Podostemaceae Podostemaceae L. Richard ex C ...

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Podostemaceae Podostemaceae L. Richard ex C. Agardh, Aphor. Bot.: 125 (1922), nom. cons. Tristichaceae J.C. Willis (1915). C.D.K. Cook and R. Rutishauser

Annual or perennial, aquatic herbs, often bizarre in form, sometimes resembling lichens, bryophytes, seaweeds, or unlike any other plants; haptophytes, attached by adhesive hairs to rock or other hard objects in flowing freshwater, mostly in rapids and waterfalls; roots usually photosynthetic, creeping or partly floating, thread-like, ribbon-shaped, crustose (foliose), sometimes short-lived or absent. Shoots nearly always arising as endogenous buds from roots; stems reduced or elongate, simple or branched, sometimes dimorphic, occasionally only present when flowering. Photosynthesis takes place under water, flowers or even separate floral shoots develop as the water level drops, the vegetative shoots or leaves often shed as plants become exposed. Phyllotaxis variable, in Podostemoideae usually distichous. Leaves borne on elongate stems or arising from prostrate, often disk-like stems, extremely variable in size and shape, from scale-like to well developed and compound; sheaths single or, in many Podostemoideae, double; sheath lobes sometimes elongated into stipule-like appendages; leaf blades stalked or sessile, entire, lobed or dissected; blade lobes or segments often bearing photosynthetic filaments and/or additional hairs; ultimate leaf segments filiform, linear or spathulate. Flowers bisexual, actinomorphic or zygomorphic, solitary, in clusters or in racemeor cyme-like inflorescences; flower buds naked in Weddellinoideae and some Tristichoideae, surrounded by a cupula (a collar-like vascularised cup) in some Tristichoideae, or completely enclosed in a spathella (a tubular or sack-like cover) in Podostemoideae; spathellas mostly enclosing a single sessile or pedicellate flower; pedicels often elongating in fruit. Anthesis takes place in air or flowers cleistogamous under water. Perianth of 1 complete or incomplete whorl of tepals, often confined to one side of the flower; tepals in Tristichoideae and Weddellinoideae large, 5 or rarely 4 or 6, imbricate and sepal-like; tepals in Podostemoideae small, 2–20, linear or subulate, usually alternating with

stamens, in flowers with only 2 basally fused stamens occasionally an additional tepal borne at top of andropodium (common stalk); stamens 1–40, in 1 or 2 complete whorls, or in 1 incomplete whorl, or confined to one side of flower and consisting of 1–3 free stamens or a Y-shaped structure consisting of an andropodium carrying 2 stamens; filaments, when in whorls, mostly free or, in Tulasneantha, their bases united to form an androecial tube; anthers dehiscing longitudinally by slits, introrsely to latrorsely or rarely extrorsely; pollen shed in monads, dyads or (rarely) tetrads, tricolporate in Weddellinoideae, tricolpate to pentacolpate in Podostemoideae, pantoporate with up to 16 pores in Tristichoideae; ovary superior, 2- or 3-locular or 1-locular in some Podostemoideae; ovules axile, anatropous, bitegmic, tenuinucellate. Fruit a capsule, smooth or ribbed, with 2 or 3, equal or unequal valves, sometimes one or more persisting; stigmas 1–3, variable in shape and size. Seeds 2 to very numerous (over 2,000); seed coat usually mucilaginous and sticky; endosperm 0; embryo straight, with 2 cotyledons and a suspensor. The family consists of 49 genera, of which 26 (53%) are monotypic or nearly so (some have two doubtfully distinct species) and about 280 species. It is distributed worldwide in tropical and warm regions, extending into temperate eastern North America and temperate East Asia. Most of the species are endemic to small geographical areas; only one, Tristicha trifaria, is widespread and occurs in the Old and New Worlds. Vegetative Morphology. The interpretation of the vegetative body is controversial. Many Podostemaceae have a flattened photosynthetic body which adheres to a hard substrate. It has been called a ‘thallus’ because the conventional demarcation into stem, leaf and root is usually not obvious (Cario 1881; Willis 1902), and various botanists have denied or doubted the homology of this vegetative body with stems (caulomes),

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leaves (phyllomes) and roots of other angiosperms (G. Cusset 1974; Cusset and Cusset 1988; C. Cusset 1992; Mohan Ram and Sehgal 1992, 2001; Schnell 1994, 1998; Khosla et al. 2000; Ota et al. 2001; Sehgal et al. 2002). These botanists consider the vegetative body of all (or most) Podostemaceae represents a unique architectural type. However, for convenience, we adopt the classical root-shoot model (CRS model) with its structural categories roots, shoots (including stems and leaves) as used by Warming (e.g. 1881), Goebel (1933), Rauh (1937), Troll (1941), Jäger-Zürn (e.g. 1970, 2000c), Rutishauser and Huber (1991) and Rutishauser (1997). We avoid the term ‘thallus’. We use the term ‘root’ for cylindrical to flattened photosynthetic structures when endogenous shoot buds are developed but no exogenous leaves. The term ‘stem’ is applied to a cylindrical or flattened photosynthetic body which develops exogenous leaves. For example, the prostrate and crustose body of Hydrobryum (Fig. 104C) and Zeylanidium olivaceum, which lacks exogenous leaves, is described as a root (Jäger-Zürn 2000b; Rutishauser and Moline 2005). The prostrate and often star-shaped body of Dalzellia zeylanica is described as a flattened stem or branch system because it bears exogenous scales which are often interpreted as leaves (Jäger-Zürn 1995; Imaichi et al. 2004). Podostemaceae show an amazing diversity of root types. Usually, the roots are persistent with long-lasting apical growth, bearing root-borne shoots and fixed to the hard substrate by adhesive hairs (Fig. 107A). They vary from thread-like

(cylindrical) to ribbon-like and further to crustose (i.e. foliose, disk-like). The roots give rise to endogenous shoot buds, either from the flanks or in crustose roots also from the upper surface (Fig. 104C). Cylindrical to narrowly ribbon-like roots of Podostemaceae are normally provided with an asymmetric cap which resembles the calyptra of a typical root (Fig. 104A; Koi and Kato 2003). Broad ribbons and crustose (i.e. foliose, disk-like) roots often lack an obvious cap. Lateral roots of ribbon-like roots arise endogenously or exogenously (Fig. 104B), or show a mosaic pattern of endogenous and exogenous formation (e.g. Cladopus spp., Koi and Kato 2003). Crustose roots are found especially in Asian Podostemoideae (e.g. Hydrobryum, Zeylanidium olivaceum) and African Podostemoideae (e.g. Dicraeanthus, Ledermanniella spp.; Cusset 1984). The crustose root of Hydrobryum contains a network of nonvascular strands (Ota et al. 2001). The crustose roots of Hydrobryum grow with a marginal meristem giving rise to exogenous lobes. The margin of these flat roots are fringed by a protective tissue which may be considered as a rudimentary cap (Suzuki et al. 2002). A progressive elaboration of the root is most obvious in Asian and Australian Podostemoideae where it is accompanied by gradual reduction of the cap (calyptra) and decrease in size of the root-borne leafy shoots (Willis 1902; Jäger-Zürn 2000a; Suzuki et al. 2002). Crustose roots have evolved at least three times in Podostemaceae, twice in Asian podostemoids and at least once in African members (Hiyama et al. 2002; Kita and Kato 2004b; Moline et al. 2006).

Fig. 104. Podostemaceae. Scanning electron micrographs. A Podostemum ceratophyllum (eastern USA). Root tip with asymmetrical cap (Rc). Scale bar, 300 μm. B Zeylanidium subulatum (southern India). Distal region of exogenously branched root; Rh rhizoids along lower side of mother root, Rx exogenous daughter roots, Sn first leaf of endogenous shoot at the tip of mother root. Scale bar, 500 μm. C Hydrobryum floribundum (southern Japan). Marginal region of lobed foliose root, seen from above. Sn first leaves of endogenous shoot arising from the upper surface. Scale bar, 300 μm. D Podostemum ceratophyllum (eastern USA). Basal portion of double-sheathed mother leaf (Ly), with 2 lateral stipular sheaths (Ls), each ensheathing a daughter leaf (Ly+1). Scale bar, 100 μm. E Tristicha malayana (Malaysia). Distal portion of nearly mature ramulus (photosynthetic branchlet) with 3 rows of scales. Scale bar, 500 μm. F Weddellina squamulosa (Venezuela). Branching zone of vigorous vegetative shoot; large toothed scale (L) at level of shoot branching; arrows point to the 2 rows of photosynthetic fil-

aments which are restricted to 2 furrows along shoot axes. Scale bar, 500 μm. G Mourera fluviatilis (Venezuela). Early stage of flower development; stamen primordia (A) in 2 complete whorls surrounding ovary (G); T tepals, Fc remnant of removed spathella. Scale bar, 100 μm. H Marathrum schiedeanum (Mexico). Flower immediately prior to anthesis, with half-whorl of 4 stamens; T tepals. Note the 2 stigmas which are basally united. Scale bar, 1 mm. I Polypleurum stylosum (southern India). Flower in anthesis; Yshaped androecium with androphore (P) carrying 2 stamens; T tepal. Scale bar, 1 mm. J Tristicha trifaria (Nigeria). Flower in anthesis; with trimerous, basally tubular perianth (T), 1 stamen, 3 stigmas. Scale bar, 500 μm. K Mourera fluviatilis (Venezuela). Tricolpate spinulose pollen. Scale bar, 5 μm. L Farmeria indica (southern India). Dyad of pentacolpate pollen grains; 3 colpi per grain visible. Scale bar, 10 μm. M Weddelina squamulosa (Venezuela), 2 tricolporate pollen grains. Scale bar, 5 μm. (Adapted from Rutishauser 1997)

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In several genera the roots are insufficiently documented. There are a few species which lack obvious roots, e.g. Castelnavia princeps, Dalzellia zeylanica, Mourera fluviatilis and Rhyncholacis carinata, although other species in the same genera are clearly provided with roots (Warming 1899; Rutishauser and Grubert 1994; Mathew et al. 2001). Holdfasts (haptera in earlier literature) are clawlike organs superficially resembling the attachment organs of brown algae such as Fucus. They stick the plants to the solid substratum. They may be branched (e.g. Polypleurum spp.) or finger-like (e.g. Saxicolella submersa, Ameka et al. 2002). They arise as exogenous (e.g. Podostemum ceratophyllum) or endogenous outgrowths (e.g. Indotristicha ramosissima) of the root. Holdfasts may also arise as exogenous outgrowths from the base of leaves and shoots. All Podostemaceae investigated to date have dicotyledonous seedlings. The shoots of most arise as endogenous buds from hypocotyl-borne outgrowths (roots) which soon replace the short-lived seedling axis (Mohan Ram and Sehgal 1997; Sehgal et al. 2002). Seedling establishment by plumular activity seems to be the exception, rather than the rule; it is found in a few New World Podostemaceae such as Apinagia multibranchiata and Mourera fluviatilis (Grubert 1976; Rutishauser and Grubert 2000). More seedling features are described below under Seedlings and Life Cycle. Many African and American members of the Podostemoideae form elongate and branched shoots over 80 cm long (e.g. Ledermanniella bowlingii, Ameka et al. 2003), whereas a reduction in size of the root-borne shoots to 1 cm or less long and often unbranched is typical for most Podostemoideae in Asia. The longest shoots formed by Asian podostemads are those of Indotristicha ramosissima which reach 60 cm. The shoots of several American genera are dorsiventral with respect to leaf orientation. Prostrate crustose shoots attached to the rock are found in, e.g. Dalzellia zeylanica (Tristichoideae, Imaichi et al. 2004) and Apinagia, Castelnavia and Marathrum (Podostemoideae, Rutishauser et al. 1999; JägerZürn 2005c). For additional features of crustose shoots (i.e. dorsiventrally flattened stems), see below the discussion of leaf sheaths. Axillary branches subtended by leaves or bracts are the exception, rather than the rule. They are found in Indotristicha ramosissima, if the ramuli (photosynthetic branchlets) are accepted as subtending compound ‘leaves’ (Rutishauser and Huber

1991). Axillary branching also occurs in African podostemoids, e.g. Saxicolella, Sphaerothylax and Stonesia spp. (Taylor 1953; Ameka et al. 2002). Most, however, have switched to alternative branching types. In several Podostemoideae, we find shoot bifurcation which is correlated with the presence of double-sheathed leaves (Figs. 104D, 116G). In Weddellina (subfam. Weddellinoideae), the vegetative shoots are often highly branched and up to 80 cm long, with scales and bunches of photosynthetic filaments. Branching appears to be extra-axillary, i.e. lateral shoots are not subtended by scale-like leaves (Fig. 104F). The leaf sheaths in American Podostemoideae such as Marathrum, Mourera and Oserya are inserted longitudinally due to leaf growth occurring in the median plane towards the abaxial side of the leaf (Rutishauser and Grubert 1994; Jäger-Zürn 2002b, 2005c). Lateral leaf insertion (as is typical for most angiosperms) is found in Diamantina; the leaves of this genus are minute and lack any vascular tissue (Fig. 109G, H; Rutishauser et al. 2005). In many American Podostemoideae, the root-borne shoots initially produce leaves with a single sheath and subsequently leaves with two sheaths. The two sheaths of a double-sheathed leaf are opposite to each other or nearly so (Podostemum ceratophyllum, Fig. 104D): an inner one pointing towards the stem tip and an outer sheath pointing towards the stem base. These double-sheathed leaves have been called ‘dithecous’ by Warming (1881, 1882). They occur in several American and African Podostemoideae but are lacking in most Asian and Australian Podostemoideae, with the exception of Zeylanidium subulatum (Jäger-Zürn 1994, 1999; Imaichi et al. 2005). Double-sheathed leaves are an evolutionary novelty or key innovation of Podostemoideae and allow unique types of shoot construction (Jäger-Zürn 1994; Rutishauser and Grubert 1999; Rutishauser et al. 2003). The presence of these leaves is linked with the formation of prostrate and often disk-like stems with marginal leaves, especially in American Podostemoideae. For example, new leaves of the prostrate stems of Marathrum spp. may arise in both sheaths of the double-sheathed leaves. The leaf sheaths of species of Castelnavia, Lophogyne and Marathrum in particular appear to be congenitally fused into a widened and flattened body which is prostrate and lobed. This body, as in Castelnavia princeps, may be interpreted as the product of congenital fusion and dorsiventral flattening of various stem

Podostemaceae

orders (Warming 1882; Matthiesen 1908; Engler 1928; Rutishauser et al. 1999; Jäger-Zürn 2005c). The coalescence of leaf sheaths and the supporting stem portion leads to pocket-like cavities in the prostrate body which become filled with new leaves or flower buds. Pocket formation due to congenital fusion of two adjacent leaf sheaths also occurs in taxa with elongate stems, as in Apinagia multibranchiata (Rutishauser and Grubert 2000). In many Podostemoideae, the leaf sheaths can be called ‘stipular’ because they have one or two lobes or teeth which extend beyond the leaf insertion area. Stipular sheaths (two per double-sheathed leaf) are found in several African and American podostemoid genera, e.g. Ledermanniella and Marathrum (Rutishauser et al. 1999; Ameka et al. 2003; Moline et al. 2006). Patterns unique with respect to position and number of stipular outgrowths are found in Podostemum spp. (Fig. 104D; Philbrick and Novelo 2004). In Ceratolacis pedunculatum, Crenias spp. and Podostemum muelleri with dorsiventral shoots, the leaf base is asymmetrical, with only one prominent stipule per leaf, restricted to the front side of the shoot (Tur 1997; Jäger-Zürn 2002a; Philbrick and Novelo 2004; Philbrick et al. 2004b). In Podostemoideae with digitate leaves (Cladopus, Diamantina), it is arbitrary whether one calls the lateral leaf lobes (teeth) stipular appendages or not (Rutishauser and Pfeifer 2002; Rutishauser et al. 2005). In Tristichoideae, a proper shoot apical meristem (SAM) is present, whereas a SAM is lacking or reduced to few meristematic cells in many Podostemoideae (Jäger-Zürn 2005b). In Asian podostemoids (e.g. Cladopus, Zeylanidium spp.) without a SAM, new leaves are formed endogenously on the adaxial side of a pre-existing leaf (Imaichi et al. 2005; Koi et al. 2005). Most taxa of Podostemoideae have distichous phyllotaxis. Leaf formation continues in the same median plane even when doublesheathed leaves or bracts are formed. There are, however, other phyllotactic patterns. For example, in reproductive shoots of Thawatchaia and Willisia the scale-like leaves are arranged around the stem in 4 (or even 6) rows, serving as exoskeleton. Ledermanniella subg. Phyllosoma is characterised by prominent compound leaves with distichous phyllotaxis and additional scales which are scattered irregularly (Cusset 1983). In Indotristicha ramosissima, the photosynthetic branchlets (ramuli) are arranged along a spiral which approaches the Fibonacci angle whereas additional scales along the stem are

