plants and angiosperms based on morphological characters. In: Fernholm B, Bremer K, Jo¨ rnvall H, eds. The hierarchy of life. Amsterdam: Excerpta Medica, 181–193. Donoghue MJ, Doyle JA. 1989b. Phylogenetic analysis of angiosperms and the relationships of Hamamelidae. In: Crane PR, Blackmore S, eds. Evolution, systematics, and fossil history of the Hamamelidae, 1: Introduction and ‘Lower’ Hamamelidae. Oxford: Clarendon Press, 17–45. Doyle JA. 1973. Fossil evidence on early evolution of the monocotyledons. The Quarterly Review of Biology 48: 399– 413. Doyle JA. 1998. Phylogeny of vascular plants. Annual Reviews of Ecology and Systematics 29: 567–599. Doyle JA, Biens P, Doerenkamp A, Jardine´ S. 1977. Angiosperm pollen from the pre-Albian Lower Cretaceous of equatorial Africa. Bulletin des Centres de Recherches Exploration-Production Elf-Aquitaine 1: 451–473.

GYNOECIUM IN BASAL MONOCOTS Doyle JA, Donoghue MJ, Zimmer EA. 1994. Integration of morphological and rRNA data on the origin of angiosperms. Annals of the Missouri Botanical Garden 81: 419–450. Doyle JA, Endress PK. 2000. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. International Journal of Plant Sciences 161: S121–S153. Doyle JA, Van Campo M, Lugardon B. 1975. Observations on exine structure of Eucommiidites and Lower Cretaceous angiosperm pollen. Pollen et Spores 17: 429–486. Ducker SC, Knox RB. 1976. Submarine pollination in seagrasses. Nature 263: 705–706. Ducker SC, Pettitt JM, Knox RB. 1978. Biology of Australian seagrasses: pollen development and submarine pollination in Amphibolis antarctica and Thalassodendron ciliatum (Cymodoceaceae). Australian Journal of Botany 26: 265–285. Duvall MR. 2000. Seeking the dicot sister group of the monocots. In: Wilson KL, Morrison DA, eds. Monocots: systematics and evolution. Collingwood, Victoria: CSIRO Publishing, 25–32. Duvall MR, Chase MW, Soltis DE, Clegg MT. 1995. A phylogeny of seed plants resulting from analysis of DNA sequence variation among the rbcL loci of 499 species, with particular emphasis on alliances among monocotyledons. Monographs in Systematic Botany of the Missouri Botanical Garden 53: 27–40. Duvall MR, Clegg MT, Chase MW, Clark WD, Kress WJ, Hills HG, Eguiarte LE, Smith JF, Gaut BS, Zimmer EA, Learn Jr GH. 1993b. Phylogenetic hypotheses for the monocotyledons constructed from rbcL sequence data. Annals of the Missouri Botanical Garden 80: 607– 619. Duvall MR, Learn GH, Eguiarte LE, Clegg MT. 1993a. Phylogenetic analysis of rbcL sequences identifies Acorus calamus as the primal extant monocotyledon. Proceedings of the Academy of Sciences USA 90: 4641–4644. Eames AJ. 1931. The vascular anatomy of the flower with refutation of the theory of carpel polymorphism. American Journal of Botany 18: 147–188. Eames AJ. 1961. Morphology of the angiosperms. New York: McGraw Hill. Eber E. 1934. Karpellbau und Plazentationsverha¨ ltnisse in der Reihe der Helobiae. Mit einem Anhang u¨ ber die verwandtschaftlichen Beziehungen zwischen Ranales und Helobiae. Flora 127: 273–330. Eckardt T. 1937. Untersuchungen u¨ ber die Morphologie, Entwicklungsgeschichte und systematische Bedeutung des pseudomonomeren Gynoeceums. Nova Acta Leopoldina 5: 5–112. Eckardt T. 1957. Vergleichende Studie u¨ ber die morphologischen Beziehungen zwischen Fruchtblatt, Samenanlage und Blu¨ tenachse bei einigen Angiospermen. Neue Hefte zur Morphologie 3: 1–91. Eie S. 1972. Floral anatomy in Tofieldia pusilla (Michx.) Pers. with special reference to the gynoecium. Norwegian Journal of Botany 19: 31–36. El-Hamidi A. 1952. Vergleichend-morphologische Untersuchungen am Gynoeceum der Unterfamilien Me-

55

lanthioideae und Asphodeloideae der Liliaceae. D. Phil. Thesis, University of Zurich. Zurich: Hug & So¨ hne. Endress PK. 1990. Evolution of reproductive structures and functions in primitive angiosperms (Magnoliidae). Memoirs of the New York Botanical Garden 55: 5–34. Endress PK. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge: Cambridge University Press. Endress PK. 1995. Major evolutionary traits of monocot flowers. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ, eds. Monocotyledons: systematics and evolution. Kew: Royal Botanic Gardens, 43–79. Endress PK, Igersheim A. 1997. Gynoecium diversity and systematics of the Laurales. Botanical Journal of the Linnean Society 125: 93–168. Endress PK, Igersheim A. 1999. Gynoecium diversity and systematics of the basal eudicots. Botanical Journal of the Linnean Society 130: 305–393. Endress PK, Igersheim A. 2000. Gynoecium structure and evolution in basal angiosperms. International Journal of Plant Sciences 161: S211–S223. Engler A. 1884. Beitra¨ ge zur Kenntnis der Araceae: V.1,2. ¨ ber den Entwicklungsgang in der Familie der Araceen U und u¨ ber die Blu¨ tenmorphologie derselben. Botanische Jahrbu¨ cher fu¨ r Systematik 5: 141–188, 287–336. Engler A. 1892. Die systematische Anordnung der monokotyledoneen Angiospermen. Abhandlungen der Ko¨ niglichen Akademie der Wissenschaften, PhysikalischMathematische Classe II 1892: 1–55. Engler A. 1920. Araceae. Pars generalis et index familiae generalis. In: Engler A, ed. Das Pflanzenreich IV.23A. Leipzig: Engelmann. Erbar C, Leins P. 1994. Flowers in Magnoliidae and the origin of flowers in other subclasses of the angiosperms. I. The relationships between flowers of Magnoliidae and Alismatidae. Plant Systematics and Evolution, Supplement 8: 193–208. Ernst-Schwarzenbach M. 1951. Die Ursachen der verminderten Fertilita¨ t von Elodea-Arten. Planta 39: 542–569. Eyde RH, Nicolson DH, Sherwin D. 1967. A survey of floral anatomy in Araceae. American Journal of Botany 54: 478–497. Fernando DD, Cass DD. 1996. Development and structure of ovule, embryo sac, embryo, and endosperm in Butomus umbellatus (Butomaceae). International Journal of Plant Sciences 157: 269–279. Fernando DD, Cass DD. 1997. Developmental assessment of sexual reproduction in Butomus umbellatus (Butomaceae): Female reproductive component. Annals of Botany 80: 457–467. Fischer A. 1880. Zur Kenntniss der Embryosackentwicklung einiger Angiospermen. Jenaische Zeitschrift fu¨ r Medizin und Naturwissenschaften, N.F 7: 90–132. French JC. 1986. Ovular vasculature in Araceae. Botanical Gazette 147: 478–495. French JC 1987. Structure of ovular and placental trichomes of Araceae. Botanical Gazette 148: 198–208. French JC, Kressler C. 1989. Molecular systematics of Araceae: are Acorus and Gymnostachys aroids? American Journal of Botany 76: 242.