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intercalated without obvious order (Rutishauser and Huber 1991; Jäger-Zürn 1992). In Tristicha, the ramuli are arranged in two opposite rows along the often very short stems (Jäger-Zürn 1970; Imaichi et al. 1999). Each ramulus consists of scales arranged in three rows in Tristicha (Fig. 104E) whereas they show spiral or irregular patterns in the ramuli of Indotristicha ramosissima. In Weddellina, stems are bunches of photosynthetic filaments which are arranged in two opposite rows whereas additional scales lack a regular phyllotactic pattern (Fig. 104F). The longest leaves of all Podostemaceae are found in Mourera fluviatilis, where they reach 200 cm. Repeatedly forked blades are typical for many taxa, such as Oserya coulteriana and Podostemum ceratophyllum. In early development, the compound leaves of Marathrum and Rhyncholacis show a three-dimensional branching pattern (Rutishauser 1995, 1997; Rutishauser et al. 1999), and may be repeatedly branched until they terminate in filamentous nonvascular pinnae 0.02–0.4 mm wide, e.g. in Marathrum schiedeanum (Matthiesen 1908). Young leaves and their subunits (pinnae) in Mourera fluviatilis, Oserya spp. and other neotropical taxa are coiled or incurved during development. The side towards which they are coiled or curved may be called the ‘front side’ (‘upper side’) because it is away from the surface of the prostrate shoot which faces the substratum. Ensiform (sword-like) blades are flattened in the median plane and usually provided with marginal pinnae. This median plane is identical to the plane of distichy, resembling leaves of Acorus, Iris and Xyris. Such ensiform and compound leaves are typical for species of Apinagia, Marathrum and Mourera (Jäger-Zürn 2002b, 2005a, c). Shoots of these genera may be also dorsiventral, with appendages (prickles, warts, hair tufts) restricted to the upper surfaces (‘front side’) of the ensiform leaves, e.g. in Apinagia multibranchiata and Mourera fluviatilis (Rutishauser and Grubert 1994, 2000). The leaves of most Asian and Australian Podostemoideae are entire, subulate to filamentous (Fig. 104C). Some of the scale-like leaves of Willisia are provided with a filamentous blade, and in Zeylanidium subulatum these leaves may reach a length of 30 cm (Cusset 1992). Digitate leaves of Cladopus are borne in a seemingly scattered phyllotactic pattern. Similarly to many American Podostemoideae, the blades of several African taxa are repeatedly forked or pinnate but some have entire,

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scale-like to filiform leaves, such as many Asian and a few American taxa. Anisophylly or heterophylly occur in some species of Ledermanniella subg. Phyllosoma: besides normally forked leaves, there are ± toothed, imbricate scales (Cusset 1983, 1987). In a few African Ledermanniella spp. (e.g. L. letouzeyi, L. prasina), epiphyllous flowers arise from the cleft of forked leaves (Schenk and Thomas 2004; Rutishauser and Moline 2005). Tristichoideae have photosynthetic, 1–2 mm long scales which may be replaced by slightly longer filamentous appendages (Warming 1901; Cusset and Cusset 1988). Jäger-Zürn (1997a) considers these to be leaves. In Tristicha and Indotristicha, these scales are arranged in short-lived shootlets (called ramuli) up to 4 cm long (Fig. 104E). Scales and filamentous appendages are only one cell-layer thick, except for a weak prosenchymatic midrib which may be present or absent. Weddellina has bunches of photosynthetic filaments arising in two opposite sectors along the stem (Grubert 1976). These cylindrical filaments are thin and (in section) consist of four cells surrounding a central cavity; they may be interpreted as pinnae of three-dimensional compound leaves (Wächter 1897; Engler 1928); in addition, there are scales of various sizes along the main stems (Fig. 104F). Vegetative Anatomy. Intercellular lacunae such as gas canals and aerenchyma seldom occur, which is very unusual for aquatic vascular plants. The roots, whether flattened or not, of most species adhere to the rocky substratum by usually unicellular adhesive hairs which are called rhizoids by Engler (1928) and Ota et al. (2001). They are usually present on the lower side of the root where it is attached to the rock (Warming 1881). These hairs are reported to secrete a ‘super-glue’ from their tips. The ‘super-glue’ secreted from adhesive hairs and epidermal cells of roots and holdfasts in Griffithella hookeriana is a polysaccharide consisting mainly of arabinose and galactose (Vidyashankari 1988b). Jäger-Zürn and Grubert (2000) observed that this super-glue is associated with biofilm composed primarily of cyanobacteria. The vascular tissue often lacks clear differentiation into xylem and phloem (Schnell 1967, 1998). Typical phloem elements are difficult to find (Romano and Dwyer 1971; Ancibor 1990; Jäger-Zürn 2000c). Typical xylem elements are often absent, except for some annular-thickened tracheids in stems and leaf midribs of Apinagia and Mourera

(Rutishauser and Grubert 1994, 2000). Both xylem and phloem elements are lacking in the ‘nonvascular strands’ of Hydrobryum roots (Ota et al. 2001). The vascular pattern in flattened plant bodies (e.g. Dalzellia zeylanica) was used to support the hypothesis of ‘congenital fusion’ of several branch orders (Jäger-Zürn 1995, 1997a, 2000c). The basal portion of the cylindrical vegetative shoot axis of Weddellina and Apinagia spp. (e.g. A. multibranchiata) may become thickened following cell division in the cortex. Hair-like outgrowths are found along one sector in filiform leaf segments of many Podostemoideae. Certain American Podostemoideae (mainly species of Apinagia, Marathrum and Mourera) have broad leaf blades with fimbriate marginal lobes and a dissected tip. Laticiferous tubes embedded in parenchyma or sclerenchyma in various organs are an anatomical speciality of various neotropical Podostemoideae such as Apinagia, Castelnavia, Marathrum, Mourera, Rhyncholacis and Weddellina (Matthiesen 1908; Engler 1928; Schnell 1967; Rutishauser and Grubert 1994). Long-lived plant parts (roots, stems, occasionally also scales and leaf bases) of many Podostemaceae have a carapace of silica bodies in the epidermal and subepidermal layers. This may help in withstanding mechanical damage and also preventing the plant from collapsing during short periods of desiccation (Metcalfe and Chalk 1950). Similarly to most aquatic plants, Podostemaceae exhibit a great capacity for regeneration from wounded or ruptured portions of the plant body (Imaichi et al. 1999; Ota et al. 2001). Warming (1881) and Hammond (1936) illustrated roots and holdfasts of Podostemum ceratophyllum which had regenerated their tips; new roots and shoots may be also regenerated from injured stems. Inflorescence Structure. Inflorescences are not always easy to define in Podostemaceae because foliage leaves and flowers are often not clearly separate. In Podostemoideae, fascicles, cyme-like and raceme-like inflorescences, and less clearly defined clusters are found. Except for the fascicles, the flowers are normally separated from each other by leaves with prominent blades or bracts with rudimentary blades. 1. Fascicles. In various New World Podostemoideae, there are two or more flowers arising as a fascicle in a sheath pocket (stem cavity) next to the substrate. Such fascicles are typical

Podostemaceae

for Rhyncholacis, Vanroyenella, Wettsteiniola and some species of Apinagia and Marathrum (Warming 1901; van Royen 1951; Tur 1997). In Rhyncholacis penicillata and Vanroyenella plumosa, such fascicles contain up to 25 and 11 flowers respectively; the flowers of each fascicle are initiated successively along a zigzag line resembling a condensed cymose inflorescence, although no subtending bracts are present (Rutishauser et al. 1999). 2. Cyme-like inflorescences. Various Apinagia spp. with stems (including A. multibranchiata) have repeated Y-shaped branching, understandable as peculiar types of cymose inflorescences (Warming 1888; Rutishauser and Grubert 2000; Jäger-Zürn 2002b, 2005a, c). The first module of a root-borne shoot consists of few to several leaves and an apparently terminal flower. Then, all additional daughter modules consist of a leaf pair with a flower in between. These leaves are often doublesheathed, i.e. provided with an adaxial inner sheath and an abaxial outer sheath. In A. multibranchiata and allies, the two inner sheaths of a leaf pair form a tube protecting the young flower. When both outer sheaths of a leaf pair subtend a daughter module, reproductive shoots occur with repeated Y-shaped branching. Species such as Apinagia riedelii have reproductive modules of a solitary doublesheathed leaf and one flower only. A chain of such reduced modules was called drepanium (‘Sichelsympodium’) by Engler (1928) and Jäger-Zürn (2005c) because the daughter modules are regularly borne on the same side. 3. Raceme-like inflorescences. Distinctive raceme-like inflorescences resembling swords are found in Mourera (Warming 1888). In M. fluviatilis, they are up to 64 cm long (including stalk), with about 40–90 flowers arranged along two flanks of the axis. The flowers along both rows are separated from each other by double-sheathed bracts which are initiated in basipetal order after the formation of a terminal double-sheathed leaf (Rutishauser and Grubert 1994, 1999). 4. Clusters. Various inflorescences of African Podostemoideae show dense groups of flowers which are here called ‘clusters’, for lack of a better term. In Dicraeanthus africanus, stalked flower clusters arise from endogenous buds of the stem cortex (Fig. 115H; Moline et al. 2006). In Macropodiella macrothyrsa,

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similar candelabrum-like clusters of up to about 12 flowers are arranged as short shoots along the main shoots. These clusters have double-sheathed bracts between neighbouring flowers and were interpreted as cymose inflorescences by Cusset (1978). According to Jäger-Zürn (2000a, 2000c), the flower clusters of Sphaerothylax abyssinica are helicoid and scorpioid cymes with congenital fusion (syndesmy) of consecutive branch orders. In Tristichoideae, solitary flowers develop at the tip of short shoots which bear either scales only in Dalzellia, or scales as well as ramuli in Indotristicha and Tristicha (Cusset and Cusset 1988). Unbranched short shoots with a terminal flower arise directly from endogenous buds of the green, flattened plant body in Dalzellia zeylanica (Imaichi et al. 2004), or of the root, as in Tristicha, or they may be exogenous, arising from branches of vigorous and branched vegetative shoots, as in Indotristicha and Tristicha. In Indotristicha ramosissima, additional floral shoots may also arise as endogenous buds along the vegetative shoot axes (Rutishauser and Huber 1991). The root-borne shoots of Weddellina squamulosa are dimorphic. Floral shoots are unbranched and 2–12 cm long. They bear 2–10 scales which are often arranged in a helix which continues into the usually 5-merous perianth of the single terminal flower (Fig. 105C, D).

Fig. 105. Podostemaceae-Weddellinoideae. Weddellina squamulosa. A Sterile shoot with photosynthetic filaments and scales (2 cm). B Sterile shoot with scales (1.5 cm). C Root with endogenous holdfasts and a fertile shoot with terminal capsule (1 cm). D Flower (2.5 mm). (Orig. Cook)

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Flower Structure. Podostemoideae are distinguishable from the two other subfamilies by the presence of a membranous, nonvascularised sacklike cover, the spathella, which encloses the young flower (Fig. 104G). Except for Macarenia, each spathella contains a single flower. In Marathrum foeniculaceum and Mourera fluviatilis, the young spathella is two-tipped, supporting the view that the spathella is formed by two fused bracts (Rutishauser and Grubert 1994; Jäger-Zürn 2005b). Diamantina has two different kinds of spathella on the one shoot; the spathella subtending the subterminal flower is scale-like and positionally homologous to a bract, whereas the spathella covering the terminal flower bud is tubular, as is usual for Podostemoideae (Rutishauser et al. 2005). In addition to a sheathing perianth, some Tristichoideae have a cover which encloses the young flower. This cup-like, vascularised cover, called a cupule, is found in Dalzellia zeylanica and Indotristicha ramosissima. Unlike the spathella, the cupule carries scales and (in Indotristicha) also photosynthetic shootlets which are called ramuli (Rutishauser and Huber 1991; Jäger-Zürn and Mathew 2002). In most Podostemaceae (including Tristichoideae, Weddellinoideae), the pedicel (flower stalk) elongates as the fruit ripens. The pedicel in Podostemoideae is inside the spathella, but in a few members (e.g. Angolaea, Ceratolacis pedunculatum) the spathella is itself clearly stalked or pedunculate (Warming 1899; Philbrick et al. 2004b). The pedicel is lacking or very short prior to anthesis in Podostemoideae with erect flower buds, but some African taxa have an inverted and pedicellate flower bud inside the spathella, and in these taxa the pedicel elongates inside the young spathella prior to anthesis (Cusset 1987; Ameka et al. 2003). An intermediate condition with oblique flower buds inside the spathella occurs in Endocaulos, Thelethylax in part and Djinga (Moline et al. 2006). Pedicels more than 5 cm long are common in New World Podostemoideae with prostrate stems and pedicel insertion close to the substrate. A short and asymmetrically inflated pedicel is typical for Castelnavia. In Podostemoideae, the number of perianth segments varies from 2 to 25; the number of stamens per flower varies from 1 to 40. The perianth is reduced to linear, spathulate or tooth-like tepals (Fig. 104H, I) which, according to Khosla and Mohan Ram (1993), may be interpreted as staminodes because they are occasionally replaced by stamens. The flowers may be placed in five goups:

1. Various species of the American genera Apinagia, Marathrum and Rhyncholacis have a complete whorl of 6–12 stamens surrounding the dimerous gynoecium (Rutishauser 1997; Rutishauser et al. 1999). The number of stamens equals the number of tooth-like tepals; the tepals alternate with the stamens. 2. Polystemonous flowers with stamens outnumbering the tepals and arranged in up to 2 whorls are found in various species of Apinagia, Rhyncholacis and Mourera (Fig. 104G). In Apinagia multibranchiata, there are 6–29 stamens per flower (Went 1926; Rutishauser and Grubert 2000), while there are 4–40 stamens per flower in Marathrum squamosum (van Royen 1951) and 14–40 stamens in Mourera fluviatilis (Rutishauser and Grubert 1994, 1999). 3. In many New World Podostemoideae, the flowers become dorsiventral by loss of stamens on one side. Marathrum schiedeanum, for example, has 4–8 stamens in a complete or incomplete whorl, although there may still be a complete whorl of rudimentary tepals (Fig. 104H; Rutishauser et al. 1999). In Castelnavia princeps and Vanroyenella, there are two or three stamens which may be free or slightly united below (forming an andropodium; Fig. 114C; Warming 1882). From the Old World Podostemoideae, only Angolaea is known to have three stamens, and these are free (Fig. 115C). 4. Many Podostemoideae, including most from the Old World, are characterised by flowers with two stamens having an andropodium at least 1 mm long. Thus, the androecium appears to be Y-shaped (Fig. 104I), and the family name ‘Podostemaceae’ (based on the genus Podostemum) refers to this distinctive feature. In all members with plagiotropous floriferous shoots (e.g. Castelnavia spp., Zeylanidium olivaceum, Fig. 124E), the andropodium is situated towards the substratum (Willis 1902; Jäger-Zürn 2000b). In Zeylanidium lichenoides, there are exceptional flowers with 3 or 4 stamens with 2 tepals inserted at different levels along the andropodium (Mathew and Satheesh 1997). Three stamens per andropodium occasionally occur in species of African genera such as Ledermanniella, Leiothylax, Macropodiella, Winklerella and Zehnderia (Engler 1928; Cusset 1987; Léonard 1993), while some populations of Podostemum ceratophyllum have a high percentage of flowers with 3–7 stamens per andropodium

Podostemaceae

(Philbrick and Bogle 1988). On the other hand, there is sometimes only a single stamen in, e.g. Letestuella tisserantii and Oserya coulteri (Warming 1899; Taylor 1953; Cusset 1980, 1987). 5. In a few species, there is only one stamen per flower associated with two lateral tepals, e.g. Polypleurum schmidtianum (Fig. 118G); the other species of Polypleurum usually have one stamen per flower and an andropodium (Cusset 1992). Three tepals, one on each side of the solitary stamen and one on the back of it, are found in Devillea (syn. Podostemum flagelliforme, Philbrick and Novelo 2004). In Tristichoideae, the perianth is in one whorl with three imbricate, sepal-like segments which protect the flower. The three tepals are basally fused or nearly free (Fig. 104J). The tristichoid flower usually has three stamens, except for the widespread Tristicha trifaria which has one or, more rarely, two or three stamens (Cusset and Cusset 1989). The monotypic subfamily Weddellinoideae has 4–6 free, imbricate tepals. In contrast to the usually veinless scales along the floral shoots, the tepals contain a minute vascular bundle. The flowers have 5–25 stamens (Fig. 105D; Jäger-Zürn 1997b; Rutishauser 1997). Podostemoideae with several stamens, such as species of Marathrum, Mourera and Rhyncholacis, tend to have elongate, 2–4 mm long anthers which are sagittate at their base (Fig. 104H), whereas the anthers of taxa with one or two stamens per flower are usually broader and shorter (Fig. 104I). The anthers mostly dehisce introrsely (to latrorsely), but the anthers of some species of the American genera Apinagia, Jenmaniella and Oserya are extrorse (van Royen 1951). The anthers of all tristichoid taxa are introrse and considerably flattened; they have a connective tip and a sagittate to cordate base (Fig. 104J; Cusset and Cusset 1988). The anthers of Weddellina are X-shaped, deeply emarginate at the top and cordate-sagittate at the base. Various Podostemoideae have a stalked ovary. Especially African taxa with an inverted flower in the unruptured spathella have a gynophore – a stalk-like structure which separates the ovary (capsule) from the insertion level of androecium and perianth. In Leiothylax and Zehnderia, the gynophore of mature capsules is up to 3 and 8 mm long respectively. A short gynophore is also found in a few American taxa (Cipoia, Diamantina; Philbrick et al. 2004a). The ovary of many