56

A. IGERSHEIM ET AL.

Frey L. 1966. Embryological studies on Alisma lanceolatum With. Acta Biologica Cracoviensia, Ser. Bot 9: 125–135. Friis EM, Crane PR, Pedersen KR. 1997. Anacostia, a new basal angiosperm from the Early Cretaceous of North America and Portugal with trichotomocolpate/monocolpate pollen. Grana 36: 225–244. Friis EM, Pedersen KR, Crane PR. 1999. Early angiosperm diversification: the diversity of pollen associated with angiosperm reproductive structures in early Cretaceous floras from Portugal. Annals of the Missouri Botanical Garden 86: 259–296. Furness CA, Rudall PJ. 1999. Microsporogenesis in monocotyledons. Annals of Botany 84: 475–499. Furness CA, Rudall PJ. 2000. The systematic significance of simultaneous cytokinesis during microsporogenesis in monocotyledons. In: Wilson KL, Morrison DA, eds. Monocots: systematics and evolution. Collingwood, Victoria: CSIRO Publishing, 189–193. Fuse S, Tamura MN. 2000. A phylogenetic analysis of the plastid matK gene with emphasis on Melanthiaceae sensu lato. Plant Biology 2: 415–427. Gamerro JC. 1968. Observaciones sobre la biologı´a floral y morfologı´a de la Potamogetona´ cea Ruppia cirrhosa (Petag.) Grand (=R. spiralis L. ex Dum.). Darwiniana 14: 575–607. Gandolfo MA, Daghlian CP. 1999. New fossil evidence on the history of monocotyledons. XVI International Botanical Congress, St. Louis, USA, Abstracts, 200. Gandolfo MA, Nixon KC, Crepet WL. 2000. Monocotyledons: a review of their Early Cretaceous record. In: Wilson KL, Morrison DA, eds. Monocots: systematics and evolution. Collingwood, Victoria: CSIRO Publishing, 44–51. Gandolfo MA, Nixon KC, Crepet WL, Stevenson DW, Friis EM. 1998. Oldest known fossils of monocotyledons. Nature 394: 532–533. Gasser CS, Broadhvest J, Hauser BA. 1998. Genetic analysis of ovule development. Annual Reviews in Plant Physiology and Plant Molecular Biology 49: 1–24. Gatin VC. 1920. Recherches anatomiques sur le pe´ doncule et la fleur des Liliace´ es. Revue Ge´ ne´ rale de Botanique 32: 369–437, 460–528, 561–591. Gerlach D. 1984. Botanische Mikrotechnik. Thieme, Stuttgart. Goebel K. 1897. Morphologische und biologische Bemerkungen. Flora 83: 426–435. Goldberg B. 1941. Life history of Peltandra virginica. Botanical Gazette 102: 641–662. Govindappa DA, Naidu TRB. 1956. The embryo sac and endosperm of Blyxa oryzetorum. Journal of the Indian Botanical Society 35: 417–422. Gow JH. 1907. Morphology of Spathyema foetida. Botanical Gazette 43: 131–136. Gow JH. 1908. Studies in the Araceae. Botanical Gazette 46: 35–42. Gow JH. 1913. Observations on the morphology of the aroids. Botanical Gazette 56: 127–132. Graham SW, Olmstead RG. 2000. Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. American Journal of Botany 87: 1712–1730.

Graves AH. 1908. The morphology of Ruppia maritima. Transactions of the Connecticut Academy of Arts and Sciences 14: 59–170. Grayum MH. 1987. A summary of evidence and arguments supporting the removal of Acorus from the Araceae. Taxon 36: 723–729. Grayum MH. 1990. Evolution and phylogeny of the Araceae. Annals of the Missouri Botanical Garden 77: 628–697. Grayum MH. 1991. Systematic embryology of the Araceae. Botanical Reviews 57: 167–203. Grayum MH. 1992. Comparative external pollen ultrastructure of the Araceae and putatively related taxa. Monographs in Systematic Botany from the Missouri Botanical Garden 43: 1–167. Gre´ goire V. 1938. La morphoge´ ne`se et l’autonomie morphologique de l’appareil floral. La Cellule 47: 287–452. Gue´ guen F. 1901. Anatomie compare´ e du tissu conducteur du style et du stigmate des Phane´ rogames. I. Monocotyle´ dones, Ape´ tales et Gamope´ tales. Paris: Mersch. Guignard L. 1901. La double fe´ condation dans le Najas major. Journal de Botanique 15: 205–213. Guo Y-H, Cook CDK. 1990. The floral biology of Groenlandia densa (L.) Fourreau (Potamogetonaceae). Aquatic Botany 38: 283–288. Gupta BL. 1934. A contribution to the life history of Potamogeton crispus L. Journal of the Indian Botanical Society 13: 51–65. Gupta BL. 1935. Studies in the development of the pollen grain and embryo sac of Wolffia arrhiza. Current Science 4: 104–105. Hagemann W. 1960. Kritische Untersuchungen u¨ ber die ¨ sOrganisation des Sprosscheitels dikotyler Pflanzen. O terreichische Botanische Zeitschrift 107: 366–402. Hahn WJ. 1998. Comparative chloroplast and nuclear molecular phylogenetics of the monocots. Second International Conference on the Comparative Biology of the Monocotyledons. University of New South Wales, Sydney. Abstracts, 25. Hakansson A. 1921. Beitra¨ ge zur Entwicklungsgeschichte der Taccaceen. Botaniska Notiser 1921: 189–220, 257–268. Hall JG. 1902. An embryological study of Limnocharis emarginata. Botanical Gazette 33: 214–219. Hallier H. 1905. Ein zweiter Entwurf des natu¨ rlichen (phylogenetischen) Systems der Blu¨ tenpflanzen. Vorla¨ ufige Mitteilung. Berichte der Deutschen Botanischen Gesellschaft 23: 85–91. Haynes RR, Holm-Nielsen LB, Les DH. 1998a. Najadaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 301–306. Haynes RR, Holm-Nielsen LB, Les DH. 1998b. Ruppiaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 301–306. Haynes RR, Les DH, Holm-Nielsen LB. 1998c. Alismataceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 11–18. Haynes RR, Les DH, Holm-Nielsen LB. 1998d. Juncaginaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 260–263.

GYNOECIUM IN BASAL MONOCOTS Haynes RR, Les DH, Holm-Nielsen LB. 1998e. Limnocharitaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 271–275. Haynes RR, Les DH, Holm-Nielsen LB. 1998f. Potamogetonaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 408–415. Haynes RR, Les DH, Holm-Nielsen LB. 1998g. Scheuchzeriaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 449–451. Haynes RR, Les DH, Holm-Nielsen LB. 1998h. Zannichelliaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 470–474. Hegelmaier F. 1868. Die Lemnaceen. Eine monographische Untersuchung. Leipzig: Engelmann. ¨ ber die Entwicklung der Blu¨ thenHegelmaier F. 1870. U theile von Potamogeton. Botanische Zeitung 28: 281–289, 297–305, 313–319. ¨ ber die Fructifikationstheile von SpiHegelmaier F. 1871. U rodela. Botanische Zeitung 29: 625–666. ¨ ber die Anlegung des Karpells von PoHelm J. 1934. U tamogeton trichoides Cham. et Schlecht. Planta 22: 443– 444. Herendeen PS, Crane PR. 1995. The fossil history of the monocotyledons. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ, eds. Monocotyledons: systematics and evolution. Kew: Royal Botanic Gardens, 1–21. Herendeen PS, Magallo´ n-Puebla S, Lupia R, Crane PR, Kobylinska J. 1999. Preliminary conspectus of the Allon flora from the Late Cretaceous (Late Santonian) of Central Georgia, U.S.A. Annals of the Missouri Botanical Garden 86: 407–471. Heslop-Harrison Y, Shivanna KR. 1977. The receptive surface of the angiosperm stigma. Annals of Botany 41: 1233–1258. Hill AW. 1906. The morphology and seedling structure of the geophilous species of Peperomia, together with some views on the origins of monocotyledons. Annals of Botany 20: 395–427. Hill TG. 1900. The structure and development of Triglochin maritimum L. Annals of Botany 14: 83–107. Hofmeister W. 1852. Zur Entwickelungsgeschichte der Zostera. Botanische Zeitung 10: 121–131, 137–149, 157–158. Hofmeister W. 1861. Neue Beitra¨ ge zur Kenntniss der Embryobildung der Phanerogamen. 2. Monokotyledonen. Abhandlungen der Ko¨ niglichen Sa¨ chsischen Gesellschaft der Wissenschaften 7: 629–760. Holferty GM. 1901. Ovule and embryo of Potamogeton natans. Botanical Gazette 31: 339–346. Holmgren J. 1913. Zur Entwicklungsgeschichte von Butomus umbellatus L. Svensk Botanisk Tidskrift 7: 58–77. Horn P. 1875. Beitra¨ ge zur Kenntniss des Blu¨ thenbaues von Scheuchzeria palustris. Archiv des Vereins der Freunde der Naturgeschichte in Mecklenburg 29: 161–166. Horn P. 1876. Beitra¨ ge zur Kenntniss der Triglochinblu¨ the. Archiv des Vereins der Freunde der Naturgeschichte in Mecklenburg 30: 120–135. Hotta M. 1971. Study of the family Araceae. General remarks. Japanese Journal of Botany 20: 269–310.

57

Huber H. 1969. Die Samenmerkmale und Verwandtschaftsverha¨ ltnisse der Liliifloren. Mitteilungen der Botanischen Staatssammlung Mu¨ nchen 8: 219–538. Huber H. 1977. The treatment of the monocotyledons in an evolutionary system of classification. Plant Systematics and Evolution, Supplement 1: 285–298. Huber H. 1998a. Dioscoreaceae. In: Kubitzki K, ed. The families and genera of vascular plants III. Berlin: Springer, 216–235. Huber H. 1998b. Trichopodaceae. In: Kubitzki K, ed. The families and genera of vascular plants III. Berlin: Springer, 441–444. Hunziker AT. 1982. Observaciones biologicas y taxonomicas sobre Hydromistria laevigata (Hydrocharitaceae). Taxon 31: 472–477. Igersheim A. 1993. The character states of the Caribbean monotypic Strumpfia (Rubiaceae). Nordic Journal of Botany 13: 545–559. Igersheim A, Cichocki O. 1996. A simple method for microtome sectioning of prehistoric charcoal specimens embedded in 2-hydroxyethyl methacrylate (HEMA). Review of Palaeobotany and Palynology 92: 389–393. Igersheim A, Endress PK. 1997. Gynoecium diversity and systematics of the Magnoliales and winteroids. Botanical Journal of the Linnean Society 124: 213–271. Igersheim A, Endress PK. 1998. Gynoecium diversity and systematics of the paleoherbs. Botanical Journal of the Linnean Society 127: 289–370. Indra R, Krishnamurthy KV. 1982. Histochemistry of the gland cells of the ovary wall of Ottelia alismoides. In: Periasamy K, ed. Histochemistry, developmental and structural anatomy of angiosperms: a symposium. Tiruchirapalli: P & O Publications, 17–23. Indra R, Krishnamurthy KV. 1984. Ovary wall obturator in Ottelia alismoides. Current Science 53: 442–443. Islam AS. 1950. A contribution to the life history of Ottelia alismoides Pers. Journal of the Indian Botanical Society 29: 79–91. Jitariu GG. 1952. Le rapport entre les carpelles des Helobiae a` gyne´ ce´ e infe´ rieur. Buletin Stiintific, Academia Republicii Populare Romine, Sectia de Biologie si Stiinte Agricole, Seria Botanica 4: 537–549. Johri BM. 1933. Contribution to the morphology of Limnophyton obtusifolium Miq. Current Science 2: 12–13. Johri BM. 1935a. Life-history of Butomopsis lanceolata Kunth. Nature 136: 338. Johri BM. 1935b. Studies in the family Alismaceae. I. Limnophyton obtusifolium Miq. Journal of the Indian Botanical Society 14: 49–66. Johri BM. 1935c. Studies in the family Alismaceae. II. Sagittaria sagittifolia L. Proceedings of the Indian Academy of Sciences B 1: 340–348. Johri BM. 1935d. Studies in the family Alismaceae. III. Sagittaria guayanensis H.B.K. and S. latifolia Willd. Proceedings of the Indian Academy of Sciences B 2: 33–48. Johri BM. 1936a. Studies in the family Alismaceae. IV. Alisma plantago L.; Alisma plantago-aquatica L. and Sagittaria graminea Mich. Proceedings of the Indian Academy of Sciences B 4: 128–138.

58

A. IGERSHEIM ET AL.

Johri BM. 1936b. The life-history of Butomopsis lanceolata Kunth. Proceedings of the Indian Academy of Sciences B 4: 139–162. Johri BM. 1938a. The embryo sac of Limnocharis emarginata. New Phytologist 37: 279–285. Johri BM. 1938b. The embryo sac of Hydrocleis nymphoides Buchen. Beihefte zum Botanischen Centralblatt A 58: 165– 172. Johri BM, Bhatnagar SP. 1957. Intracarpellary pollen grains in angiosperms. Phytomorphology 7: 292–296. Jo¨ nsson B. 1881. Om embryosa¨ ckens utveckling hos Angiospermerna. Lunds Universitets Aars-skrift 16 (2): 1–86. Juhnke G, Winkler H. 1938. Der Balg als Grundelement des Angiospermengynaeceums. Beitra¨ ge zur Biologie der Pflanzen 25: 290–324. Ju ¨ ssen FJ. 1928. Die Haploidgeneration der Araceen und ihre Verwertung fu¨ r das System. Botanische Jahrbu¨ cher fu¨ r Systematik 62: 155–283. Kale NN, Pai RM. 1979. The floral anatomy of Trichopus zeylanicus Gaertn. Proceedings of the Indian Academy of Sciences B 88: 63–67. Ka¨ llersjo¨ M et al. 1998. Simultaneous parsimony jackknife analysis of 2538 rbcL sequences reveals support for major clades of green plants, land plants, seed plants and flowering plants. Plant Systematics and Evolution 213: 259–287. Kamelina OP. 1990. Potamogetonaceae. In: Batygina TB, Yakovlev MS, eds. Comparative embryology of flowering plants, Monocotyledones. Leningrad: Nauka, 34–39. Kamelina OP, Teryokhin ES. 1990a. Ruppiaceae. In: Batygina TB, Yakovlev MS, eds. Comparative embryology of flowering plants, Monocotyledones. Leningrad: Nauka, 39–44. Kamelina OP, Teryokhin ES. 1990b. Zannichelliaceae. In: Batygina TB, Yakovlev MS, eds. Comparative embryology of flowering plants, Monocotyledones. Leningrad: Nauka, 44–50. Kaul RB. 1967a. Development and vasculature of the flowers of Lophotocarpus calycinus and Sagittaria latifolia (Alismaceae). American Journal of Botany 54: 914–920. Kaul RB. 1967b. Ontogeny and anatomy of the flower of Limnocharis flava (Butomaceae). American Journal of Botany 54: 1223–1230. Kaul RB. 1968. Floral morphology and phylogeny in the Hydrocharitaceae. Phytomorphology 18: 13–35. Kaul RB. 1969. Morphology and development of the flowers of Boottia cordata and Ottelia alismoides and their synthetic hybrid. American Journal of Botany 56: 951–959. Kaul RB. 1976. Conduplicate and specialized carpels in the Alismatales. American Journal of Botany 63: 175–182. Kaul RB. 1993. Meristic and organogenetic variation in Ruppia occidentalis and R. maritima. International Journal of Plant Sciences 154: 416–424. Kausik SB. 1939. Pollination and its influences on the behaviour of the pistillate flower in Vallisneria spiralis. American Journal of Botany 26: 207–211. Kausik SB. 1940a. A contribution to the embryology of Enalus acoroides (L. fil.) Steud. Proceedings of the Indian Academy of Sciences 11: 83–99.

Kausik SB. 1940b. Vascular anatomy of the pistillate flower of Enalus acoroides (L. fil.) Steud. Current Science 9: 182– 184. Koschewnikoff DA. 1877. Zur Entwicklungsgeschichte der Araceenblu¨ te. Bulletin de la Socie´ te´ des Naturalistes de Moscou 52: 235–292. Krasnikov LG. 1990. Butomaceae. In: Batygina TB, Yakovlev MS, eds. Comparative embryology of flowering plants, Monocotyledones. Leningrad: Nauka, 7–14. Kubin E. 1878. Die Entwicklung von Pistia stratiotes. Hansteins Botanische Abhandlungen 3: 1–30. Kubitzki K. 1998a. Taccaceae. In: Kubitzki K, ed. The families and genera of vascular plants III. Berlin: Springer, 425–428. Kubitzki K, ed. 1998b. The families and genera of vascular plants IV. Berlin: Springer. Kubitzki K. 1998c. Conspectus of families treated in this volume. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 1–4. Kubitzki K, Rudall PJ, Chase MW. 1998. Systematics and evolution [of monocotyledons]. In: Kubitzki K, ed. The families and genera of vascular plants III. Berlin: Springer, 23–33. Kudryashov LW, Savich EI. 1963. Some data on the embryology of Alisma plantago-aquatica L. Byulletin Moscowskogo Obshchestva Ispytateley Prirody, Otdel Biol 68: 50–63. Kunth CS. 1841. Enumeratio plantarum 3. Stuttgart: Cotta. Kuo J, Kirkman H. 1987. Floral and seedling morphology and anatomy of Thalassodendron pachyrhizum den Hartog (Cymodoceaceae). Aquatic Botany 29: 1–17. Kuo J, McComb AJ. 1998a. Cymodoceaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 133–140. Kuo J, McComb AJ. 1998b. Posidoniaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 404–408. Kuo J, McComb AJ. 1998c. Zosteraceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 496–502. Lacor MAM. 1970. Some physiological and morphogenetic aspects of flowering of Spirodela polyrhiza (L.) Schleiden. Acta Botanica Neerlandica 19: 53–60. Lacroix CR, Kemp JR. 1997. Developmental morphology of the androecium and gynoecium in Ruppia maritima L.: considerations for pollination. Aquatic Botany 59: 253–262. Lakshmanan KK. 1961. Embryological studies in the Hydrocharitaceae I. Blyxa octandra Planch. Journal of Madras University B 31: 133–142. Lakshmanan KK. 1963a. Embryological studies in the Hydrocharitaceae II. Halophila ovata Gaudich. Journal of the Indian Botanical Society 42: 15–18. Lakshmanan KK. 1963b. Embryological studies in the Hydrocharitaceae III. Nechamandra alternifolia. Phyton 20: 49–58. Lakshmanan KK. 1968. Preliminary note on the embryology of Diplanthera uninervis Aschers. Current Science 37: 534– 535.