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Podostemoideae is bicarpellate and usually bilocular, with a prominent central placenta and a thin septum. Bilocular ovaries represent the plesiomorphic condition in Podostemonoideae, occurring in most non-African members and some African-Madagascan taxa such as Endocaulos, Sphaerothylax, Thelethylax and Saxicolella in part (Jäger-Zürn 2000c; Ameka et al. 2002). Most African members have unilocular ovaries, occasionally with a rudimentary septum at the very base (Ameka et al. 2003). There are normally two free, linear stigmas (Fig. 104I). Some species, e.g. Hydrobryum griffithii, Zeylanidium lichenoides, are variable in stigma shape: in both taxa, . . . “every stage may be found from simple, narrow, subulate to broadly obcuneate with many teeth” (Willis 1902). The two stigmas of all Crenias spp., except one, are multilobed whereas the closely related Podostemum has two entire stigmas (Warming 1882; see also Philbrick and Novelo 2004 who sunk Crenias into Podostemum). A few taxa show stigmatic lobes which are united basally into a short stylar region (Marathrum schiedeanum, Fig. 104H). A single semi-globose stigma is found in Angolaea. Tristichoideae have three simple, linear stigmas. The stigmas may be almost smooth (Tristicha trifaria) or hairy (Indotristicha ramosissima; Rutishauser and Huber 1991). The gynoecium of Weddellina (Weddellinoideae) consists of a bilocular ovary and a globular, papillose stigma. Weddellina shares the apical septum of the ovary with basal podostemoid genera such as Apinagia, Marathrum, Mourera and Rhyncholacis (Jäger-Zürn 1997b, 2003a, b). Embryology. Starting with Warming (1882), the embryology of various (especially Indian) members of Podostemaceae has been studied; summaries were given by Davis (1966), Kapil (1970), Battaglia (1987), Johri et al. (1992) and Mohan Ram and Sehgal (2001). Embryological data on African and American Podostemaceae, however, are scarce (Jäger-Zürn 1997b; Murguía-Sánchez et al. 2001, 2002). The ovules are anatropous, bitegmic and tenuinucellate. The inner integument is much shorter than the outer one, with the nucellus much exceeding the inner integument in all three subfamilies. Embryo sac development takes place in the nucellar region which projects beyond the inner integument. In all Podostemaceae investigated to date, the embryo sac deviates considerably from the usual

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pattern of angiosperms. A 4-celled embryo sac develops from four nuclei, the micropylar quartet, in the apical portion of the nucellus, whereas the basal nucellar region gives rise to a ‘nucellar plasmodium’, also called a ‘pseudo-embryo sac’. There are no antipodals. Embryo sac development of all Podostemaceae may be interpreted as following a reduced Allium type (Jäger-Zürn 1997b; MurguíaSanchez et al. 2001, 2002). Double fertilization has not been observed in Podostemaceae (observations in, e.g. Razi 1955, are doubtful). Thus, most, if not all Podostemaceae have single fertilization, the polar cell degenerating without being fertilized. Consequently, there is no endosperm, and its nutritive role is performed by the nucellar plasmodium. Embryogeny is always of the Solanad type (Engler 1928; Kapil 1970). Pollen Morphology. Pollen grain numbers per anther have been determined for a few Podostemaceae; for example, there are as few as 1,000 pollen grains per anther in Tristicha whereas there are up to more than 25,000 grains per anther in Apinagia longifolia and Mourera fluviatilis (Okada and Kato 2002). The pollen grains are relatively small: mean pollen diameter is 11–25 μm. The grains are typically spherical to ellipsoid, microechinate, with a tectate-granular sexine (ectexine) and a lamellar and/or granular nexine (endexine) in non-apertural regions. A tectate-columellate sexine, as is found elsewhere in most non-aquatic eudicots, is lacking in Podostemaceae. This granular exine architecture may be of adaptive significance for the aquatic habit (O’Neill et al. 1997; Osborn et al. 2000). Characters which vary among the taxa include the dispersal unit (grains may be dyads or tetrads), surface sculpture, infratectal granule size, and aperture morphology (Bezuidenhout 1964; O’Neill et al. 1997; Lobreau-Callen et al. 1998). In the presumably basal New World genera of Podostemoideae such as Apinagia, Marathrum, Mourera and Rhyncholacis, the pollen grains are shed in monads (Fig. 104K). In more derived Podostemoideae, including all Asian, Australian and many African taxa, they are in dyads (Fig. 104L; Bezuidenhout 1964; Jäger-Zürn 1967; Miyoshi and Kato 1982; Philbrick 1984; Vartak and Kumbhojkar 1984; Lobreau-Callen et al. 1998). Diamantina is the only genus which produces pollen in tetrads (Philbrick et al. 2004a). The grains of most Podostemoideae are echinate (spinulose) and tricolpate, but some species also have tetracolpate

and even pentacolpate grains, e.g. Farmeria indica, Oserya coulteriana and Polypleurum stylosum (Fig. 104L; O’Neill et al. 1997). In Tristichoideae, the pollen is spherical and pantoporate with up to 16 pores which are often inconspicuous (Tristicha trifaria, Bezuidenhout 1964; O’Neill et al. 1997; Osborn et al. 2000). The grains of Weddellina squamulosa are ellipsoidal, tricolporate and rugulo-areolate (Fig. 104M; van Royen 1953; Lobreau-Callen et al. 1998). Occurrence of monads in Podostemaceae seems to be correlated with simultaneous microsporogenesis, whereas dyads are found in podostemoid taxa (e.g. Polypleurum, Zeylanidium) with successive microsporogenesis (Jäger-Zürn et al. 2005). Anthesis and Pollination. Anthesis of most Podostemaceae takes place in the air, or flowers developing under water may be cleistogamous (Philbrick 1984). The duration of anthesis is known for only a few species. Grubert (1974) observed that it lasted 4–5 h in Weddellina and 1 day in Apinagia multibranchiata, Rhyncholacis penicillata and Mourera fluviatilis, whereas in Marathrum rubrum it was 3 or 4 days, according to Philbrick and Novelo (1998). Some American Podostemoideae (especially species of Apinagia, Mourera and Rhyncholacis) and Weddellina are polystemonous and pollinated by insects (e.g. Trigona bees), although additional wind pollination cannot be excluded (Gessner and Hammer 1962; Grubert 1974; Okada and Kato 2002). Wind pollination occurs in all Tristichoideae and those Podostemoideae which have less-conspicuous flowers, including all non-American Podostemoideae (Bezuidenhaut 1964; Grubert 1974; Rutishauser and Huber 1991); normally, stamen number is reduced. In some oligostemonous Podostemoideae, self-pollination, including pre-anthesis cleistogamy within the unruptured spathella, may be more frequent than allogamy (e.g. in Griffithella, Hydrobryopsis, Leithylax warmingii, Podostemum ceratophyllum, Polypleurum stylosum; Philbrick 1984; Khosla and Mohan-Ram 1993; Khosla et al. 2000, 2001). Okada and Kato (2002) found low pollen:ovule ratios in autogamous podostemads, while allogamous species have high values. Fruits and Seeds. The period from flowering to capsule maturation is up to 2 or 3 weeks in species of Apinagia, Mourera, Rhyncholacis and Weddellina (Grubert 1974). Philbrick and Novelo (1998) observed in Marathrum rubrum apparently ma-

Podostemaceae

ture capsules 9 days after anthesis; the capsules were brown, with prominent longitudinal ribs and a dark, hardened pedicel lacking outer parenchymatous tissue. In Marathrum and Vanroyenella, the seeds require at least an additional 2 weeks to develop within the capsule (Philbrick and Novelo 1995). The fruits of Polypleurum stylosum appear to mature in the incredibly short period of 4 or 5 days after pollination (Khosla et al. 2000). The fruits of most Podostemaceae are septicidal capsules. Farmeria metzgerioides seems to be the sole exception, in having indehiscent fruits with one or rarely two mature seeds (Willis 1902). Mature capsules are usually about the same size as the ovaries during anthesis; capsules can be 1–3 mm long in Zeylanidium, 3–6 mm long in Marathrum, or up to 13 mm long in Mourera fluviatilis. Capsule symmetry and the number of capsule ribs are used as convenient taxonomic characters in subfamily Podostemoideae. The ribs become more prominent once the capsule is mature and the epidermis and outer parenchymous cortex have been lost (Rutishauser and Pfeifer 2002; Ameka et al. 2003). The sutures are often marked by twin-ribs. In our generic descriptions, the number of ribs per valve ignores the sutures. Using a wider generic concept, genera such as Cladopus, Podostemum sensu lato and Zeylanidium all have species with both smooth and ribbed capsules (Philbrick and Novelo 2004). There are two valves which are either equal (isolobous, Fig. 123D) or unequal (anisolobous, Figs. 108F, 121E). The seeds of most Podostemaceae are nearly the same size as the ovules; they are very small (± 0.1–0.3 mm long) and any dispersed is by wind or water. Ornithochory is also possible; the sticky seed coat (myxospermy) suggests that the seeds could adhere to the feet of birds walking over exposed rocks (Philbrick 1984). In Polypleurum stylosum, there are 1,200,000 seeds per gram and in Griffithella hookeriana 700,000 seeds per gram (Vidyashankari 1988b; Khosla and Mohan Ram 1993). Podostemoideae vary considerably in seed number per capsule: 2,000–2,400 seeds per fruit have been counted in Mourera fluviatilis, 300–700 in Apinagia, Marathrum and Rhyncholacis, less than 300 in Asian taxa such as Cladopus and Polypleurum, ± 30 in Hydrobryum, 4–8 in Farmeria indica and only two in F. metzgerioides (Philbrick and Novelo 1997; Rutishauser 1997; Khosla et al. 2000). Ovule number, seed number and seed size in Central and North American species have been reviewed by Philbrick and Novelo (1997).

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Seeds can remain viable for up to 18 months when stored dry (Vidyashankari and Mohan Ram 1987; Vidyashankari 1988a; Philbrick and Novelo 1998). Seedlings and Life Cycle. Most species are annual but some are perennial as long as they remain submersed. Oserya spp., Podostemum ceratophyllum and some races of Tristicha trifaria are habitually perennial and tend to have fewer ovules than the annual species (Philbrick 1984; Philbrick and Novelo 1997). Germination is correlated with rainy seasons (Willis 1902; Mohan Ram and Sehgal 1992; Philbrick and Novelo 1995). The seeds become sticky when wet, due to expanding mucilage cells of the outer integument (Grubert 1970, 1976; Philbrick and Novelo 1997). Germination takes place at the beginning of the rainy season. The seedling has two cotyledons and a plumule which usually stops growth after some appendages develop (e.g. Indotristicha ramosissima; Schnell and Cusset 1963; Vidyashankari 1988a; Mohan Ram and Sehgal 1997, 2001; Sehgal et al. 2002). However, no plumular activity was seen in Hydrobryum, according to Suzuki et al. (2002). Zeylanidium olivaceum seems to be the only Asian taxon with a persistent seedling axis (Jäger-Zürn 2003b) but, in New World taxa such as Apinagia spp., Mourera fluviatilis and Weddellina squamulosa, the plumule gives rise to vigorous shoots (Grubert 1976; Rutishauser and Grubert 1999). The radicular pole may rarely develop a rudimentary primary root, according to Kita and Kato (2005). In seedlings with short-lived plumules, development continues by lateral endogenous or exogenous outgrowths of the hypocotyledonary region which are usually called secondary roots or adventitious roots (Rauh 1937; Grubert 1970, 1976; Philbrick 1984; Sehgal et al. 2002; Suzuki et al. 2002). Karyology. Podostemaceae are cytologically poorly known. Oropeza et al. (1998, 2002) reviewed the existing literature and estimated that worldwide only 3.3% of the species have been cytologically investigated, none of them from Africa. Chromosome numbers are clearly very variable. The following numbers have been reported: n = 8, 10, 12, 14, 20; 2n = 20, 26, 28, 30, 34, 40. For example, Uniyal and Mohan Ram (1994) counted 2n = 34 in Polypleurum stylosum, 2n = 26 in Zeylanidium (syn. Hydrobryopsis) sessilis, and 2n = 30 in Dalzellia zeylanica (see also Mohan Ram and Sehgal 2001).

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Phytochemistry. Burkhardt et al. (1992, 1994) examined species of Mourera and Rhyncholacis; Romo Contreras et al. (1993) examined Marathrum, Oserya, Podostemum, Tristicha and Vanroyenella, all from the New World. Two xanthone aglycones with the following oxidation patterns were detected: 1,3,5-trihydroxylation in Mourera and 1,3,6,7-tetrahydroxylation in Marathrum, Oserya and Vanroyenella. Xanthones are also known in Weddellina (Weddellinoideae) but are not known from Tristichoideae (Kato et al. 2005). In Podostemum ceratophyllum, •-mangostin and its 6-glucoside was found. Classification. The division of Podostemaceae into three subfamilies proposed by Engler (1928) is followed in this treatment. Tristichoideae and Weddellinoideae are clearly distinguishable from the large subfamily Podostemoideae. Tristichoideae, Weddellinoideae and then the New World Mourera, Apinagia, Marathrum and Oserya within Podostemoideae are successive sister taxa (Les et al. 1997; Kita and Kato 2001; Kato et al. 2003). Basal members of Podostemaceae are (in ascending order) the Tristichoideae, Weddellinoideae and the New World genera Mourera, Apinagia, Marathrum and Oserya within Podostemoideae (Les et al. 1997; Kita and Kato 2001; Kato et al. 2003). All podostemoids studied from continental Africa form a clade which is sister to the Madagascan genera Endocaulos and Thelethylax. The sister of this African-Madagascan lineage is the American genus Podostemum and all Asian podostemoids (Moline et al. 2006). At present, considerable work is being devoted at the family and a reduction in the number of genera and species would be expected – the reverse is the case. As many as four new genera were described within the last years: Cipoia C.T. Philbrick, Novelo & Irgang, Diamantina Novelo, C.T. Philbrick & Irgang, Thawatchaia M. Kato, Koi & Y. Kita, and Vanroyenella Novelo & Philbrick. Using a rather wide genus concept, we have merged several small genera with closely related genera, e.g. Cladopus (incl. Torrenticola), Hydrobryum (incl. Synstylis), Tristicha (incl. Malaccotristicha and Terniopsis), Zeylanidium (incl. Hydrobryopsis). A few monotypic genera, however, are maintained, despite other botanists (Cheek et al. 2000; Philbrick and Novelo 2004) having merged these with larger genera, e.g. Butumia (not included in Saxicolella), Crenias and Devillea (not included in Podostemum). However,

a complete resolution of the phylogeny of the family has not yet been achieved and we present the podostemoid genera in alphabetic sequence. Affinities. The relationships of Podostemaceae within the angiosperms remained unresolved for more than a century and a half, and quite divergent affinities have been hypothesized. Cusset and Cusset (1988) even proposed to place them in the class Podostemopsida coordinate with monocotyledons and dicotyledons. A closer relationship of Podostemaceae to eudicots, especially Saxifragales, and with Crassulaceae in particular was suggested by Mauritzon (1933), Kapil (1970), Les et al. (1997) and Ueda et al. (1997); the highly developed suspensor haustorium, and other embryological characters seemed to support this position. Hydrostachyaceae, also highly modified plants of river rapids in Africa (especially Madagascar), are probably not close to Podostemaceae, as molecular evidence indicates that Hydrostachyaceae belong to Cornales, in the asterids (see Vol. VI of this series). Recent results based on analysis of rbcL, matK and 18S rDNA sequences indicate that Podostemaceae are members of eurosid I Malpighiales. Within Malpighiales, Clusiaceae/Hypericaceae and Bonnetiaceae appear to be most closely related (Soltis et al. 1999; Chase et al. 2000; Savolainen, Fay et al. 2000; Kita and Kato 2001; Gustafsson et al. 2002; Suzuki et al. 2002). From the shared common ancestor hypothesized for Hypericum and the two genera of Podostemaceae (Tristicha, Marathrum) included in the molecular analysis by Savolainen, Fay et al. (2000), the estimated branch length for Tristicha and Marathrum is twice that for Hypericum, which makes it appear as though rbcL is evolving twice as fast in Podostemaceae as in Hypericaceae (Chase et al. 2000). Non-molecular evidence that Podostemaceae are related to Clusiaceae includes the polystemonous and centrifugal androecium in both families (see, e.g. Mourera fluviatilis, Fig. 104G; Rutishauser and Grubert 1999), tenuinucellate ovules, resin cells and/or latex channels (Gustafsson et al. 2002). Distinctive xanthones are shared by some Podostemaceae, Clusiaceae and Bonnetiaceae (APG II 2003; Kato et al. 2005; Stevens 2005). Distribution and Habitats. Podostemaceae are cosmopolitan in tropical regions of the world, extending into warm-temperate eastern North America and East Asia (Engler 1928; Mathew and

Podostemaceae

Satheesh 1997). They grow in flowing water and are therefore confined to hilly regions, being largely absent from the Amazon, Congo and Gangetic plains. Most of the species are restricted to small geographical areas; only one species, Tristicha trifaria, is widespread and occurs in the Old and New World (Kato et al. 2003). Kita and Kato (2004a) found that the American and West African T. trifaria are closely related, despite the great distance between their locations. The biogeographic history of the Asian genera Cladopus and Hydrobryum was explored by Kita and Kato (2004b) using molecular data. Their matK phylogeny revealed that the East Asian temperate species of both genera form monophyletic groups which are derived from tropical/subtropical species. Much has been published on the ecology of Podostemaceae; see especially Gessner and Hammer (1962), Grubert (1970, 1974, 1976, 1991), Léonard (1993) and Noro et al. (1994a, b). Podostemaceae are haptophytes normally fixed to a hard substrate in rapids and waterfalls, usually in sunny places. In most species, flowering takes place when the water level drops. The substrate does not seem to be important as long as it is hard; C.D.K. Cook has seen Polypleurum stylosum growing on wood, concrete and a discarded bicycle in southern India. Most reports, e.g. Pannier (1960), Gessner and Hammer (1962), Quiroz et al. (1997) and OdinetzCollart et al. (2001), state that Podostemaceae grow in oligotrophic and oxygen-rich water. Endemism, Conservation Biology and Population Structure. Most species occupy rather small areas, often being confined to a single set of river-rapids or a single river. About half of all American species are very local endemics (van Royen 1951, 1953, 1954; Tur 1997; Cook 1999). The very high degree of endemism may well be a taxonomic artefact because few species have been sufficiently studied, and the related group of species of one taxonomist may be seen as environmental forms by others (see Novelo and Philbrick 1997). Various localities of endangered New and Old World taxa have already been lost due to industrial pollution, hydroelectric power plants and for other reasons (Grubert 1991; Mohan Ram and Sehgal 2001). A continuous and consistent effort is required to improve methods of ex situ and in situ conservation (Mohan Ram and Sehgal 2001). Ex situ culture and, thus, ex situ conservation of Podostemaceae were impossible until recently, but Mohan Ram and his school started to cultivate Podostemaceae us-

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ing in vitro techniques. Polypleurum stylosum was the first podostemad grown in vitro until it flowered (Sehgal et al. 1993). Various podostemads have been cultivated in vitro since then (Uniyal and Mohan Ram 1996; Mohan Ram and Sehgal 1997, 2001; Imaichi et al. 2004; Kita and Kato 2005). Isozyme variation and population structure was studied by Philbrick and Crow (1992) in the perennial Podostemum ceratophyllum, which is the only northern temperate member of New World Podostemaceae. A population of this species even grows near the sea in a freshwater river under tidal influence, as described by Capers and Les (2001). Plant-Animal Interactions. According to Gessner and Hammer (1962), Mourera is an important food for fish. A fisherman on the Essequibo River in Guyana reported to C.D.K. Cook that some fish species are confined to stands of Podostemaceae. Connelly et al. (1999) describe the riverweed darter (Etheostoma podostemonae), a small freshwater fish of the perch family, as being closely associated with the habitats of Podostemum ceratophyllum in North America. Hutchens et al. (2004) found a strong positive relationship between surface area of Podostemum ceratophyllum and macroinvertebrate abundance and biomass. Léonard and Dessart (1994) report that some species of the Torridincolidae (Myxophaga, Coleoptera) possibly have a symbiotic relationship with Ledermanniella, Leiothylax and Macropodiella in Central Africa. Palaeobotany. According to Collinson et al. (1993), the earliest fossil records are leaves, named Nitophyllites zaisanica, from the Upper Eocene from the Zaisan Basin in Russia. Leaves and flowers have been reported from the Pliocene in Poland and there are records from the Lower Miocene in Germany; Mai (1985) doubts that the material is correctly identified. Economic Importance. According to van Royen (1951), in Panama and Colombia Podostemaceae are used as forage in the dry season – cattle are driven into the river to graze. Cusset (1987) records that Dicraeanthus africanus, Macropodiella heteromorpha, Marathrum foeniculaceum and Thelethylax minutiflora are eaten as salad or vegetable. Leaves of Rhyncholacis sp. are dried and pulverized and used as a pepper-like seasoning (Philbrick and Novelo 1995, citing R. Schultes). Amerindians extract salt from the

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burnt leaves of Mourera fluviatilis and other large species. Salt can be also produced from Ledermanniella warmingiana, as described by Gilg (cited in Warming 1901). Marathrum utile is reported to be refreshing and febricidal (van Royen 1951). In parts of Mexico, species of Marathrum are evidently employed as a liver treatment (Philbrick and Novelo 1995). Rhynchonin A (a chromene newly found in Rhyncholacis penicillata) showed broad insecticidal, acaricidal and nematicidal potency, including strong biological activity against Heliothis zea (Burkhardt et al. 1994). Keys to the Genera In the key and taxonomic treatment, genera are dealt with in three separate geographic groups – American, African (including Madagascan) and Asian/Australian. Only the genera Tristicha and Cladopus (including Torrenticola) occur on more than one continent. Within the geographical groups, genera are presented alphabetically; the present state of knowledge does not permit to arrange them in a phylogenetically meaningful order. The number of ribs per valve ignores the lateral sutures but includes the midrib when it is rib-like. Key to the Genera of America 1. Tepals filamentous, subulate or scale-like, free, 2–20, not enclosing young flowers; young flowers totally enclosed in a spathella (a sack-like cover); ovary 2-locular 3 – Tepals broad and imbricate, oblanceolate to ovate, 3– 6, free or united below, enclosing the young flowers; young flowers may be enveloped by a few leaves but are never enclosed in a spathella; ovary 2- or 3-locular 2 2. Tepals 5 or rarely 4 or 6; stamens 5–25; capsule opening by 2 valves (Northern to central South America) 1. Weddellina – Tepals 3; stamens 1, 2 or rarely 3; capsule opening by 3 valves (America, also in Africa, Madagascar, Malaysia, Australia) 2. Tristicha 3. Spathellas containing 10–20 flowers (Colombia) 15. Macarenia – Spathellas containing a single flower 4 4. Flowers not in 2-sided, raceme-like inflorescences; leaves not rough, without wart-like and prickle-like processes on the upper surface 7 – Flowers in 2-sided, simple or branched, raceme-like inflorescences; leaves with (more rarely, without) warts and/or prickles on the upper surface 5 5. Stamen filaments united to halfway or slightly less, forming a tube below (Brazil) 21. Tulasneantha

– Stamen filaments free or rarely some united at the very base, not forming a tube below, usually persisting in fruit 6 6. Stamen filaments flat, widened and wing-like, elliptic, membranous; stigmas flattened, crested (Brazil) 13. Lonchostephus – Stamen filaments linear, terete, not winged; stigmas linear or spathulate, not crested (widespread in South America) 17. Mourera 7. Capsules strongly asymmetrical when viewed laterally; upper capsule valve smaller and narrower than the lower and almost free from the pedicel, the lower valve saucer-shaped (central Brazil) 6. Castelnavia – Capsules symmetrical or asymmetrical when viewed laterally; upper and lower capsule valves distinctly attached to the pedicel, boat- or cup-shaped 8 8. Roots thread-like, cylindrical or sometimes somewhat flattened 9 – Roots usually distinctly flattened, ribbon-like 14 9. Shoots solitary, borne at irregular intervals along the root (SE Brazil) 10. Devillea – Shoots in ± opposite pairs, borne at almost regular intervals along the root 10 10. Leaves bearing 3–8 digitally arranged segments on expanded and sheathing bases (Minas Gerais, Brazil) 11. Diamantina – Leaves simple or forked, never digitate 11 11. Capsules smooth; stigmas palmately lobed or (in Crenias glazioviana) simple (SE Brazil) 9. Crenias – Capsules ribbed; stigmas simple 12 12. Capsules with 2 subequal or unequal valves, the suture slightly acentric; stamens 2 or rarely 1 or 3 (Central and South America) 18. Oserya – Capsules with 2 equal or subequal valves, the suture centric or nearly so 13 13. Flowering stems sympodially branched, elongate, each module bearing 2 or rarely 1 leaf (widespread in South America) 5. Apinagia – Flowering stems simple and short, each one bearing several leaves (NE South America) 12. Jenmaniella 14. Ovary enclosed within the ruptured spathella during anthesis, only stigmas and stamens projecting; stamen 1 (Minas Gerais, Brazil) 8. Cipoia – Ovary emerging above the ruptured spathella during anthesis; stamens 2 or more, or rarely 1 in some flowers 15 15. Stamens 2 or more, free 19 – Stamens normally 2, united below or borne on an andropodium, occasional flowers with 1 stamen 16 16. Stigmas persisting in fruit, horn-like; midrib of each capsule valve running into the stigma (SE Brazil) 7. Ceratolacis – Stigmas withering after anthesis, simple or palmately branched, never horn-like; midrib of each capsule valve not running into the stigma 17 17. Capsules smooth, not ribbed, globose; stigmas palmately lobed or (in Crenias glazioviana) simple, with hair-like papillae (SE Brazil) 9. Crenias – Capsule valves with 3 ribs, ovoid to spindle-shaped; stigmas simple, with inconspicuous papillae 18 18. Capsules ellipsoidal, opening by 2 equal valves; pollen shed in monads (mainly NE South America) 12. Jenmaniella

Podostemaceae – Capsules ovoid, opening by 2 unequal valves, the larger usually persistent; pollen shed in dyads (tropical to temperate America) 19. Podostemum 19. Stigmas flattened, lobed or serrated at the apex, somewhat resembling a cock’s comb (C Brazil) 14. Lophogyne – Stigmas terete or flattened, when flattened, then entire or toothed but not resembling a cock’s comb 20 20. Capsules flattened; midrib of each capsule valve winged, the remaining ribs unwinged (N South America) 20. Rhyncholacis – Capsules terete; midrib of the capsule valves not winged or, if winged, then other ribs also winged 21 21. Pinnae and pinnules of the leaves with scale-like stipels; capsule valves with 5 ribs (S Brazil) 23. Wettsteiniola – Pinnae and pinnules naked, without free stipels; capsule valves with 1–7 ribs 22 22. Capsule valves with 5 or 7 ribs (Central and South America) 5. Apinagia – Capsule valves with 3 or less ribs or furrows 23 23. Stems elongate, frequently branched (Central and South America) 5. Apinagia – Stems very short, never branched 24 24. Capsule valves without ribs or with 3 grooves or stripes 5. Apinagia – Capsule valves with 3 ribs 25 25. Capsule ribs winged (West Indies, Central and NW South America) 16. Marathrum – Capsule ribs not winged 26 26. Stigmas linear, not toothed (Central and South America) 5. Apinagia – Stigmas boat- or spoon-shaped, often toothed 27 27. Leaf blades repeatedly pinnate or forked; stamens 2–40; stamen filaments deciduous after anthesis (West Indies, Central and NW South America) 16. Marathrum – Leaf blades plumose with the smallest segments forked and hair-like; stamens 2 or 3; stamen filaments persistent and indurate, remaining attached to the ribs of the capsule after anthesis (W Mexico) 22. Vanroyenella

Key to the Genera of Africa and Madagascar 1. Tepals 2 or occasionally 3 or 4, not imbricate, restricted to one side of the flower, linear to subulate; young flowers totally enclosed in a spathella (a sack-like cover); capsules opening by 2 valves 2 – Tepals 3, imbricate, surrounding the young flowers, ovate to oblong-obovate; young flowers not enclosed in a spathella; capsules opening by 3 valves (widespread in Africa and Madagascar) 2. Tristicha 2. Stigma 1, semi-globose; stamens 3 or rarely 4, united only at the base (Angola) 24. Angolaea – Stigmas 2, linear, horn-like, or flattened and lobed; stamens 1, 2 or rarely 3, when 2 or 3, then borne on an elongate andropodium 3 3. Flowers erect or rarely slightly inclined within the unruptured spathellas 13 – Flowers inverted or strongly inclined within the unruptured spathellas 4 4. Tepals 2, 1 each side of the andropodium base, without an appendage between the stamens 6

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– Tepals 3, 1 each side of the andropodium base and 1 borne terminally on the andropodium between the stamens 5 5. Capsules broadly ellipsoidal; capsule valves with 5 or 7 narrow ribs, those closest to the sutures not reaching the base and the apex (tropical W Africa) 36. Stonesia – Capsules obovoid; capsule valves with 3 wide ribs, each extending from base to apex (Madagascar) 37. Thelethylax 6. Capsules smooth, globose or subglobose (Cameroon, D.R. Congo, Zambia) 30. Leiothylax – Capsules with longitudinal ribs or wings, laterally flattened or cylindrical to ellipsoidal or globose 7 7. Ovaries and capsules terete, not flattened; capsules without winged nerves 9 – Ovaries and capsules flattened; capsules with or without winged nerves 8 8. Capsules strongly flattened, with winged middle nerves; wings longer than the capsule and forming apical horns; stamens 2 (Cameroon) 38. Winklerella – Capsules slightly to strongly flattened, without wings or apical horns; stamens 1, 2 or 3 (tropical W Africa) 32. Macropodiella 9. Capsules ovoid-ellipsoidal or partly cylindrical 11 – Capsules globose or subglobose 10 10. Pedicels less than 5 mm long; capsules sessile or borne on minute gynophores; stamen 1 or perhaps sometimes 2; pollen shed in dyads (Madagascar, tropical and South Africa) 35. Sphaerothylax – Pedicels up to 15 mm long; capsules borne on up to 8 mm long gynophores; stamens 2 or rarely 3; pollen shed in monads (Cameroon) 39. Zehnderia 11. Flowers or flower clusters arranged in one row along the shoot; andropodium usually less than 1 mm long; stigmas conical, erect, rigid; capsules cylindrical to oblong (W and C Africa) 26. Dicraeanthus – Flowers or flower clusters arranged around the shoot, rarely in a row; andropodium usually much exceeding 1 mm long; stigmas linear, spreading or reflexed, flexible; capsules obovoid to ovoid or fusiform 12 12. Capsule valves with 3 narrow or occasionally crest-like ribs; capsules ovoid to ellipsoidal or fusiform (species rich and widespread in tropical Africa) 29. Ledermanniella – Capsule valves with 3 wide and flattened ribs; capsules obovoid (Madagascar) 37. Thelethylax 13. Capsule valves equal, usually both persistent; capsule sutures centric 15 – Capsule valves somewhat unequal, one valve caducous, the other persistent on pedicel or gynophore; capsule sutures acentric and oblique 14 14. Stamen 1; capsules globose or subglobose; capsule valves with 3 wide ribs, each extending from base to apex (Cameroon) 27. Djinga – Stamens 2, borne on an andropodium; capsules asymmetrically ovoid and somewhat laterally flattened; capsule valves with 7 narrow ribs, those closest to the sutures not reaching the base and the apex (Madagascar) 28. Endocaulos 15. Capsules globose or subglobose, smooth and shiny (W Africa from Namibia to Niger) 31. Letestuella – Capsules ovoid to ellipsoidal or fusiform, with longitudinal ribs 16

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16. Flowering stems covered with at least 8 but usually many more, overlapping, scale-like leaves; stamens 2, borne on an andropodium (Madagascar) 33. Paleodicraeia – Flowering stems with elongate, simple or forked leaves or, if leaves scale-like, then rarely more than 4; stamen 117 17. Leaves below the flowers scale-like, shorter than the flowers; capsules ovoid, laterally flattened; stigmas unequal, flattened, elliptic to ovate in outline (Nigeria) 25. Butumia – Leaves below the flowers linear or divided into linear segments, longer than the flowers; capsules elliptic to fusiform, terete; stigmas equal, linear (tropical W Africa) 34. Saxicolella

Key to the Genera of Asia and Australia 1. Tepals 2 or occasionally 3 or 4, restricted to one side of the flower, linear to subulate, not imbricate; young flowers totally enclosed in a spathella (a sack-like cover); capsules opening by 2 valves or indehiscent; stamens 1 or 2, when 2, then borne on an andropodium; pollen shed as dyads 4 – Tepals 3, surrounding the young flowers, ovate to oblong-obovate, imbricate; young flowers not enclosed in a spathella; capsules opening by 3 valves; stamens 1–3, free; pollen shed as monads 2 2. Stems, at least partly elongate, bearing ramuli (mosslike branchlets with scale-like or linear appendages); roots elongate, thread-like or ribbon-like 3 – Stems, flattened, closely attached to substrate, crustose (foliose), without ramuli, often bearing photosynthetic scales above; roots absent or flattened and somewhat irregular in shape (S and SE Asia) 3. Dalzellia 3. Flowers borne on slender pedicels without cup-like structures at the base; stems variable, often creeping, when free, then usually considerably less than 10 cm long; ramuli with scales arranged in 3 rows (China, Malaysia, Australia) 2. Tristicha – Flowers arising from cup-like structures of united scales and ramuli; stems usually free, branched, up to 60 cm long; scales or linear appendages of ramuli arranged in many rows or irregularly scattered (S India) 4. Indotristicha 4. Leaves or scales on flowering stems all entire 8 – Leaves or scales on flowering stems with at least some divided into 2–8 simple lobes or lateral teeth 5 5. Leaves or scales on flowering stems arranged in 2 rows or appearing to be irregular 7 – Leaves or scales of flowering stems arranged in 4 or 6 neat rows 6 6. Capsule valves unequal, the larger persisting; 2 of the rows of leaves or scales on flowering stems with filamentous tips (SW India) 48. Willisia – Capsule valves equal; 2 of the rows of leaves or scales on flowering stems 2-lobed (N Thailand) 44. Hanseniella 7. Capsule valves equal; spathellas thick, with 2 or 3 ridges; stamens mostly 2, borne on an andropodium;

–

8. – 9. – 10.