GYNOECIUM IN BASAL MONOCOTS Lakshmanan KK, Rajeswari S. 1979. Sea grasses of Krusadai island in the gulf of Mannar, India – II. Syringodium isoetifolium (Aschers.) Dandy. Indian Journal of Botany 2: 87–95. Landolt E. 1986. The family of Lemnaceae – a monographic study 1. Vero¨ ffentlichungen des Geobotanischen Institutes der Eidgeno¨ ssischen Technischen Hochschule, Stiftung Rubel, in Zu¨ rich 71: 1–564. Lawalre´ e A. 1952. L’embryologie des Lemnaceae. Observations sur Lemna minor L. La Cellule 54: 305–326. Lehmann NL, Sattler R. 1992. Irregular floral development in Calla palustris (Araceae) and the concept of homoeosis. American Journal of Botany 79: 1145–1157. Leinfellner W. 1940. Das epidermale Randwachstum der Fruchtbla¨ tter. Botanisches Archiv 41: 507–515. ¨ ber die Variabilita¨ t der Blu¨ ten von Leinfellner W. 1962. U ¨ bersicht der Tofieldia calyculata. III. Zusammenfassende U ¨ vorgefundenen Abweichungen. Osterreichische Botanische Zeitschrift 109: 395–430. ¨ ber peltate Karpelle, deren Leinfellner W. 1969. U Schlauchteil aussen vom Ventralspalt unvollkommen ¨ sterreichische Botanische Zeitschrift aufgeschlitzt ist. O 117: 276–283. Leinfellner W. 1973. Zur Lage des wahren Karpellrandes. ¨ sterreichische Botanische Zeitschrift 121: 285–301. O Leins P, Stadler P. 1973. Entwicklungsgeschichtliche Un¨ stersuchungen am Androeceum der Alismatales. O terreichische Botanische Zeitschrift 121: 51–63. Les DH, Cleland MA, Waycott M. 1997. Phylogenetic studies in Alismatidae II: Evolution of marine angiosperms (seagrasses) and hydrophily. Systematic Botany 22: 443– 463. Les DH, Garvin DK, Wimpee CF. 1993. Phylogenetic studies in the monocot subclass Alismatidae: Evidence for a reappraisal of the aquatic order Najadales. Molecular Phylogenetics and Evolution 2: 304–314. Les DH, Haynes RR. 1995. Systematics of subclass Alismatidae: a synthesis of approaches. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ, eds. Monocotyledons: systematics and evolution. Kew: Royal Botanic Gardens, 353– 377. Les DH, Schneider EL. 1995. The Nymphaeales, Alismatidae, and the theory of an aquatic monocotyledon origin. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ, eds. Monocotyledons: systematics and evolution. Kew: Royal Botanic Gardens, 23–42. Lieu SM. 1979. Organogenesis in Triglochin striata. Canadian Journal of Botany 57: 1418–1438. Lindley J. 1832. Aristolochia cymbifera. Botanical Register 18: Plate 1543. Loconte H. 1996. Comparison of alternative hypotheses for the origin of angiosperms. In: Taylor DW, Hickey LJ, eds. Flowering plant origin, evolution and phylogeny. New York: Chapman & Hall, 267–285. Loconte H, Stevenson DW. 1991. Cladistics of the Magnoliidae. Cladistics 7: 267–296. Loew E, Kirchner O. 1934. Tofieldia. In: Wangerin W, Schro¨ ter C, eds. Lebensgeschichte der Blu¨ tenpflanzen Mitteleuropas I,3. Stuttgart: Ulmer.

59

Lotsy JP. 1911. Vortra¨ ge u¨ ber botanische Stammesgeschichte, 3. Jena: Fischer. Maas-van de Kamer, Weustenfeld T. 1998. Triuridaceae. In: Kubitzki K, ed. The families and genera of vascular plants III. Berlin: Springer, 452–458. Magnus P. 1870. Beitra¨ ge zur Kenntniss der Gattung Najas L. Berlin: Reimer. Maheshwari P. 1933. ¨ A note on the life history of Hydrilla verticillata Presl. Current Science 2: 13–14. Maheshwari P, Johri BM. 1950. The occurrence of persistent pollen tubes in Hydrilla, Ottelia and Boerhaavia, together with a discussion of the possible significance of this phenomenon in the life-history of angiosperms. Journal of the Indian Botanical Society 29: 47–51. Maheshwari P, Singh B. 1943. Studies in the family Alismaceae. V. The embryology of Machaerocarpus californicus (Torr.) Small. Proceedings of the National Institute of Science of India 9: 311–322. Maheshwari SC. 1954. The embryology of Wolffia. Phytomorphology 4: 355–365. Maheshwari SC. 1958. Spirodela polyrrhiza: the link between the aroids and the duckweeds. Nature 181: 1745– 1746. Maheshwari SC, Kapil RN. 1963. Morphological and embryological studies on the Lemnaceae. I. The floral structure and gametophytes of Lemna paucicostata. American Journal of Botany 50: 677–686. Maheshwari SC, Khanna PP. 1956. The embryology of Arisaema wallichianum Hook.f. and the systematic position of the Araceae. Phytomorphology 6: 379–388. Maheshwari SC, Maheshwari N. 1963. The female gametophyte, endosperm and embryo of Spirodela polyrrhiza. Beitra¨ ge zur Biologie der Pflanzen 39: 179–188. Manya-Chernej EN. 1978. Anatomical and morphological studies of inflorescence in some species of Araceae. Botanicheskij Zhurnal 63: 510–522. Markgraf F. 1936. Blu¨ tenbau und Verwandtschaft bei den einfachsten Helobiae. Berichte der Deutschen Botanischen Gesellschaft 54: 191–228. Ma´ rquez-Guzma´ n J, Engleman M, Martı´nez-Mena A, Martı´nez E, Ramos C. 1989. Anatomia reproductiva de Lacandonia schismatica (Lacandoniaceae). Annals of the Missouri Botanical Garden 76: 124–127. Martı´nez E, Ramos CH. 1989. Lacandoniaceae (Triuridales): una nueva familia de Me´ xico. Annals of the Missouri Botanical Garden 76: 128–135. Mathews S, Donoghue MJ. 1999. The root of angiosperms phylogeny inferred from duplicate phytochrome genes. Science 286: 947–950. Mayo SJ. 1989. Observations of gynoecial structure in Philodendron (Araceae). Botanical Journal of the Linnean Society 100: 139–172. Mayo SJ, Bogner J, Boyce PC. 1995. The Arales. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ, eds. Monocotyledons: systematics and evolution 1. Kew: Royal Botanic Gardens, 277–286. Mayo SJ, Bogner J, Boyce PC. 1997. The genera of Araceae. Kew: Royal Botanic Gardens.