–

11.

–

12. – 13

–

leaves or scales on flowering stems mostly 3-lobed (N Thailand) 47. Thawatchaia Capsule valves unequal; spathellas thin, without ridges; stamen mostly 1, simple; leaves or scales on flowering stems 2-to 8-lobed, rarely consistently 3-lobed (E and SE Asia, New Guinea, NE Australia) 40. Cladopus Capsule valves unequal, the smaller one caducous 11 Capsule valves equal, usually both persisting or sometimes both caducous 9 Capsule valves each with 9 fine ribs (excluding the lateral sutures); capsules laterally flattened (Vietnam, Laos) 41. Diplobryum Capsule valves each with 2–6 ribs (excluding the lateral sutures); capsules ± terete 10 Roots crustose, closely attached to substrate; flowers usually subsessile, scarcely raised above the spathella at anthesis (E Himalaya, S China, E and SE Asia) 45. Hydrobryum Roots elongate (ribbon- or thread-like), with the distal part usually free and floating; flowers pedicellate, held well above the spathella at anthesis (Sri Lanka, India, Thailand) 46. Polypleurum Flowers sessile or nearly so, usually remaining within the opened spathella or barely emerging above it; pedicels not more than 1 mm long; shoots confined to the margins of elongate roots; stamen 1 (consistently so from flower to flower); stigmas unequal; capsules indehiscent or dehiscent; seeds 1–8(–18) (S India, Sri Lanka) 42. Farmeria Flowers stalked or subsessile, emerging above the opened spathella; pedicels usually more than 1 mm long; flowering shoots developing from the upper surface of crustose (foliose) roots or in the sinuses of lobed, ribbon- or thread-like roots; stamens 2, borne on an andropodium or rarely 1 (usually some flowers with 2); stigmas equal; capsules dehiscent; seeds 12 to numerous 12 Capsules with prominent, longitudinal ribs (Sri Lanka, S, W and NE India, Myanmar) 49. Zeylanidium Capsules smooth or obscurely ribbed 13 Spathellas erect, funnel-shaped, splitting into several rather irregular apical teeth; roots irregular in form, varying from star- to cup-shaped or ribbon-like but not regularly pinnate (S India) 43. Griffithella Spathellas prostrate, boat-shaped, splitting longitudinally; roots ± regularly, pinnately branched (S India) 49. Zeylanidium

Genera of Podostemaceae I. Subfam. Weddellinoideae (Warming) Engler (1928). Young flowers not enclosed in spathella or cupule; tepals (4)5(6), imbricate; stamens 5–25, free; pollen tricolporate, shed in monads; ovary 2-locular; capsule opening by 2 equal valves; valves with 1 rib-like midrib and 2 lateral ribs. Only one genus, Weddellina Tulasne, northern to central South America.

Podostemaceae

1. Weddellina Tulasne

Figs. 104F, M, 105A–D

Weddellina Tulasne, Ann. Sci. Nat., Bot. III, 11:90, 113 (1849).

Roots thread-like, laterally flattened, up to 2 mm wide, creeping, branched, with numerous disk-like holdfasts; stems arising laterally from the root; vegetative stems erect, up to 80 cm long, irregularly pinnately branched; branches thickly covered with entire or divided scale-like leaves and bunches of photosynthetic filaments; flowering stems unlike vegetative ones, unbranched, 2–12 cm long, bearing scale-like leaves and solitary terminal flowers. Flowers enveloped in scale-like leaves when young; scale-like leaves intergrading with tepals and usually spirally arranged; tepals oblanceolate, 3–6 mm long, free or slightly united at base, pink to lilac or white; stamen filaments terete. Capsules ellipsoidal to subglobose, 2.5–4 mm long; style linear, 0.5–1 mm long; stigma capitate; seeds ± 160. One species, W. squamulosa Tulasne, with two ‘formae’, northern to central South America.

simple or branched, up to 10 cm long, bearing scales and ramuli (photosynthetic branchlets); ramuli moss-like, 2–4 cm long; scale-like appendages of ramuli entire or divided, arranged in 3 rows, usually 2 rows spreading and the third row smaller and appressed. Flowers solitary or sometimes in clusters, pedicellate; tepals 3, lanceolate to narrowly ovate, free or united at the base. Capsules ellipsoidal to ovoid; style short; stigmas linear, simple or rarely forked. Seeds up to ± 70. Probably only one, very polymorphic species, T. trifaria (Bory ex Willdenow) Sprengel, or up to 6 species, tropical America, Africa, Madagascar, Mascarene Islands, Malaysia, East China and north-eastern Australia. Terniopsis sessilis Chao, Tristicha australis C. Cusset & G. Cusset [= Malaccotristicha australis (C. Cusset & G. Cusset) M. Kato] and Malaccotristicha malayana (Dransfield & Whitmore) C. Cusset & G. Cusset seem to be no more than prostrate states of Tristicha trifaria. 3. Dalzellia R. Wight

II. Subfam. Tristichoideae (J.C. Willis) Engler (1928). Young flowers either without spathella or, in Dalzellia and Indotristicha, enclosed in cupule (collar-like, vascularised cup); spathella 0; tepals 3, imbricate; stamens 1–3, free; pollen pantoporate with up to 16 pores, shed in monads; ovary 3-locular; stigmas 3; capsule opening by 3 equal valves; valves with 1 rib-like midrib and 2 lateral ribs. Three genera (using a wide genus concept), tropical America, tropical and southern Africa, Madagascar, Mascarene Islands, South and Southeast Asia and northern Australia.

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Fig. 106D–F

Dalzellia R. Wight, Ic.. Pl. Ind. Orient. 5, 2:34, t. 1919, 1920, 1919 (1852). Lawia Griffith ex Tulasne (1849), nom. illegit. Mnianthus Walpers (1852).

2. Tristicha Du Petit-Thouars Figs. 104E, J, 106A–C Tristicha Du Petit-Thouars, Gen. Nova Madag. 3 (1806). Dufourea Bory (1810), nom. illegit. Philocrena Bongard (1837). Potamobryum Liebmann (1849). Tristichopsis A. Chevalier (1938), nom. illegit. Terniopsis H.C. Chao (dated 1948, publ. 1949). Heterotristicha Tobler (1953). Dalzellia non R. Wight, sensu Cusset & Cusset (1988). Malaccotristicha C. Cusset & G. Cusset (1988).

Roots creeping, ± cylindrical or laterally flattened and ribbon-like, 0.5–1 mm wide, branched, attached to rock by disk-like holdfasts; stems polymorphic, creeping or floating; floating stems

Fig. 106. Podostemaceae-Tristichoideae. A–C Tristicha trifaria. A Creeping root with ramuli (5 mm). B Flower (0.5 mm). C Fruiting shoot with three ramuli (2 mm). D–F Dalzellia zeylanica. D Fragment of crustose plant with exogenous scales and an endogenously formed rosette (1 cm). E Flower (1 mm). F Stalked capsule (1 mm). (Orig. Cook)

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Terniola Tulasne (1852). Tulasnea R. Wight (1852), nom. illegit.

Roots 0 or, in D. gracilis Mathew, Jäger-Zürn & Nileena, flattened and irregular in outline; plant body closely attached to rock, flattened, crustose, often ± star-shaped, up to 35 cm in diameter, the lobes usually rather irregular. Leaves numerous, simple, scale-like or linear, occurring on upper surface and along edges of plant body or in closely packed rosettes arising on older parts; ramuli (photosynthetic branchlets) 0; rosettes forming cupules (cup-like structures) of many scales which surround the individual flowers, cupules apparently lacking in D. gracilis. Flowers solitary, terminal, pedicellate; pedicel 2–3 mm long at anthesis, elongating in fruit to 10–20 mm long; tepals 3, narrowly ovate to ovate, united below; stamens 3(2). Capsules ellipsoidal to ovoid, remaining within tepals until dehiscence; stigmas 3, ovate to linear. Seeds 200– 300. Four or perhaps more species, in South and Southeast Asia. 4. Indotristicha P. Royen

lacking, not imbricate, linear, spathulate or subulate; stamens 1–40, often free; many genera with Yshaped androecium, consisting of 2 stamens borne on an andropodium (a common stalk); pollen tricolpate or sometimes tetracolpate or pentacolpate, shed in monads or dyads (Diamantina in tetrads); ovary 2-locular or rarely, due to absence of a septum, 1-locular; capsule opening by 2 equal or unequal valves, or rarely indehiscent. Forty-five genera, tropical America to temperate eastern North America, tropical and subtropical Africa, Madagascar, tropical South and Southeast Asia to temperate East Asia and tropical Australia.

Fig. 107A–H

Indotristicha P. Royen, Acta Bot. Neerl. 8:475 (1959).

Roots thread-like, much branched, creeping, with finger- or disk-like holdfasts arising from same buds as shoots; vegetative stems totally submerged, becoming discarded as the water recedes, arising from the root, branched, up to 60 cm long, bearing photosynthetic scales and ramuli (photosynthetic branchlets); ramuli up to 4 cm long, with scale-like to filamentous appendages arranged spirally or irregularly but never in 3 rows; flowering stems short, each densely clothed in ramuli and scales; uppermost scales and ramuli united at their bases and forming a cupule (cup-like structure) of 5–7 scales and 1–3 ramuli at base of pedicel. Flowers solitary, terminal on short-shoots, pedicellate; tepals elliptic to ovate, united below; stamens 3; stigmas linear. Seeds ± 100 in I. ramosissima. Two species, I. ramosissima (P. Wight) P. Royen and the poorly known I. tirunelveliana Sharma, Karthikeyan & Shetty, both from southern India. Molecular data (Kato et al. 2003) indicate that Indotristicha ramossissima and Dalzellia zeylandica (Gardner) Wight are closely related. III. Subfam. Podostemoideae (Warming) Engler (1928). Young flowers enclosed in spathella (a membranous, nonvascularised cover); tepals 2–20, rarely

Fig. 107. Podostemaceae-Tristichoideae. A–D Indotristicha ramosissima. A Vegetative shoot with some branches and ramuli removed (2 cm). B Fertile branch (2 mm). C Capsule (1 mm). D Fragment of vegetative shoot with one ramulus (2 cm). E–H Indotristicha tirunelveliana. E Tip of a flowering shoot with two ramuli (1 mm). F Ramulus with scales (1 mm). G Capsule viewed from the side with three perianth segments attached (1 mm). H Capsule viewed from above (1 mm). (Orig. Cook)

Podostemaceae

321

Podostemoid Genera of America 5. Apinagia Tulasne emend. P. Royen Fig. 108A–C Apinagia Tulasne, Ann. Sci. Nat., Bot. III, 11:97 (1849); van Royen, Med. Bot. Mus. Herb. Rijksuniv. Utrecht 107:25–69, 128–131 (1951), rev. Ligea Poiteau ex Tulasne (1849). Oenone Tulasne (1849). Monostylis Tulasne (1853). Neolacis Weddell (1873).

Roots ribbon-like to ± cylindrical and thread-like, branched; holdfasts, in most species, develop from basal portions of root-borne stems; stems arising along root margins, usually in opposite or subopposite pairs, either very short, disk-like and appearing stemless or elongate, when elongate, then simple or branched, when flowering, then each module with rarely 1 or mostly 2 leaves with a flower between them. Leaves in species with disk-like stems united at their bases and confluent with short stems which serve as holdfasts, in species with elongate stems, free; petioles present or 0; sheaths simple or double; leaf blades very variable in shape, lanceolate, lobed to pinnatisect with the tips and, rarely also the lobes, highly divided into filamentous segments, flat portions of blades often with tufts of filaments on upper surface; ultimate filamentous segments sometimes inrolled when young. Spathellas clubshaped to tubular. Flowers solitary, in cyme-like inflorescences or as fascicles in cavities of disklike stems; pedicels (0.5–)1–7(–12) cm long; tepals 2–16, free or united, whorled or confined to one side of flower; stamens 1–30, whorled or confined to one side of flower; anthers dehiscing introrsely or, in 2 species, extrorsely; pollen in monads. Capsules ovoid; each valve with 1–7 ribs, the ribs sometimes unequal in length, sometimes represented by grooves or stripes; stigmas cylindrical to linear. Seeds 20 to ± 600. About 50 species, probably much less when critically examined, northern and central South America. 6. Castelnavia Tulasne & Weddell

Fig. 108D–F

Castelnavia Tulasne & Weddell, Ann. Sci. Nat., Bot. III, 11:108 (1849).

Roots absent in C. princeps Tulasne & Weddell and perhaps also in other species; stems flattened, forked or lobed, firmly attached to rock. Leaves, unknown for some species, filiform and simple or forked, or lanceolate to fan-shaped and palmately lobed, the lobes ultimately divided into branched

Fig. 108. Podostemaceae-Podostemoideae. A–C Apinagia. A A. surumuensis. Vegetative shoot (2 cm). B A. batrachifolia. Flower (2 mm). C A. pygmaea. Flower (1 mm). D–F Castelnavia princeps. D Creeping crustose stem (1 cm). E Flower viewed from below (1 mm). F Capsule viewed from the side (1 mm). G–I Ceratolacis erythrolichen. G Creeping root with leafy shoots (2 cm). H Capsule (1 mm). I Flower (1 mm). (Orig. Cook)

filaments. Spathellas ovoid, becoming ± tubular when open with several teeth at apex, ovary usually remaining within spathella. Flowers numerous, borne in cavities on upper side of flattened stem, distinctly zygomorphic, shortly pedicellate; pedicel inflated above and asymmetrical, not elongating in fruit; tepals 2 or 3 (rarely none), alternating with and sometimes united to stamens; stamens 1–3, free or united at the base; filaments membranous, cohering with base of ovary; anthers dehiscing introrsely; pollen in monads. Capsules often at right angles to pedicel; valves very unequal, the smaller almost free from pedicel, caducous, either smooth or with 3 or 5 ribs, with or without

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papillae, the larger valve saucer-like, persistent, with 5, 7 or 9 ribs; stigmas linear, usually unequal in length, often longer than ovary at anthesis. Seeds relatively few. Nine species, central Brazil, most confined to the Araguaya and Tocantins. 7. Ceratolacis (Tulasne) Weddell

Fig. 108G–I

Ceratolacis (Tulasne) Weddell in A. de Candolle, Prodromus 17:66 (1873); van Royen, Acta Bot. Neerl. 3:224–228 (1954), rev.; Philbrick, Novelo & Irgang, Novon 14:108–113 (2004), rev.

Roots thread-like, cylindrical to semicylindrical, branched, rarely up to 5 mm wide, red or dark green; stems short and obscured by leaf bases, borne along lateral margins of roots, usually in opposite or subopposite pairs. Leaves 2–30 or more mm long, either entire and linear or a few times forked with linear segments, with 1 stipule on the dorsal side of the shoot, attached to the associate leaf. Spathellas club-shaped. Flowers up to 6 per shoot; pedicel in fruit either short or up to ±8 mm long, peduncle as additional stalk below spathella up to 8 mm long in C. pedunculatum; tepals 2 or 3, one each side of andropodium and one (when present) between the two filaments; stamens 2, borne on an andropodium; anthers dehiscing introrsely; pollen in dyads. Capsules spindle-shaped; valves equal, each with midrib running into stigmas and 2 faint lateral ribs; stigmas equal, persistent, horn-like, diverging. Seeds unknown. Two species, C. erythrolichen (Tulasne & Weddell) Weddell from Rio Tocantins, Brazil and C. pedunculatum C.T. Philbrick, Novelo & Irgang, from Minas Gerais, Brazil. 8. Cipoia C.T. Philbrick, Novelo & Irgang Fig. 109A–E Cipoia C.T. Philbrick, Novelo & Irgang, Syst. Bot. 29:113 (2004).

Roots thread-like and usually laterally flattened, branching; stems arising from lateral margins of root, usually in opposite or subopposite pairs, unbranched, (0.1–)2(–3.5) mm long, with hardened leaf remains below and a tuft of leaves at the tip. Leaves filamentous, (2)3 times forked or rarely simple, (3.8–)10(–20.4) mm long, ultimate segments linear to spathulate, stipule as boat-shaped extension of the leaf base. Spathellas club-shaped, (0.9–)1.7(–2.7) mm long, splitting irregularly from top. Flowers 1(–3) per shoot, remaining within spathella during anthesis; borne

Fig. 109. Podostemaceae-Podostemoideae. A–E Cipoia inserta. A Fragment of root bearing two subopposite shoots, each with an unopened spathella (5 mm). B Flower at anthesis, emerging from the spathella (2 mm). C Capsule showing suture and three ribs (5 mm). D Pre-anthesis flower with spathella removed (1 mm). E Two leaf bases with stipules (1 mm). F–K Diamantina lombardii. F Fragment of root bearing two subopposite shoots (5 mm). G Digitate leaf from immediately below a flower bud (1 mm). H Leaf with one elongate segment (4 mm). I Flower at anthesis (3 mm). J Unopened spathella (2 mm). K Detail showing tepals, stamens and gynophore. (Orig. Cook)

on gynophore which elongates during anthesis and exceeds the pedicel; pedicels minute, shorter than spathella; tepals one each side of the stamen filament; stamen 1; filaments elongating during anthesis and projecting from ruptured spathella; anthers dehiscing introrsely; pollen in dyads. Capsules borne within spathella, ellipsoidal, each

Podostemaceae

3-ribbed, 2-locular, valves equal, the sutures thickened; stigmas equal, simple. Seeds unknown. One species, C. inserta C.T. Philbrick, Novelo & Irgang, Minas Gerais, Brazil. 9. Crenias A. Sprengel

Fig. 110A–C

Crenias A. Sprengel in K.P.J. Sprengel, Syst. Veg. 4, 2, Curae postoriores: 246 (1827); van Royen, Acta Bot. Neerl. 3:224– 228 (1954), rev. (under Mniopsis); Philbrick & Novelo, Syst. Bot. Monogr. 70:1–106 (2004), rev. (under Podostemum). Mniopsis Mart. (1823 or 1824), nom. illegit.

323

± 0.5 mm long, one each side of solitary stamen and one on back of it; anthers dehiscing introrsely; pollen in monads. Capsules ellipsoidal to globose, up to 1.2 mm long, smooth; valves unequal, the larger persisting, suture sometimes acentric; stigmas very short. Seeds unknown. One species, D. flagelliformis Tulasne & Weddell, Goiás, Brazil. Philbrick and Novelo (2004) sunk this species into Podostemum.

Roots thread-like and usually laterally flattened, branching; stems arising from lateral margins of root, usually in opposite or subopposite pairs, simple or branched, usually with leaf remains below and a tuft of leaves at the tip. Leaves entire or a few times forked, with 1 stipule on front side of dorsiventral shoot, attached to or detached from associated leaf, the 2 dorsal rows of stipules accompanying the 2 lateral leaf rows. Spathellas bellor club-shaped, up to 3 mm long, splitting irregularly from top. Flowers few to numerous; pedicels hardly exceeding spathella; tepals 2 or 3, one each side of andropodium and one, when present, between or below filaments; stamens 2, borne on andropodium; anthers dehiscing introrsely; pollen in dyads. Capsules globose to ellipsoidal, smooth, 2locular, valves unequal, the larger persistent, the sutures oblique; stigmas equal, covered with hair-like papillae, usually palmately branched. One species (Crenias glazioviana) with simple stigmas. About five species, south-eastern Brazil. Phylogenetic analyses (Philbrick and Novelo 2004) place this genus within Podostemum. 10. Devillea Tulasne & Weddell

Fig. 110G, H

Devillea Tulasne & Weddell, Ann. Sci. Nat., Bot. III, 11: 107 (1849); van Royen, Acta Bot. Neerl. 3:223 (1954), rev.; Philbrick & Novelo, Syst. Bot. Monogr. 70:1–106 (2004), rev. (under Podostemum).

Roots thread-like, filamentous, branched; stems simple or few times branched, ±1 cm long, arranged irregularly but never in opposite or subopposite pairs. Leaves simple or repeatedly forked with filamentous segments, up to 2.5 cm long; leaf base sheathing and usually with symmetrical boat-shaped stipule. Spathellas bell-shaped, up to 3 mm long, when immature, then enveloped in the sheaths of the apical leaves. Flowers 1(2) per shoot; pedicels 0.5–1 mm long, elongating up to 6 mm in fruit; tepals 3, lanceolate to triangular,

Fig. 110. Podostemaceae-Podostemoideae. A–C Crenias weddelliana. A Fragment of creeping root with two subopposite shoots (1 cm). B Stigmas (0.5 mm). C Flower (1 mm). D–F Lonchostephus elegans. D Flowering shoot (1 cm). E Flower (2 mm). F Stigmas (1 mm). G, H Devillea flagelliformis. G Fragment of creeping root with leafy shoots (5 mm). H Flower (1 mm). I, J Jenmaniella tridactylifolia. I Fragment of creeping root with subopposite leafy shoots (5 mm). J Flower (0.5 mm). (Orig. Cook)

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11. Diamantina Novelo, Philbrick & Irgang Fig. 109F–K Diamantina Novelo, Philbrick & Irgang, Syst. Bot. 29:109 (2004); Rutishauser et al., Flora 200:245–255 (2005).

Roots thread-like or slightly flattened, branching; stems arising from lateral margins of root, usually in opposite or subopposite pairs with disk-like holdfasts, branched, erect, (3.5–)19.5(–40) mm long, with hardened leaf remains below and leaves above, their bases becoming broadened and disk-like when older. Leaves crowded, clothing the stem; first leaves thread-like, entire or with 2 or 3 segments; later leaves dimorphic, with expanded sheathing base bearing (2)3–7(8) digitally arranged segments lacking vascular tissue, segments variable in size and form; ‘short leaves’ with all segments alike, 0.5–1.5 mm long, rigid, tooth-like, borne towards base of stem or branch; ‘long leaves’ with 1 or 2 median segments longer than the lateral tooth-like laterals, median segments linear and flexible, up to 10 or more mm long, deciduous, borne towards tip of stem or branch. Spathellas dimorphic; that subtending the subterminal flower scale-like; that of terminal flower tubular, (1.5–)2.2(–2.9) mm long, splitting irregularly from top. Flowers 1 or 2 at tip of stem or branch, developing terminally or subterminally, borne on gynophore which elongates during anthesis to (0.5–)1.8(–2.5) mm long; pedicels (2.5–) 4.6(–7) mm long after anthesis; tepals (2)3(4), scale-like, alternating with stamens; stamens (1)2(3), free; filaments elongating during anthesis but never reaching length of ovary; anthers often rudimentary and sterile; if present, then dehiscing introrsely; pollen in tetrads. Capsules spherical or nearly so, with an apical cleft, opening by 2 equal valves, with thickened sutures; valves 3- or rarely 4- or 5-ribbed; stigmas 2 or rarely 3, equal, simple, horn-like. Seeds unknown. One species, D. lombardii Novelo, Philbrick & Irgang, Minas Gerais, Brazil. 12. Jenmaniella Engler

Fig. 110I, J

Jenmaniella Engler, Bot. Jahrb. Syst. 61 Beibl. 138:7 (1927); van Royen, Med. Bot. Mus. Herb. Rijksuniv. Utrecht 107:119–127, 137 (1951), rev.

Roots thread-like or flattened, branched; stems closely adhering to rock, prostrate, flattened, short, represented by a holdfast, usually in opposite or subopposite pairs, at more or less regular intervals along the root. Leaf bases often united below and

forming a collar around each flower; leaf blades variable, usually a few times forked or pinnate with forked segments; ultimate segments linear, filiform to flattened, inrolled when young; sheaths simple or double, stipule-like on leaves subtending flowers. Spathellas club-shaped. Flowers solitary at end of root-borne stems; pedicels erect, up to 2.5 cm long; tepals 2–7, usually in an incomplete whorl, not all of them closely associated with base of stamens; stamens 1–7, free or sometimes 2 stamens united below, the number, shape and size of stamens often variable from flower to flower on the same plant; anthers dorsifixed, dehiscing introrsely in 4 species, extrorsely in 2 species; pollen in monads. Capsules borne on an up to 3-mm-long gynophore, ellipsoidal; valves equal, each with 3 or 5 ribs; stigmas simple, equal. Seven species, north-eastern South America, probably also Bolivia. 13. Lonchostephus Tulasne

Fig. 110D–F

Lonchostephus Tulasne, Arch. Mus. Hist. Nat. 6:198 (1852).

Roots insufficiently documented; holdfasts ±1 cm long, 0.2–0.5 cm wide; stems very short. Leaves in basal rosettes, very irregular in shape and size, 1–8 cm long, usually somewhat flabellate, blades smooth on both surfaces, repeatedly forked, ultimate segments capillary, narrowed below into short, flattened petiole. Spathellas 4–10 mm long, splitting radially. Flowers 3–6, alternating with bracts in a slightly flattened, 2-sided, simple, raceme-like inflorescence, borne on an up to 8-cm-long naked peduncle; pedicels 0.5–2.5 cm long; bracts ±5 mm long, borne between 2 flowers, with double sheaths, double boat-shaped; tepals linear to lanceolate, ±0.5 cm long, free, reflexed; stamens 5–8, in one whorl; filaments free, flat, widened and wing-like, ellipsoidal, 3–5 mm long, membranous, persisting in fruit; anthers introrse. Capsules ovoid, 3–6 mm long; valves equal, each with 3 ribs; stigmas flattened, crested, persisting in fruit. One species, L. elegans Tulasne, upper Amazon, Brazil. This genus is close to Mourera and Tulasneantha. 14. Lophogyne Tulasne

Fig. 111A, B

Lophogyne Tulasne, Ann. Sci. Nat., Bot. III, 11:90, 99 (1849).

Roots closely attached to rock or partly floating, ribbon-like, up to 5 cm long; stems crustose, developing along edges of root, often hidden in leaf bases. Leaves with swollen bases which coalesce

Podostemaceae

with stem; leaf blades finely dissected or repeatedly forked with capillary ultimate segments. Spathellas club-shaped or apically 2-lipped, up to 7 mm long, embedded in leaf bases when young. Flowers solitary, arising in clefts in the thallous stems; pedicels up to 2 cm long; tepals 2–5, up to 2.5 mm long, in one complete or incomplete whorl, lanceolate to linear, acute; stamens 2–4, free; anthers sometimes spirally wound when dry; anthers dehiscing introrsely; pollen in monads. Capsules ellipsoidal to ovoid, up to 4.5 mm long, inserted subobliquely on pedicel; valves equal, each with 3 ribs; stigmas ±1 mm long, flattened with a serrate or lobed apex, resembling a cock’s comb, persisting in fruit. Two species, L. arculifera Tulasne & Weddell and L. helicandra Tulasne, eastern central Brazil. The two species often grow in the same cataract but are more or less ecologically distinct. 15. Macarenia P. Royen

325

stems; sheaths simple or double, sometimes elongated into stipules; petioles long, short or absent, terete or flattened; blades 1 or more times pinnate or entire in M. utile Tulasne. Spathellas club-like or tubular. Flowers solitary or in fascicles of up to 5, arising from sheath pockets on stem; pedicels (0.5–) 1–9 cm long; tepals scale-like to filiform, 2–25, as many as or 1 more than stamens, in 1 complete or incomplete whorl, alternating with and more or less fused to base of stamen filaments; stamens 3–40 or more, in 1 or 2 whorls or confined to one side of flower; filaments linear to linear-lanceolate or triangular, sometimes united at base; pollen in

Fig. 111C–E

Macarenia P. Royen, Med. Bot. Mus. Herb. Rijksuniv. Utrecht 107:137 (1951), rev.

Roots unknown; stems absent or indistinct and represented by amorphous, somewhat corm-like base or holdfast, merging into leaves, ±7 mm wide. Leaves more or less in a basal rosette, up to 30 cm long; petiole terete, up to 10 cm long, provided at base with an up to 3-mm-long, obtuse stipule; blades repeatedly forked, ultimate segments linear up to 15 mm long, each with a distinct nerve. Spathellas each containing 10–20 flowers, club-shaped, up to 12 cm long, solitary or 2 or 3 together, enveloped at base by 2 membranous bracts, individual flowers without a spathella occasionally found. Flowers 10–20, erect in a single spathella; peduncles terete, slightly winged, up to 3 cm long; tepals 2–5, lanceolate, ±0.8 mm long; stamens 2–4, up to 4 mm long; anthers dehiscing introrsely. Capsules ellipsoidal to obovoid, up to 4 mm long; valves equal, each with 3 ribs; stigmas simple. One species, M. clavigera P. Royen, Macarena Mountains, Colombia. 16. Marathrum Humboldt & Bonpland Figs. 104H, 111F, G Marathrum Humboldt & Bonpland, Pl. Aequin. 1:39. t. 11 (dated 1806, publ. 1808); van Royen, Meded. Bot. Mus. Herb. Rijksuniv. Utrecht 107:70–91, 131–133 (1951), rev.

Roots thread-like and slightly flattened, branched; stems prostrate, flattened, often short and disk-like. Leaves arranged along lateral margins of prostrate

Fig. 111. Podostemaceae-Podostemoideae. A, B Lophogyne helicandra. A Flowering shoot (1 mm). B Flower (0.5 mm). C–E Macarenia clavigera. C Spathella in longitudinal section (2 mm). D Flower (1 mm). E Flowering plant (1 mm). F, G Marathrum utile. F Elongate root with subopposite pairs of sterile shoots and one flowering shoot (1 cm). G Flower (1 mm). (Orig. Cook)

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monads. Capsules ellipsoidal, opening by 2 equal or subequal valves; each valve with 3 ribs, the ribs sometimes winged; pedicel in fruit expanded and cup-like at tip in some species; stigmas 2, linear to boat- or spoon-shaped, joined at base, often toothed at tip. Seeds ± 200–1,500. About 25 species (probably less when critically examined), Mexico, Central America, West Indies and north-western South America.

17. Mourera Aublet

Figs. 104G, K, 112A,B

Mourera Aublet, Hist. Pl. Guiane 582 (1775).

Roots 0 in M. fluviatilis Aublet, thread-like in M. aspera (Bongard) Tulasne and M. schwackeana Warming, insufficiently documented in other species; stems creeping, simple, 1–20 cm long, 0.5–5 cm thick, merging with leaf bases; holdfasts developing from leaf bases, polymorphic, clawshaped to tendril-like, up to 4 cm long. Leaves in basal rosettes, very variable, 8–100(–200) cm long, elliptical or pinnately lobed with marginal fimbriae, or repeatedly forked into capillary segments, ultimate segments inrolled when young, with hairs along concave sector; upper surface in M. fluviatilis very coarse and provided with warts and rigid, conical, vascularised prickles, in 2 other species with warts only; lower surface in all species glabrous, sometimes with prominent palmate to net-like veins; leaf bases cuneate, merging with the holdfast; sheaths simple or double. Spathellas tubular, 10–15 mm long, splitting irregularly. Flowers alternating with bracts in a stalked, 2-sided, simple or forked, raceme-like inflorescence, with up to 90 flowers, or rarely reduced to 1 or 2 flowers, anthesis starting at distal end; pedicels pink to pale violet; bracts 5–13 mm long, borne between 2 flowers, occasionally with a leaf-like appendage, with double sheaths, appearing double boat-shaped, shorter than spathella; tepals free, 5–20; stamens 5–35(–40), in 1 or 2 whorls; filaments free or united in pairs or groups at base, linear, terete, pink to pale violet, persistent and indurate in fruit; anthers dehiscing extrorsely in inner whorl, introrsely in outer whorl. Capsules ovoid; valves equal, each with 2–13 ribs; stigmas linear or spathulate. Seeds up to 2,000 or more in each capsule. About six species, northern to central South America. 18. Oserya Tulasne & Weddell

Fig. 112C, D

Oserya Tulasne & Weddell, Ann. Sci. Nat., Bot. III, 11:105 (1849).