60

A. IGERSHEIM ET AL.

McConchie CA. 1983. Floral development of Maidenia rubra Rendle (Hydrocharitaceae). Australian Journal of Botany 31: 585–603. McConchie CA, Ducker SC, Knox RB. 1982. Biology of Australian seagrasses: floral development and morphology in Amphibolis (Cymodoceaceae). Australian Journal of Botany 30: 251–264. McConchie CA, Kadereit JW. 1987. Floral structure of Vallisneria caulescens Bailey & F. Mueller. Aquatic Botany 29: 101–110. McConchie CA, Knox RB. 1989. Pollen-stigma interaction in the seagrass Posidonia australis. Annals of Botany 63: 235–248. Mercado-Noriel LR, Mercado BT. 1978. Floral anatomy and seed morphology of water lettuce (Pistia stratiotes). Philippine Agriculturist 61: 281–290. Michell MR. 1916. The embryo sac of Richardia africana. Botanical Gazette 61: 325–336. Miki S. 1937. The origin of Najas and Potamogeton. Botanical Magazine, Tokyo 51: 472–480. Montesantos N. 1912. Morphologische und biologische Untersuchungen u¨ ber einige Hydrocharideen. Flora 105: 1–32. ¨ ber den Bau und die Entwicklung der Mu ¨ cke M. 1908. U Fru¨ chte und u¨ ber die Herkunft von Acorus calamus L. Botanische Zeitung 66: 1–23. Mu ¨ ller JF. 1875. Zur Entwickelungsgeschichte der Vallisneria spiralis. Doctoral Thesis, University of Bonn. Bonn: Georgi. Mu ¨ ller JF. 1878. Die Entwicklung von Vallisneria spiralis. Hansteins Botanische Abhandlungen 3 (4): 33–70. Murbeck S. 1902. u¨ ber die Embryologie von Ruppia rostellata Koch. Kongl. Svenska Vetenskaps-Akademiens Handlingar 36, 5: 1–21. Murthy SK. 1933. Cytological and embryological studies in Limnophyton obtusifolium Miq. Mysore University Journal 7: 135–166. Nadot S, Bittar G, Carter L, Lacroix R, Lejeune B. 1995. A phylogenetic analysis of monocotyledons based on the chloroplast gene rps4, using parsimony and a new numerical phenetics method. Molecular Phylogenetics and Evolution 4: 257–282. Nandi O, Chase MW, Endress PK. 1998. A combined cladistic analysis of angiosperms using rbcL and non-molecular data sets. Annals of the Missouri Botanical Garden 85: 137–212. Narasimha Murthy SK. 1935. The life-history of Ottelia alismoides Pers. Proceedings of the Indian Academy of Sciences B 2: 59–66. Nayar BK, Sworupanandan K. 1978. Morphology of the fruit and mechanism of seed dispersal of the freshwater weed Limnocharis flava. Proceedings of the Indian Academy of Sciences B 87: 49–53. Nikiticheva ZI. 1990a. Alismataceae. In: Batygina TB, Yakovlev MS, eds. Comparative embryology of flowering plants, Monocotyledones. Leningrad: Nauka, 16–20. Nikiticheva ZI. 1990b. Scheuchzeriaceae. In: Batygina TB, Yakovlev MS, eds. Comparative embryology of flowering plants, Monocotyledones. Leningrad: Nauka, 26–28.

Nikiticheva ZI, Proskurina OB. 1990. Juncaginaceae. In: Batygina TB, Yakovlev MS, eds. Comparative embryology of flowering plants, Monocotyledones. Leningrad: Nauka, 28–34. Nikiticheva ZI, Proskurina OB. 1992. Embryology of Scheuchzeria palustris (Scheuchzeriaceae). Botanicheskij Zhurnal, St. Petersburg 77 (1): 3–18. Nitzschke J. 1914. Beitra¨ ge zur Phylogenie der Monocotyledonen, gegru¨ ndet auf der Embryosackentwicklung apokarper Nymphaeaceen und Helobien. Beitra¨ ge zur Biologie der Pflanzen 12: 223–267. Ohsawa TA. 1998. Permineralized monocot flowers from the Cretaceous of Japan. Monocots II. Second International Conference on the Comparative Biology of the monocotyledons. University of New South Wales, Sydney. Abstracts, 62. Ono T. 1929. Embryologie der Liliaceae, mit besonderer Ru¨ cksicht auf die Endospermbildung. I. Melanthioideae und Aletrioideae. Science Reports of the Toˆ hoku Imperial University, Ser. 4 4: 383–393. Padhye MD, Rao H. 1960. Contribution to the embryology of Lagarosiphon roxburghii Benth. Proceedings of the Indian Science Congress, Bombay 47 (3): 356–357. Paetow W. 1931. Embryologische Untersuchungen an Taccaceen, Meliaceen und Dilleniaceen. Planta 14: 441–470. Palm B. 1915. Studien u¨ ber Konstruktionstypen und Entwicklungswege des Embryosackes der Angiospermen. D. Phil. Thesis, University of Stockholm. Stockholm: Svenska Tryckeriaktiebolaget. Panicker TKB. 1965. Female gametophyte and endosperm in Lagenandra ovata Thw. Current Science 34: 614–615. Parameswaran N. 1959. A contribution to the embryology of Theriophonum minutum. Proceedings of the Indian Academy of Sciences B 50: 15–25. Parlatore F. 1854. Nuovi generi e nuove specie di piante monocotiledoni. Firenze: Tipografia Le Monnier. Payer JB. 1857. Traite´ d’organoge´ nie compare´ e de la fleur. Paris: Masson. Pellmyr O, Patt JM. 1986. Function of olfactory and visual stimuli in pollination of Lysichiton americanum (Araceae) by a staphylinid beetle. Madron˜ o 33: 47–54. Pettitt JM. 1976. Pollen wall and stigma surface in the marine angiosperms Thalassia and Thalassodendron. Micron 7: 21–32. Pettitt JM. 1980. Reproduction in seagrasses: nature of the pollen and receptive surface of the stigma in the Hydrocharitaceae. Annals of Botany 45: 257–271. Pettitt JM. 1984. Aspects of flowering and pollination in marine angiosperms. Oceanography and Marine Biology 22: 315–342. Pettitt JM, Ducker SC, Knox RB. 1981. Submarine pollination. Scientific American 244 (3): 92–101. Pettitt JM, McConchie CA, Ducker SC, Knox RB. 1980. Unique adaptations for submarine pollination in seagrasses. Nature 286: 487–489. Pettitt JM, McConchie CA, Ducker SC, Knox RB. 1983. Reproduction in seagrasses: pollination in Amphibolis antarctica. Proceedings of the Royal Society of London B 219: 119–135.

GYNOECIUM IN BASAL MONOCOTS Pickett FL. 1913. The development of the embryo sac of Arisaema triphyllum. Bulletin of the Torrey Botanical Club 40: 229–235. Pickett FL. 1915. A contribution to our knowledge of Arisaema triphyllum. Memoirs of the Torrey Botanical Club 16: 1–55. Planchon JE. 1844. Sur le genre Aponogeton et sur ses affinite´ s naturelles. Annales des Sciences Naturelles, Se´ r. 3 1: 107–119. Pogan E. 1965. Embryological studies in a triploid hybrid of Alisma. Acta Biologica Cracoviensia, Ser. Bot 8: 11–18. Pohl F. 1935. Ein Fall von zweckloser Proterandrie (Butomus umbellatus L.). Berichte der Deutschen Botanischen Gesellschaft 53: 779–782. Poisson G, Barabe´ D. 1998. Architecture de l’appareil ve´ ge´ tatif et organisation florale du Dracontium polyphyllum L. (Araceae). Adansonia 20: 195–210. Pole M. 1999. Latest Albian–earliest Cenomanian monocotyledonous leaves from Australia. Botanical Journal of the Linnean Society 129: 177–186. Posluszny U. 1981. Unicarpellate floral development in Potamogeton zosteriformis. Canadian Journal of Botany 59: 495–504. Posluszny U. 1983. Re-evaluation of certain key relationships in the Alismatidae: floral organogenesis of Scheuchzeria palustris (Scheuchzeriaceae). American Journal of Botany 70: 925–933. Posluszny U, Charlton WA. 1993. Evolution of the helobial flower. Aquatic Botany 44: 303–324. Posluszny U, Charlton WA, Jain DK. 1986. Morphology and development of the reproductive shoots of Lilaea scilloides (Poir.) Hauman (Alismatidae). Botanical Journal of the Linnean Society 92: 323–342. Posluszny U, Charlton WA, Les DH. 1998. Modularity in helobial flowers. Monocots II. Second International Conference on the Comparative Biology of the Monocotyledons. University of New South Wales, Sydney. Abstracts, 44. Posluszny U, Sattler R. 1973. Floral development of Potamogeton densus. Canadian Journal of Botany 51: 647– 656. Posluszny U, Sattler R. 1974a. Floral development of Potamogeton richardsonii. American Journal of Botany 61: 209–216. Posluszny U, Sattler R. 1974b. Floral development of Ruppia maritima var. maritima. Canadian Journal of Botany 52: 1607–1612. Posluszny U, Sattler R. 1976a. Floral development of Zannichellia palustris. Canadian Journal of Botany 54: 651– 662. Posluszny U, Sattler R. 1976b. Floral development of Najas flexilis. Canadian Journal of Botany 54: 1140–1151. Posluszny U, Tomlinson PB. 1977. Morphology and development of floral shoots and organs in certain Zannichelliaceae. Botanical Journal of the Linnean Society 75: 21–46. Poulsen VA. 1906. Sciaphila nana Bl. Et Bidrag til Stoevvejens Udvikling hos Triuridaceerne. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Koebenhavn 58: 161–176.

61

Prillieux E. 1864. Recherches sur la ve´ ge´ tation et la structure de l’Althenia filiformis Petit. Annales des Sciences Naturelles, Botanique, Se´ rie 5 2: 169–190. Prychid CJ, Rudall PJ. 1999. Calcium oxalate crystals in monocotyledons: a review of their structure and systematics. Annals of Botany 84: 725–739. Qiu Y-L, Chase MW, Les DH, Parks CR. 1993. Molecular phylogenetics of the Magnoliidae: Cladistic analyses of nucleotide sequences of the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 587–606. Qiu Y-L, Lee J, Bernasconi-Quadroni F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW. 1999. The earliest angiosperms: evidence from mitochondrial, plastid, and nuclear genomes. Nature 402: 404– 407. Qiu Y-L, Palmer JD. 1998. Intron evolution and monocot phylogeny. Monocots II. Second International Conference on the Comparative Biology of the Monocotyledons. University of New South Wales, Sydney. Abstracts, 45. Ramı´rez BW, Go´ mez PLD. 1978. Production of nectar and gums by flowers of Monstera deliciosa (Araceae) and of some species of Clusia (Guttiferae) collected by New World Trigona bees. Brenesia 14–15: 407–412. Rangasamy K. 1934. Contribution to the life-history of Vallisneria spiralis L. Journal of the Indian Botanical Society 13: 129–148. Rangasamy K. 1941. A morphological study of the flower of Blyxa echinosperma Hook.f. Journal of the Indian Botanical Society 20: 123–133. Rao AN. 1953. Embryology of Dioscorea oppositifolia L. Phytomorphology 3: 121–126. Rao VS. 1969. The vascular anatomy of the flowers of Tacca pinnatifida. Journal of the University of Bombay, N.S., Part 5B 38: 18–24. Riede W. 1921. Untersuchungen u¨ ber Wasserpflanzen. Flora 114: 1–118. Rohrbach P. 1873. Beitra¨ ge zur Kenntniss einiger Hydrocharideen. Abhandlungen der Naturforschenden Gesellschaft zu Halle 12: 50–114. Roper RB. 1952. The embryo sac of Butomus umbellatus. Phytomorphology 2: 61–74. ¨ ber die Embryologie von Zostera Rosenberg O. 1901. U marina L. Svenska Kongl. Vetenskaps-Akademiens Handlingar, Afd III 27 (6), 1–26. Rosendahl CO. 1909. Embryo-sac development and embryology of Symplocarpus foetidus. Minnesota Botanical Studies, Ser. 7 4: 1–9. Roth I. 1949. Zur Entwicklungsgeschichte des Blattes, mit besonderer Beru¨ cksichtigung von Stipular- und Ligularbildungen. Planta 37: 299–336. Rowlee WW. 1896. The stigmas and pollen of Arisaema. Bulletin of the Torrey Botanical Club 23: 369–370. Ru ¨ bsamen-Weustenfeld T. 1991. Morphologische, embryologische und systematische Untersuchungen an Triuridaceae. Bibliotheca Botanica 149: 1–113. Rudall PJ. 1997. The nucellus and chalaza in monocotyledons: structure and systematics. Botanical Review 63: 140–181.

62

A. IGERSHEIM ET AL.

Rudall PJ, Furness CA. 1997. Systematics of Acorus: ovule and anther. International Journal of Plant Sciences 158: 640–651. Rudall PJ, Prychid CJ, Jones C. 1998. Intra-ovarian trichomes in monocotyledons. In: Owens SJ, Rudall PJ, eds. Reproductive biology in systematics, conservation and economic botany. Kew: Royal Botanic Gardens, 219–230. Sahni B, Johri BM. 1936. Pollen grains in the stylar canal and in the ovary of an angiosperm. Current Science 4: 587–589. Salisbury EJ. 1926. Floral construction in the Helobiales. Annals of Botany 40: 419–445. Saˆ ne´ YK. 1939. A contribution to the embryology of the Aponogetonaceae. Journal of the Indian Botanical Society 18: 79–91. Sattler R. 1973. Organogenesis of flowers. Toronto: University of Toronto Press. Sattler R, Singh V. 1973. Floral development of Hydrocleis nymphoides. Canadian Journal of Botany 51: 2455–2458. Sattler R, Singh V. 1978. Floral organogenesis of Echinodorus amazonicus Rataj and floral construction of the Alismatales. Botanical Journal of the Linnean Society 77: 141–156. Saunders E. 1928. Illustrations of carpel polymorphism I. New Phytologist 27: 47–60. Saunders E. 1929. On carpel polymorphism III. Annals of Botany 43: 459–481. Saunders E. 1931. Illustrations of carpel polymorphism, VII. New Phytologist 30: 80–118. Saunders E. 1937/1939. Floral morphology. A new outlook with special reference to the gynaeceum. Cambridge: Heffer. Schaffner JH. 1896. The embryo sac of Alisma plantago. Botanical Gazette 21: 123–132. Schaffner JH. 1897. The life history of Sagittaria variabilis. Botanical Gazette 23: 252–273. Schnarf K. 1925. Kleine Beitra¨ ge zur Kenntnis der En¨ ber zwei kritwicklungsgeschichte der Angiospermen. V. U tische Fa¨ lle der Endospermentwicklung (Verbena und ¨ sterreichische Botanische Zeitschrift 74: 40– Triglochin). O 50. Schneider EL, Carlquist S. 1997. Origins and nature of vessels in monocotyledons. 2. Juncaginaceae and Scheuchzeriaceae. Nordic Journal of Botany 17: 397–401. Schneider EL, Carlquist S. 1998. Origin and nature of vessels in monocotyledons. 4. Araceae subfamily Philodendroideae. Journal of the Torrey Botanical Society 125: 253–260. Schneitz K. 1999. The molecular and genetic control of ovule development. Current Opinions in Plant Biology 2: 13–17. Schniewind-Thies J. 1897. Beitra¨ ge zur Kenntnis der Septalnectarien. Jena: Fischer. Schu ¨ epp O. 1966. Meristeme. Wachstum und Formbildung in den Teilungsgeweben ho¨ herer Pflanzen. Basel: Birkha¨ user. Scribailo RW, Posluszny U. 1985. Floral development of Hydrocharis morsus-ranae (Hydrocharitaceae). American Journal of Botany 72: 1578–1589. Scribailo RW, Tomlinson PB. 1992. Shoot and floral de-