Fig. 112. Podostemaceae-Podostemoideae. A, B Mourera fluviatilis. A Flowering shoot (3 cm). B Young capsule (1 mm). C, D Oserya minima. C Fragment of creeping root with one pair of opposite flowering shoots (5 mm). D Flower (1 mm). E–H Podostemum ceratophyllum. E Elongate stem arising from a creeping root (2 cm). F Persistent empty capsule valve (1 mm). G Flower at anthesis arising from ruptured spathella (3 mm). H Two short stems arising from a creeping root (3 mm). (Orig. Cook)

Roots thread-like, often becoming flattened when old, branched; stems short, developing at almost regular intervals along sides of root, usually in opposite or subopposite pairs. Leaf sheaths simple or double; petioles cylindrical or flattened; blades simple or repeatedly forked with filamentous ultimate segments, inrolled when young. Spathellas club-shaped, slightly exceeding base, opening irregularly. Flowers solitary, terminating the stem or several in leaf axils; pedicels 0.1–0.8(1.4) cm

Podostemaceae

327

long; tepals (2)3, when stamens 2, then one each side of the stamen and the third on back of the fork of filaments or rarely absent; stamens (1)2(3), when stamens 2, then usually united below into short andropodium; anthers basifixed, introrse in Mexican species, or extrorse in South American species; pollen in monads. Capsules ovoid; valves equal (Mexico) or unequal (South America) with oblique and acentric sutures, the larger one persistent, with 3–13 ribs; stigmas very short. Seeds up to ± 80. Six species, Mexico, northern South America and central Brazil.

The Asian species are now placed in Zeylanidium and Polypleurum. Crenias (south-eastern Brazil) and Devillea (Goiás, Brazil) are closely related to Podostemum. Crenias and Devillea are retained here as a distinct genera, although Philbrick and Novelo (2004) have sunk them into Podostemum.

19. Podostemum A. Michaux Figs. 104A, D, 112E–H

Roots thread-like to slightly flattened, perhaps 0 in R. carinata P. Royen, simple or branched; stems prostrate, flattened, often disk-like, merging into root and leaves. Leaf sheaths simple or double; petioles terete or slightly flattened, sometimes shortly winged; blades usually pinnate with forked lobes or palmate with lobes divided into filiform segments at tips; ultimate segments filamentous. Spathellas club-shaped or tubular, rupturing at apex. Flowers solitary or up to 20 in fascicles, arising from sheath pockets which often form cavities in the stem; pedicels (0.5–)2–10(–20) cm long; tepals 2–20 in a complete whorl, an incomplete whorl, or at one side of flower, some occasionally reduced to small teeth; stamens 2–30, in 1 or 2 whorls; filaments sometimes flattened at base; pollen in monads; anthers introrse. Capsules ellipsoidal to ovoid, laterally compressed; valves equal, each with 2 lateral ribs and a winged midrib; stigmas beak-like or clavate. Seeds numerous, up to ± 720 in R. penicillata Matthiesen. About 26 species (probably less when critically examined), northern South America.

Podostemum A. Michaux, Fl. Bor.-Amer. 2:164 (1803), Podostemon orth. mut.; van Royen, Acta Bot. Neerl. 3:228–244 (1954); Philbrick & Novelo, Syst. Bot. Monogr. 70:1–106 (2004), rev.

Roots thread-like, usually flattened, branched, attached to rocks with finger-like holdfasts; stems distinct, arising from lateral margins of root, usually in opposite or subopposite pairs, simple or branched; flowering stems only in one species (P. comatum) distinct from vegetative ones, both borne along same root. Leaf sheaths simple or double; 1–3(–11) stipular lobes or teeth per sheath, attached to associated sheath in leaf axils, or in P. muelleri Warming stipule 1 per leaf borne on dorsal side of shoot; leaf blades simple or, more often, repeatedly forked into linear segments or, in P. distichum (Chamisso) Weddell and P. irgangii C.T. Philbrick & A. Novelo, leaf segments (rachides) covered with triangular to subulate scales in halfwhorls or whorls. Spathellas club-shaped, splitting irregularly from top. Flowers 1–several per stem; pedicels 0.1–0.5(–0.8) cm long; tepals 3, linear, 2 at each side of andropodium base, in P. muelleri Warming sometimes 0, and usually 1 on top of andropodium in fork between the two filaments (abnormal flowers with proliferation of tepals and stamens are uncommon); stamens usually 2, borne on an andropodium; anthers dehiscing introrsely and latrorsely; pollen in dyads. Capsules ovoid; valves unequal, the larger persistent; each valve with 3 ribs; style short; stigmas linear, equal or unequal. Seeds from ± 30 to ± 100 but P. rutifolium subsp. ricciiforme (Liebmann) A. Novelo & C.T. Philbrick rarely sets seed and, if so, then only 1 or 2 ripen. About seven species (17 recognised by P. van Royen), America, extending from northern Argentina to eastern North America.

20. Rhyncholacis Tulasne

Fig. 113A, B

Rhyncholacis Tulasne, Ann. Sci. Nat., Bot. III, 11:95 (1849); van Royen, Med. Bot. Mus. Herb. Rijksuniv. Utrecht 107:133–138 (1951), rev.

21. Tulasneantha P. Royen

Fig. 113C, D

Tulasneantha P. Royen, Acta Bot. Neerl. 2:16 (1953).

Root insufficiently documented; stems very short; holdfasts 1–5 cm long, 0.5–2 cm wide. Leaves in basal rosettes, 10–30 cm long; petioles slightly flattened, smooth, 5–16 cm long, 1–3 mm wide; leaf blades fan-shaped, repeatedly forked. Spathellas club-shaped, 0.5–1 cm long. Flowers alternating with bracts, in a 2-sided, compressed, unbranched, raceme-like, 8–30 cm long inflorescence; bracts with double-sided sheaths, double-boat-shaped, 0.5–1 cm long; pedicels 1–3.5 cm long; tepals 6–10 or rarely rudimentary, lanceolate, ±0.5 mm long; stamens 6–10, in 1 whorl, 5–12.5 mm long; filaments terete, united halfway or slightly less into

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ultimate divisions forked and hair-like; flowers in fascicles of up to 13; tepals 3 or 4; stamens 2(3), confined to one side of flower; stamen filaments filiform, persistent, indurate, remaining attached to ribs of capsule after anthesis; capsule valves with 3 ribs; seeds up to 1,000 or more. One species, V. plumosa Novelo & Philbrick, Jalisco & Oaxaca, Mexico. 23. Wettsteiniola Suessenguth

Fig. 114E, F

Wettsteiniola Suessenguth, Repert. Spec. Nov. Regni Veg. 39:18 (1935).

Roots ribbon-like, up to 1 cm wide; stems disk-like and prostrate or represented by fused leaf bases. Leaves up to 30 cm long, either repeatedly pinnate or irregularly 2-pinnate with secondary pinnae repeatedly forked; ultimate segments filiform; bases of pinnae and pinnules with stipel-like appendages. Spathellas trumpet-shaped, up to 1 cm long. Flowers in fascicles of 2–8; pedicels up to 3.5 cm long; tepals linear to linear-lanceolate, (2–)3–6, in an incomplete whorl; stamens (1)2–4, in an incom-

Fig. 113. Podostemaceae-Podostemoideae. A, B Rhyncholacis dentata. A Flowering shoot (1 cm). B Flower (1 mm). C, D Tulasneantha monodelpha. C Leaf with detached inflorescence (2 cm). D Flower (3 mm). (Orig. Cook)

a tube below; pollen in monads; anthers introrse. Capsules ovoid to obovoid, 3.5–8 mm long; valves equal, each with 2 lateral ribs and a midrib slightly winged above; stigmas linear, persisting in fruit. Seeds unknown. One species, T. monadelpha (Bongard) P. Royen, western Brazil, which is close to Lonchostephus and Mourera. 22. Vanroyenella Novelo & C.T. Philbrick Fig. 114A–D Vanroyenella Novelo & C.T. Philbrick, Syst. Bot. 18:64 (1993).

Like Marathrum but leaf blades plumose with filamentous segments arising directly from rachis,

Fig. 114. Podostemaceae-Podostemoideae. A–D Vanroyenella plumosa. A Fragment of vegetative shoot (1 cm). B Filamentous leaf segments (1 mm). C Flower (0.5 mm). D Capsule with persistent filaments (0.5 mm). E, F Wettsteiniola pinnata. E Pinnate leaf (1 cm). F Capsule (1 mm). (Orig. Cook)

Podostemaceae

329

plete whorl; filaments sometimes united in pairs at base; anthers dehiscing introrsely; pollen in monads. Capsules ellipsoidal to ovoid; valves equal, each with 5 ribs; stigmas linear. Three species, southern Brazil and northern Argentina. Podostemoid Genera of Africa and Madagascar 24. Angolaea Weddell

Fig. 115A–C

Angolaea Weddell in A. de Candolle, Prodromus 17:300 (1873).

Roots unknown; stems branched, floating, up to 50 cm long. Leaves repeatedly forked, segments filiform. Spathellas ellipsoidal, borne on 5–8 mm long stalks. Flowers erect in the spathella, borne in umbel-like clusters; tepals 2, small, one each side of stamens or andropodium base if present; stamens 3(4), free or united below, borne in a cluster on one side of flower; andropodium very short or apparently 0; pollen in dyads; ovaries 1- or 2-locular. Capsules ellipsoidal; valves equal, each with 3 ribs; style short, erect, bearing a semi-globose stigma. One species, A. fluitans Weddell, from the River Cuanza, Angola. 25. Butumia G. Taylor

Fig. 115D–F

Butumia G. Taylor, Bull. Brit. Mus. Nat. Hist., Bot. 1:55 (1953).

Roots ribbon-like, ±2 mm wide, branched, resembling a liverwort, sometimes connected by thread-like roots; stems arising endogenously along margins of root, very short, not branched. Leaves in rosettes, sessile, subulate; inner leaves subtending flowers with stipule-like teeth. Spathellas ovoid, apiculate, ±1 mm long. Flowers erect in spathella, terminal, solitary, subsessile; tepals 2, minute, 1 each side of stamen; stamen 1; filament ultimately 1–2 mm long; anther ±0.5 mm long; pollen in dyads; ovary 1-locular. Capsules ovoid, ±1 mm long; valves equal, each with 3 ribs; stigmas unequal, flattened, ovate to elliptic in outline, divergent, persisting in fruit. One species, B. marginalis G. Taylor, Cameroon and Nigeria. M. Cheek et al. (2000) transferred this monotypic genus to Saxicolella. 26. Dicraeanthus Engler

Fig. 115G–I

Dicraeanthus Engler, Bot. Jahrb. Syst. 38:94 (1905).

Roots usually ± star-shaped; stems arising from upper surface of roots, elongate, branched, float-

Fig. 115. Podostemaceae-Podostemoideae. A–C Angolaea fluitans. A Flowering shoot (1 cm). B Rupturing spathella. C Flower with spathella removed (2 mm). D–F Butumia marginalis. D Creeping root with flowering shoots (2 cm). E Spathella with leaves (0.5 mm). F Flower (5 mm). G–I Dicraeanthus africanus. G Young plant (10 cm). H Fragment of a flowering shoot (1 cm). I Flower emerging from spathella (2 mm). (Orig. Cook)

ing, up to 1 m long, bearing leaves in 2 rows and, in a third row, flowers. Leaves arising at almost regular distances along opposite sides of stem; blades linear or up to 3 times forked, often fan-like; ultimate segments linear. Spathellas elongate. Flowers inverted within unruptured spathella, solitary or 3–20 in sessile or pedunculate clusters, mostly appearing to be opposite leaves; pedicels up to 60 mm long in fruit; tepals 2, much shorter than ovary, one each side of andropodium; andropodium rarely exceeding 1 mm in length; stamens 2, about half as long as ovary; filaments half as long as anther; pollen in dyads; ovaries 1-locular. Capsules cylindrical to oblong, all ribs running entire length of capsule; valves equal, persistent, each with 3 ribs;

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stigmas conical, erect, persistent in fruit. Two species, D. africanus Engler and D. zehnderi Hess, West and Central tropical Africa. 27. Djinga C. Cusset

Fig. 116A–C

Djinga C. Cusset, Fl. Cameroun 30:58 (1987).

Roots crustose or ribbon-like; stems arising endogenously along root margin, elongate, up to 12 cm or more long, irregularly branched, with long shoots or rosette-like short shoots. Leaves

0.5–1.5 cm long, subulate, entire or once forked. Spathellas ovoid to elliptic, arising in a rosette of linear or scale-like leaves. Flowers erect or inclined in spathella, solitary or 3 or 4 as part of dense short shoots; subsessile at anthesis; pedicels hardly elongating in fruit, up to 4 mm long; tepals 2, linear, much shorter than filament; stamen 1; filament 1.2–1.4 mm long; pollen in monads or in loose dyads; ovaries 1-locular. Capsules globose to subglobose, ± 1.2 mm long; valves unequal, each with 3 ribs; ribs somewhat flattened, wider than furrows; stigmas equal, linear to lanceolate and flattened, 0.7–0.8 mm long. One species, D. felicis C. Cusset, Cameroon. 28. Endocaulos C. Cusset

Fig. 116D, E

Endocaulos C. Cusset, Adansonia II, 12:560 (dated 1972, publ. 1973).

Roots ribbon-like, 0.3–1 mm wide, infrequently branched, closely attached to rock or partly floating; stems arising along margins of root, very short, not branched. Leaves simple, elongate, 2–3 cm long, swollen at base; base sometimes with 2 stipule-like lobes; elongate portions of leaves become detached at flowering time. Spathellas ovoid, obtuse at tip, opening irregularly. Flowers somewhat inclined within spathella, solitary; pedicel in fruit 2–3 mm long; tepals 2, obovate, one each side of andropodium base; stamens 2, borne on an andropodium, somewhat exceeding ovary; pollen in dyads; ovaries 2-locular. Capsules asymmetrically ovoid, somewhat flattened laterally, held obliquely at tip of pedicel; valves unequal and persistent, each with 7 ribs, the ribs nearest the sutures shortest and not extending whole length of capsule; stigmas 2, elongate, equal. One species, E. mangorense (Perrier) C. Cusset, Madagascar. 29. Ledermanniella Engler

Fig. 116. Podostemaceae-Podostemoideae. A–C Djinga felicis. A Plant with flower buds (1 cm). B Flower emerging from spathella (0.5 mm). C Capsule (0.5 mm). D, E Endocaulos mangorense. D Creeping root with sterile and flowering shoots (4 mm). E Two fertile shoots with one flower (1 mm). F–H Ledermanniella abbayesii. F Diagrammatic longitudinal section through a spathella (1 mm). G Fragment of a flowering shoot (5 mm). H Flower (2 mm). (Orig. Cook)

Fig. 116F–H

Ledermanniella Engler, Bot. Jahrb. Syst. 43:378 (1909); Cusset, Adansonia II, 14:271–275 (1974), rev.; Cusset, Bull. Mus. Natl Hist. Nat. Paris IV, B, Adansonia 5:361–390 (1983), rev.; Cusset, op. cit., 6:249–278 (1984), rev. Sphaerothylax Bischoff ex Krauss (1844), pro parte. Inversodicraeia Engler ex R.E. Fries (1914). Monandriella Engler (1926).

Roots ribbon-like or crustose; stems rudimentary to well developed, erect, simple or branched, from very short to 1 m or more long. Leaves very variable, simple, lobed or forked, linear with thread-like segments, or scale-like, imbricate, with entire or

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toothed margins and sometimes with apical teeth; imbricate scales and elongate leaves often develop on same stem in subg. Phyllosoma. Spathellas opening irregularly at tip. Flowers inverted within unruptured spathella, solitary or sometimes in sessile or stalked clusters; tepals 2, linear or filiform, one each side of solitary filament or andropodium base; stamens 1 or 2(3), either single or borne on an andropodium; andropodium usually more than 1 mm long, usually exceeding ovary at anthesis; pollen in monads or dyads. Ovaries 1-locular. Capsules ovoid to ellipsoidal or fusiform, with all ribs running entire length of capsule; valves unequal or rarely equal, each with 3 ribs; one or both valves persistent; stigmas linear, spreading or reflexed. About 46 species, tropical Africa, most in Central and West Africa. Molecular data indicate that this is not a natural genus (Moline et al. 2006); perhaps it should incorporate Dicraeanthus, Djinga and Macropodiella, or it should be split into smaller entities. 30. Leiothylax Warming

Fig. 117A, B

Leiothylax Warming, Overs. Kong. Danske Vidensk. Selsk. Skr. VI, 9:147 (1899); Cusset, Adansonia II, 20:199–209 (1980), rev. Leiocarpodicraeia (Engler) Engler (1905).