velopment in Calla palustris (Araceae-Calloideae). International Journal of Plant Sciences 153: 1–13. Seelieb W. 1924. Beitra¨ ge zur Entwicklungsgeschichte von Tofieldia calyculata (L.) Wahlenb. Botaniska Notiser 1924: 172–178. Serbanescu-Jitariu G. 1964. Zur Brachysynkarpie bei Butomus umbellatus L. Revue Roumaine de Biologie, Se´ rie de Botanique 9: 235–239. Serbanescu-Jitariu G. 1966. Conside´ rations sur le gyne´ ce´ e et le fruit de Scheuchzeria palustris L. Revue Roumaine de Biologie, Se´ rie de Botanique 11: 435–439. Serbanescu-Jitariu G. 1972a. Conside´ rations sur le gyne´ ce´ e, le fruit, la biologie de la disse´ mination et la germination chez Zannichellia palustris L. Analele Universitatii Bucuresti, Seria Stiintelor Naturii, Biologie Vegetala 21: 63–70. Serbanescu-Jitariu G. 1972b. La morphologie du gyne´ ce´ e chez certaines espe`ces du genre Potamogetum. Bulletin de la Socie´ te´ d’Historie Naturelle de l’Afrique du Nord 63 (3–4): 3–7. Serbanescu-Jitariu G. 1973a. Betrachtungen u¨ ber Gyna¨ zeum, Frucht und Keimung bei Triglochin maritimum L. und Triglochin palustre L. Revue Roumaine de Biologie, Se´ rie de Botanique 18: 9–20. Serbanescu-Jitariu G. 1973b. Betrachtungen u¨ ber das Gyno¨ zeum und die Keimung der Samen bei der Gattung Limnocharis. Lucrarile Gradinii Botanice din Bucuresti 1972-3: 41–50. Serbanescu-Jitariu G. 1974a. Ein Beitrag zur Kenntnis des Gyno¨ zeums, der Frucht und der Samenkeimung bei Alisma plantago-aquatica L. Lucrarile Gradinii Botanice din Bucuresti 1974: 109–118. Serbanescu-Jitariu G. 1974b. Observations sur le gyne´ ce´ e de Ruppia maritima L. et de Zostera marina L. Bulletin de la Socie´ te´ d’Histoire Naturelle de l’Afrique du Nord 65 (1–2): 215–225. Serbanescu-Jitariu G. 1986. Observations concernant le gyne´ ce´ e de Najas marina L. Revue Roumaine Biologique, Biologie Ve´ ge´ tale 31: 23–25. Sergue´ eff M. 1907. Contribution a` la morphologie et la biologie des Aponoge´ tonace´ es. Doctoral dissertation, University of Geneva. Gene`ve: W. Ku¨ ndig & Fils. Shadowsky AF. 1931. Einige Angaben u¨ ber die Embryologie von Pistia stratiotes L. Berichte der Deutschen Botanischen Gesellschaft 49: 350–356. Shaffer-Fehre M. 1991. The position of Najas within the subclass Alismatidae (Monocotyledones) in the light of new evidence from seed coat structures in the Hydrocharitoideae (Hydrocharitaceae). Botanical Journal of the Linnean Society 107: 189–209. Shamrov II. 1998. Ovule classification in flowering plants – new approaches and concepts. Botanische Jahrbu¨ cher fu¨ r Systematik 120: 377–407. Shih CY. 1979. SEM studies of the flowering of duckweed, Lemna perpusilla, 6746. Scanning Electron Microscopy 1979 (III): 479–486. Singh V. 1965a. Morphological and anatomical studies in Helobiae. II. Vascular anatomy of the flower of Potamogetonaceae. Botanical Gazette 126: 137–144.

GYNOECIUM IN BASAL MONOCOTS Singh V. 1965b. Morphological and anatomical studies in Helobiae. III. Vascular anatomy of the node and flower of Najadaceae. Proceedings of the Indian Academy of Sciences B 61: 98–108. Singh V. 1965c. Morphological and anatomical studies in Helobiae IV. Vegetative and floral anatomy of Aponogetonaceae. Proceedings of the Indian Academy of Sciences B 61: 147–159. Singh V. 1965d. Morphological and anatomical studies in Helobiae. V. Vascular anatomy of the flower of Lilaea scilloides (Poir.) Hamm. Proceedings of the Indian Academy of Sciences B 61: 316–325. Singh V. 1966a. Morphological and anatomical studies in Helobiae. VI. Vascular anatomy of the flower of Alismaceae. Proceedings of the National Academy of Sciences, India, B 36: 329–344. Singh V. 1966b. Morphological and anatomical studies in Helobiae. VII. Vascular anatomy of the flower of Butomus umbellatus Linn. Proceedings of the Indian Academy of Sciences B 63: 313–320. Singh V. 1967a. Morphological and anatomical studies in Helobiae VIII. Vascular anatomy of the flower of Hydrocharitaceae – Stratioideae and Thalassioideae. Agra University Journal of Research (Science) 15: 43–60. Singh V. 1967b. Morphological and anatomical studies in Helobiae IX. Vascular anatomy of the flower of Hydrocharitaceae – Vallisneroideae and Halophiloideae. Agra University Journal of Research (Science) 15: 83–106. Singh V. 1973. Development of gynoecium in Triglochin in three dimensions. Current Science 42: 813–815. Singh V, Sattler R. 1972. Floral development of Alisma triviale. Canadian Journal of Botany 50: 619–627. Singh V, Sattler R. 1973. Nonspiral androecium and gynoecium of Sagittaria latifolia. Canadian Journal of Botany 51: 1093–1095. Singh V, Sattler R. 1974. Floral development of Butomus umbellatus. Canadian Journal of Botany 52: 223–230. Singh V, Sattler R. 1977. Floral development of Aponogeton natans and A. undulatus. Canadian Journal of Botany 55: 1106–1120. Smets EF, Ronse Decraene L-P, Caris P, Rudall PJ. 2000. Floral nectaries in monocotyledons: distribution and evolution. In: Wilson KL, Morrison DA, eds. Monocots: systematics and evolution. Collingwood, Victoria: CSIRO Publishing, 230–240. Sokolowska-Kulczycka A. 1980. Embryological studies of Tofieldia calyculata (L.) Whlb. Acta Biologica Cracoviensia, Ser. Bot 22: 113–128. Soltis DE, Hibsch-Jetter C, Soltis PS, Chase MW, Farris JS. 1997. Molecular phylogenetic relationships among angiosperms: an overview based on rbcL and 18S rDNA sequences. In: Iwatsuki K, Raven PH, eds. Evolution and diversification of land plants. Tokyo: Springer, 157–176. Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Prince LM, Kress WJ, Nixon KC, Farris JS. 2000. Angiosperm phylogeny inferred from 18S DNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society 133: 381–461.

63

Soltis PS, Soltis DE, Chase MW. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402: 402–404. Soros-Pottruff C, Posluszny U. 1994. Developmental morphology of reproductive structures of Phyllospadix (Zosteraceae). International Journal of Plant Sciences 155: 405–420. Soros-Pottruff C, Posluszny U. 1995. Developmental morphology of reproductive structures of Zostera and a reconsideration of Heterozostera (Zosteraceae). International Journal of Plant Sciences 156: 143–158. Sprotte K. 1940. Untersuchungen u¨ ber Wachstum und Nervatur der Fruchtbla¨ tter. Botanisches Archiv 40: 463–506. Stenar H. 1935. Embryologische Beobachtungen u¨ ber Scheuchzeria palustris L. Botaniska Notiser 1935: 78–86. Sterling C. 1979. Comparative morphology of the carpel in the Liliaceae: Tofieldieae. Botanical Journal of the Linnean Society 79: 321–332. Stevenson DW, Davis JI, Freudenstein JV, Hardy CR, Simmons MP, Specht CD. 2000. A phylogenetic analysis of the monocotyledons based on morphological and molecular character sets, with comments on the placement of Acorus and Hydatellaceae. In: Wilson KL, Morrison DA, eds. Monocots: systematics and evolution. Collingwood, Victoria: CSIRO Publishing, 17–24. Stevenson DW, Loconte H. 1995. Cladistic analysis of monocot families. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ, eds. Monocotyledons, systematics and evolution. Kew: Royal Botanic Gardens, 543–578. Stopes MC, Fujii K. 1910. Studies on the structure and affinities of Cretaceous plants. Philosophical Transactions of the Royal Society of London 201 B: 1–90. Suessenguth K. 1921. Beitra¨ ge zur Frage des systematischen Anschlusses der Monocotylen. Beihefte zum Botanischen Centralblatt 38: 1–79. Svedelius N. 1904. On the life history of Enalus acoroides. Annals of the Royal Botanic Garden Peradenya 2: 267–297. Svedelius N. 1910. Om den florala organisationen hos Arace´ sla¨ ktet Lagenandra. Svensk Botanisk Tidskrift 4: 225– 252. Swamy BGL, Krishnamurty KV. 1970. On the so-called endothelium in the monocotyledons. Phytomorphology 20: 262–269. Swamy BGL, Lakshmanan KK. 1962. Contribution to the embryology of the Najadaceae. Journal of the Indian Botanical Society 41: 247–267. Takaso T, Bouman F. 1984. Ovule ontogeny and seed development in Potamogeton natans L. (Potamogetonaceae) with a note on the campylotropous ovule. Acta Botanica Neerlandica 33: 519–533. Takeuchi Y. 1971. Embryo sac development in Dioscorea izuensis Akahori. Science Reports of the Toˆ hoku Imperial University, Ser IV (Biol) 35: 225–229. Takeuchi Y. 1972. Embryo sac development in Dioscorea japonica Thunb. and D. quinqueloba Thunb. Acta Phytotaxonomica Geobotanica 25: 57–60. Takeuchi Y, Kimura C. 1968. On the embryo sac formation of Dioscorea nipponica Makino and D. tokoro Makino. Sci-

64

A. IGERSHEIM ET AL.

ence Reports of the Toˆ hoku Imperial University, Ser IV (Biol) 34: 137–140. Takhtajan A. 1997. Diversity and classification of flowering plants. New York: Columbia University Press. Tamura MN. 1998. Nartheciaceae. In: Kubitzki K, ed. The families and genera of vascular plants III. Berlin: Springer, 381–392. Tanaka N, Setoguchi H, Murata J. 1997. Phylogeny of the family Hydrocharitaceae inferred from rbcL and matK gene sequence data. Journal of Plant Research 110: 329–337. Tassi F. 1900. Sulla struttura dell’ovulo dell’Hydromistria stolonifera G.F.W. Mey. Bulletino del Laboratorio ed Orto Botanico, Siena 3: 81–88. Teryokhin ES, Chubarov SI. 1991. The embryological and carpological investigation of Althenia filiformis (Zannichelliaceae). Botanicheskij Zhurnal, Moscow & Leningrad 76: 226–236. Teryokhin ES, Chubarov SI, Romanova O. 1997. The anthecology of the species of Potamogeton (Potamogetonaceae). The modes of pollination and systems of crossing. Botanicheskij Zhurnal, St. Petersburg 82 (10): 14–25. Thorne RF. 1992. Classification and geography of the flowering plants. Botanical Review 58: 225–348. Tillich H-J. 1985. Keimlingsbau und verwandtschaftliche Beziehungen der Araceae. Gleditschia 13: 63–73. Tomlinson PB. 1969. On the morphology and anatomy of turtle grass, Thalassia testudinum (Hydrocharitaceae). III. Floral morphology and anatomy. Bulletin of Marine Science 19: 286–305. Tomlinson PB. 1982. Helobiae (Alismatidae) (including the seagrasses). In: Metcalfe CR, ed. Anatomy of the monocotyledons. Oxford: Clarendon Press. Tomlinson PB, Posluszny U. 1978. Aspects of floral morphology and development in the seagrass Syringodium filiforme (Cymodoceaceae). Botanical Gazette 139: 333–345. Troll W. 1931. Beitra¨ ge zur Morphologie des Gynaeceums. ¨ ber das Gynaeceum der Hydrocharitaceen. Planta 14: I. U 1–18. Troll W. 1932. Beitra¨ ge zur Morphologie des Gynaeceums. ¨ ber das Gynaeceum von Limnocharis Humb. et Bonpl. II. U Planta 17: 453–460. Troll W. 1933. Beitra¨ ge zur Morphologie des Gynaeceums. ¨ ber das Gynaeceum der Nymphaeaceen. Planta 21: IV. U 447–485. Tucker SC, Douglas AW. 1996. Floral structure, development and relationships of paleoherbs: Saruma, Cabomba, Lactoris and related Piperales. In: Taylor DW, Hickey LJ, eds. Flowering plant origin, evolution and phylogeny. New York: Chapman & Hall, 141–175. Uhl NW. 1947. Studies in the floral morphology and anatomy of certain members of the Helobiae. Unpublished D. Phil. Thesis, Cornell University. Utech FH. 1978. Floral vascular anatomy of Pleea tenuifolia Michx. (Liliaceae-Tofieldieae) and its reassignment to Tofieldia. Annals of the Carnegie Museum 47: 423–454. van Bruggen HWE. 1985. Monograph of the genus Aponogeton. Bibliotheca Botanica 137: 1–76.

van Bruggen HWE. 1998. Aponogetonaceae. In: Kubitzki K, ed. The families and genera of vascular plants IV. Berlin: Springer, 21–25. van Heel WA. 1983. The ascidiform early development of free carpels, a S.E.M.-investigation. Blumea 28: 231–270. van Heel WA. 1988. On the development of some gynoecia with septal nectaries. Blumea 33: 477–504. van Tieghem P. 1867. Recherches sur la structure des Aroide´ es. Annales des Sciences Naturelles, Botanique, Se´ r. 5 6: 72–210. van Tieghem P. 1871. Recherches sur la structure du pistil et sur anatomie compare´ e de la fleur. Paris: Imprimerie Nationale. van Tieghem P. 1907. Remarques sur l’organisation florale et la structure de l’ovule des Arace´ es. Annales des Sciences Naturelles, Botanique, Se´ r. 9 5: 312–320. Va´ zquez-Santana S, Engleman EM, Martı´nez-Mena A, Ma´ rquez-Guzma´ n J. 1998. Ovule and seed development of Lacandonia schismatica (Lacandoniaceae). American Journal of Botany 85: 299–304. Vergara F, Ferra´ ndiz C, Meyerowitz E, Alvarez-Buylla ER. 1999. Molecular basis and evolution of the insideout flower of Lacandonia schismatica. XVI International Botanical Congress, St. Louis, USA, Abstracts, 188. Vesque J. 1878. De´ veloppement du sac embryonnaire des phane´ rogames angiospermes. Annales des Sciences Naturelles, Botanique, Se´ r. 6 6: 237–285. Vesque J. 1879. Nouvelles recherches sur le de´ veloppement du sac embryonnaire des phane´ rogames angiospermes. Annales des Sciences Naturelles, Botanique, Se´ r. 6 8: 261– 390. Vignoli L. 1939. Gametofiti e cromosomi di Ambrosinia bassii L. Lavori del Reale Instituto Botanico di Palermo 10: 54–80. Vijayaraghavan MR, Kapoor T. 1980. Cytochemical studies of secretory cells and substances in a subaquatic angiosperm Najas flexilis. In: Periasamy K, ed. Histochemistry, developmental and structural anatomy of angiosperms: a symposium. Tiruchirapalli: P & O Publications, 300–304. Vijayaraghavan MR, Kumari Vidya A. 1974. Embryology and systematic position of Zannichellia palustris L. Journal of the Indian Botanical Society 53: 292–302. Visayenskaya TD. 1985. Araceae. In: Takhtajan A, ed. Anatomia seminum comparativa, I. Leningrad: Nauka, 264–275. ¨ l beim Kalmus, ¨ ber das a¨ therische O von Schantz M. 1958. U Acorus calamus L. Acta Botanica Fennica 59: 1–138. Vuille F-L. 1987. Reproductive biology of the genus Damasonium (Alismataceae). Plant Systematics and Evolution 157: 63–71. Walker JW. 1976. Comparative pollen morphology and phylogeny of the ranalean complex. In: Beck CB, ed. Origin and early evolution of angiosperms. New York: Columbia University Press, 241–299. Walker JW. 1986. Classification and evolution of the monocotyledons. American Journal of Botany 73: 746. Walker JW, Walker AG. 1985. Ultrastructure of Lower

GYNOECIUM IN BASAL MONOCOTS Cretaceous angiosperm pollen and the origin and early evolution of flowering plants. Annals of the Missouri Botanical Garden 71: 464–521. Wang QF, Chen JK. 1997. Floral organogenesis of Caldesia parnassifolia (Bassi ex L.) Parl. (Alismataceae). Acta Phytotaxonomica Sinica 35: 289–292. Wang YG, Wang QF, Chen JK, Yuan XP. 1998. Floral organogenesis of Ranalisma rostratum (Alismataceae). Acta Botanica Yunnanica 20: 303–308. Ward HM. 1880. A contribution to our knowledge of the embryo-sac in angiosperms. Journal of the Linnean Society, Botany 57: 519–546. Weber M, Igersheim A. 1994. ‘Pollen buds’ in Ophiorrhiza (Rubiaceae) and their role in pollenkitt release. Botanica Acta 107: 257–262. Weberling F. 1970. Weitere Untersuchungen zur Morphologie des Unterblattes bei den Dikotylen V. Piperales. Beitra¨ ge zur Biologie der Pflanzen 46: 403–434.

65

Wiegand KM. 1898. Notes on the embryology of Potamogeton. Botanical Gazette 25: 116–117. Wiegand KM. 1900. The development of the embryo sac in some monocotyledonous plants. Botanical Gazette 30: 25–47. Wirz H. 1910. Beitra¨ ge zur Entwicklungsgeschichte von Sciaphila spec. und von Epirrhizanthes elongata Bl. Flora 101: 395–446. Witmer SW. 1937. Morphology and cytology of Vallisneria spiralis L. American Midland Naturalist 18: 309–333. Wylie RB. 1904. The morphology of Elodea canadensis. Botanical Gazette 37: 1–22. Wylie RB. 1917. The pollination of Vallisneria spiralis. Botanical Gazette 63: 135–145. Zazhurilo KK, Kuznetsova EA. 1939. The nature of diffuse placentation in the analysis of Nymphaeaceae and Butomaceae. Acta Universitatis Voronegiensis 10 (5): 79–98.