Roots crustose, entirely attached to rock or partly free and floating, stems branched, erect, up to 30 cm or more long. Leaves up to 4 cm long, linear or forked with linear segments. Spathellas ovoid or subglobose. Flowers inverted in unruptured spathella, solitary or in clusters; pedicels elongating after anthesis, becoming 1–2 cm long in fruit; tepals 2, one each side of andropodium base, much shorter than ovary or stamens, less than 0.4 mm long; stamens 2(3), borne on an andropodium; pollen in monads; ovaries 1-locular. Capsules borne on a gynophore up to 3 mm long, subglobose, smooth; valves equal, caducous; stigmas linear. Three species, Cameroon, D.R. Congo and Zambia. 31. Letestuella G. Taylor

Fig. 117C, D

Letestuella G. Taylor, Bull. Brit. Mus. Nat. Hist., Bot. 1:57 (1953); C. Cusset, Adansonia II, 20:199–209 (1980), rev.

Roots ribbon-like, branched; stems arising along margins of root, elongate, branched, up to 6 cm long. Leaves simple and linear or forked with linear segments, up to 4 cm long but usually less, often with stipule-like teeth at base. Spathellas oblong-

Fig. 117. Podostemaceae-Podostemoideae. A, B Leiothylax quangensis. A Distal part of a flowering shoot (2.5 mm). B Flower emerging from spathella (1 mm). C, D Letestuella tisserantii. C Distal part of shoot with spathellas (2.5 mm). D Flower (1 mm). E–G Macropodiella heteromorpha. E Fragment of shoot with leaves and unopened spathellas (10 cm). F Flower (1 mm). G Capsule viewed from the wide and from the narrow side (1 mm). (Orig. Cook)

ovoid, surface rough, becoming campanulate with revolute teeth after rupturing. Flowers erect in spathella, 2 or 3 in irregular clusters, or rarely solitary, subsessile at anthesis; pedicels elongating to become ±1 cm long in fruit; tepals 2, very small, 1 each side of base of andropodium or filament; stamens (1)2, when 2, then borne on an andropodium with very short filaments; pollen in monads; ovaries 1-locular. Capsules borne on a 0.4–0.5 mm long gynophore, globose, smooth and shiny, papil-

332


late at tip; valves equal and quickly shed; stigmas 2, linear to clavate. One species, L. tisserantii G. Taylor, western Africa, from Namibia to Niger. 32. Macropodiella Engler

Fig. 117E–G

Macropodiella Engler, Bot. Jahrb. Syst. 60:466 (1926); Cusset, Adansonia II, 17:293–303 (1978), rev.

Roots crustose or ribbon-like; stems simple or branched, very short or in some species up to ±80 cm long. Leaves usually divided into linear or capillary segments, or scale-like. Flowers inverted within unruptured spathella, solitary or in clusters of up to ± 12, either terminal or borne on elongated stems in leaf axils but appearing opposite leaves; pedicel becoming up to 1.5 cm long in fruit; tepals 2, linear to filiform, borne one each side of andropodium base; stamens 1–3; pollen in monads; ovaries 1-locular. Capsules borne on an up to 2-mm-long gynophore, ellipsoidal,

laterally flattened; valves equal and caducous, each with 3 ribs; stigmas variable, simple and elongate or divided into linear lobes or cock’s comb-like with flattened and serrated margins. Six species, tropical West Africa. 33. Paleodicraeia C. Cusset

Fig. 118A, B

Paleodicraeia C. Cusset, Adansonia II, 12:562 (dated 1972, publ. 1973).

Roots ribbon-like, branched, ±1 cm wide; stems arising along margins of root, up to ±2 cm long, branched and covered with at least 8 overlapping, scale-like leaves. Leaf bases persistent, 1.5–2 mm long, swollen and overlapping, shallowly 3-lobed; lateral lobes stipular; central lobe (or blade) linear and entire or bifid, caducous. Spathellas ovoid, splitting more or less regularly down one side. Flowers erect in spathella, subsessile, solitary, borne terminally; pedicel becoming up to 2 mm long in fruit; tepals 2, lanceolate, 0.5 mm long, 0.2 mm wide at base, one each side of andropodium base; stamens 2 borne on an andropodium; pollen unknown; ovaries 2-locular. Capsules ovoid; valves equal, each with 5 ribs; stigmas 2, linear and short. One species, P. imbricata (Tulasne) C. Cusset, Madagascar. 34. Saxicolella Engler

Fig. 118C, D

Saxicolella Engler, Bot. Jahrb. Syst. 60:456 (1926). Pohliella Engler (1926). Aulea C. Cusset ex Lebrun & Stork (1991), nom. illegit.

Roots crustose or ribbon-like; stems rudimentary or well developed, up to 20 cm long, somewhat flattened, simple or branched. Leaves simple and linear, or forked or laciniate; ultimate segments linear. Spathellas ovoid, opening irregularly at apex. Flowers erect in spathella, solitary or in loose clusters; pedicels elongating during anthesis, becoming up to 2 mm long; tepals 2, minute, one each side of filament base; stamen 1; pollen in dyads; ovaries 1- or 2-locular, depending on species. Capsules ellipsoidal to fusiform; valves equal and persistent, each valve with 3 or 5 narrow ribs; stigmas linear. About five species, in western tropical Africa, from Angola to Nigeria. Fig. 118. Podostemaceae-Podostemoideae. A, B Paleodicraeia imbricata. A Shoot with persistent capsule valve (1 mm). B Young capsule (0.5 mm). C, D Saxicolella nana. C Flowering shoot (5 mm). D Flower (2.5 mm). E–G Sphaerothylax abyssinica. E Crustose root bearing flowers and a flowering shoot (1 cm). F Capsule (0.5 mm). G Flower (0.5 mm). (Orig. Cook)

35. Sphaerothylax Bischoff ex Krauss Fig. 118E–G Sphaerothylax Bischoff ex Krauss, Flora 25:426 (1844). Anastrophea Weddell (1873).

Roots crustose, lobed with rounded lobes, resembling a liverwort, or ribbon-like and branched;

Podostemaceae

333

stems arising from upper surface of root, either very short and simple, or elongate and branched, up to 50 cm or more long. Leaves either scale-like or repeatedly forked with linear segments, up to 10 cm or more long. Spathellas globose, rupturing irregularly. Flowers inverted in unruptured spathella, arising from upper surface of root or on elongate stems, solitary or in clusters; tepals 2, one each side of filament base; stamen 1 or perhaps sometimes 2; filament often flattened; pollen in dyads; ovaries 2locular. Capsules subsessile, globose to subglobose; valves nearly equal, the larger one persistent, each with 3 wide and flattened ribs; stigmas ±0.2 mm long, linear to ovate. Two or perhaps more species, Madagascar, northern tropical and southern Africa. 36. Stonesia G. Taylor

Fig. 119A–C

Stonesia G. Taylor, Bull. Brit. Mus. Nat. Hist., Bot. 1, 3:59 (1953); Cusset, Adansonia II, 13:307–312 (1973), rev.

Roots crustose; stems simple or branched, short or elongate and then 10–40 cm long. Leaves repeatedly forked into linear segments or scale-like, when scale-like, then often lobed, with 1 or 2 of the lobes prolonged into thread-like appendages. Spathellas subsessile, ±2 mm long, subtended by 2–6, usually lobed, scale-like leaves. Flowers inverted in unruptured spathella, either sessile on upper surface of creeping root, or along elongate stems, solitary or in clusters; pedicel 0.4–1 cm long in fruit; tepals 3, one each side of andropodium base, the third between the two filaments; stamens 2, borne on an andropodium; pollen in dyads; ovaries 2-locular. Capsules broadly ellipsoidal; valves equal and persistent, each with 5 or 7 ribs, the ribs nearest the sutures shorter than others and not reaching ends of valves; stigmas linear. Four species, West tropical Africa, confined to a small region in Guinea and Sierra Leone. 37. Thelethylax C. Cusset

Fig. 119D–F

Thelethylax C. Cusset, Adansonia II, 12:564 (1972).

Roots ribbon-like, up to 1 mm wide, branched, bearing shoots along margins; vegetative shoots and reproductive short-shoots of different shapes; vegetative stems bearing up to 20 simple leaves in a rosette, or up to 4 elongate and repeatedly forked leaves with linear ultimate segments, up to 1 m long; flowering stems bearing few-leaved rosettes, widened and overlapping at base, filamentous above. Spathellas obovoid, splitting irreg-

Fig. 119. Podostemaceae-Podostemoideae. A–C Stonesia gracilis. A Crustose root bearing flowers and two elongate shoots bearing flowers (1 cm). B Flower (1 mm). C Capsule. D–F Thelethylax minutiflora. D Vegetative shoot (1 cm). E Flower (1 mm). F Inverted flower removed from the spathella (1 mm). (Orig. Cook)

ularly. Flowers strongly inclined or inverted in unruptured spathella, terminal, solitary; tepals usually 3, one each side of andropodium base, the third between the two filaments, or rarely 2 one each side of andropodium base; stamens 2, borne on an andropodium; pollen in dyads; ovaries 2-locular. Capsules obovoid, ±1 mm long; valves equal or unequal, each with 3 wide ribs; stigmas linear. Two species, T. isalensis (Perrier) C. Cusset and T. minutiflora (Tulasne) C. Cusset, Madagascar. 38. Winklerella Engler

Fig. 120A–C

Winklerella Engler, Bot. Jahrb. Syst. 38:97 (1905).

Roots crustose or ribbon-like, 4–5 mm wide; stems simple or branched, 1–3 cm long. Leaves up to 6 mm long, once or twice forked into linear segments; ultimate segments filamentous. Spathellas

334


obovoid. Flowers inverted in unruptured spathella, solitary or in clusters; pedicel up to 1 cm long in fruit; tepals 2, very small, not more than 0.2 mm long, one each side of andropodium base; stamens 2(3); pollen in monads; ovaries 1-locular. Capsules ovate in outline, strongly flattened laterally with 2 lateral wings, each longer than capsule and forming 2 flattened, horn-like protuberances each side of stigmas; valves equal; stigmas linear. One species, W. dichotoma Engler, Edéa, Cameroon. 39. Zehnderia C. Cusset

mens 2 or rarely 3; anthers ±0.7 mm long; pollen in monads; ovaries 1-locular. Capsules globose, 0.6–0.7 mm long; valves equal, each with 3 ribs; gynophore up to 8 mm long; stigmas equal, linear, 0.7–0.8 mm long. One species, Z. microgyna C. Cusset, Edéa, Cameroon, differing from Leiothylax in having a ribbed capsule.

Podostemoid Genera of Asia and Australia

Fig. 120D–F

Zehnderia C. Cusset, Fl. Cameroun 30:56 (1987).

Roots crustose; stems simple or branched, up to 3 cm long. Leaves ribbon-like, simple, 2–3 mm long, with stipules. Spathellas obovoid, ±1.5 mm long. Flowers inverted in unruptured spathella, arranged irregularly, either solitary or in clusters; pedicels up to 1.5 cm long in fruit; tepals 2, filiform, 0.2–0.3 mm long, one each side at base of andropodium; sta-

Fig. 120. Podostemaceae-Podostemoideae. A–C Winklerella dichotoma. A Distal part of flowering shoot (2.5 mm). B Flower (1 mm). C Transverse section of a capsule. D–F Zehnderia microgyna. D Flower (0.7 mm). E Flowering plant (4 mm). F Flower emerging from the spathella (0.7 mm). (Orig. Cook)

40. Cladopus H. Moeller

Fig. 121A–E

Cladopus H. Moeller, Ann. Jard. Bot. Buitenzorg 16:115 (1899). Mniopsis Mart. pro parte (1823 or 1824), nom. illegit. Lawiella Koidzumi, in Y. Doi, Fl. Satsum. 1, 2:21 (1927); emend. Koidzumi, in Y. Doi, Fl. Satsum. 2:94 (1931). Hemidistichophyllum Koidzumi, in Y. Doi, Fl. Satsum. 1, 3:24 (1928), cum descr.; Koidzumi, Fl. Symb. Orient.-Asiat. 96 (1930), in syn. Lecomtea Koidzumi (1929). Torrenticola Domin ex Steenis (1949).

Roots ribbon-like to almost cylindrical, irregularly lobed or branched, (0.5–)2–6 mm wide; stems erect, very short or up to 10 cm long, simple or rarely branched, arising along lateral margins of roots and on upper surface near sinuses of root lobes, some remaining embedded in root as rosettes with only the leaves emerging, others eventually emerging and bearing flowers. Leaves on young stems subulate, linear, with a few lateral teeth at base; leaves on older and flowering stems imbricate, scale-like, 2-lobed or palmately divided with 3–9 lobes or linear teeth, one or more median lobes sometimes with caducous, subulate to filamentous tips. Spathellas ovoid to globose, with an apical papilla, ±2 mm long, splitting at tip, ± circumscissile. Flowers solitary, terminal; pedicels very short to 1.25 mm long, sometimes elongating to ±3 mm long in fruit, the flowers barely emerging from spathella; tepals 2, minute, one each side of stamen or andropodium; stamens 1 or 2(3), when 2 or 3, then borne on an andropodium, when 1, then the anther halves separated by a broad connective; pollen in dyads. Capsules ovoid to almost globose, 1.25–1.75 mm long, borne on a short or a 1.5–3 mm long pedicel, obliquely 2-locular; valves unequal, each smooth or with 3 or 5 faint ribs, the larger valve persistent; stigmas linear or oblong-lanceolate. Seeds ± 100. About six species (more have been described), South-

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335

east and East Asia, New Guinea, north-eastern Australia. Cook and Rutishauser (2001) have sunk Torrenticola into Cladopus (see morphological and molecular data in Rutishauser and Pfeifer 2002, and Kita and Kato 2004b). 41. Diplobryum C. Cusset

Fig. 121F, G

Diplobryum C. Cusset, Adansonia II, 12:279 (1972).

Roots crustose and closely attached to rock, or cylindrical to ribbon-like with lower part attached to rock and upper part floating; stems very short, simple, apparently arising on upper surface of root and in the sinuses of root branches. Leaves imbricate, scale-like, ovate-elliptic, up to 2 mm long, either obtuse at tip or with an elongated, caducous, linear tip. Spathellas with an apical beak, opening by a slit. Flowers solitary; pedicel very short, barely bearing the flower above the leaves; tepals 2, linear, 1 each side of andropodium; stamens 2, borne on an andropodium; pollen in dyads. Capsules ellipsoidal to fusiform, laterally flattened, 1–1.5 mm long; valves equal and persistent, each with 9 ribs; stigmas linear or globose. Seeds ± 40–70, elongate with fine, longitudinal ribs. Four species, Southeast Asia, closely related to Hydrobryum. 42. Farmeria Willis

Figs. 104L, 121H–K

Farmeria Willis ex J.D. Hooker in Trimen, Handb. Fl. Ceylon 5:386 (1900). Maferria C. Cusset (1992).

Roots thread-like, cylindrical or somewhat flattened, 1–2(–4) mm wide, up to 25 mm long, branched, forming entangled mats, closely attached to rocks by holdfasts associated with root-borne shoots; stems very short, simple, arising along lateral margins of roots, some remaining embedded in root with only the leaves emerging, the others barely emerging and bearing flowers. Leaves scattered in groups along edge of root or 1, 2 or rarely 3 pairs on flowering stems, linear, 2–5 mm long, with thread- or band-like, caducous tips. Spathellas ovoid, splitting at tip. Flowers sessile, remaining within opened spathella, only anthers and stigmas emerging; tepals 2, linear to subulate, borne one each side of stamen filament; stamen 1; filament slightly flattened laterally, exceeding ovary and stigmas; pollen in dyads. Capsules sessile or with stalk up to 1 mm long, obliquely ovoid or subglobose, ±0.7 mm long, valves smooth

Fig. 121. Podostemaceae-Podostemoideae. A–E Cladopus nymani. A Ribbon-like root with shoot buds (2 mm). B Stem with unruptured spathella (1 mm). C Leaf (1 mm). D Flower (1 mm). E Persistent empty capsule valve (1 mm). F, G Diplobryum minutale. F Crustose root with six fertile shoots (1 mm). G Shoot with flower emerging from boat-shaped spathella (0.5 mm). H–K Farmeria indica. H Creeping root with vegetative shoots (5 mm). I Flowering shoot (1 mm). J Flower removed from spathella (1 mm). K Capsule (1 mm). (Orig. Cook)

or with 3 or 5 ribs, very unequal, in F. metzgerioides indehiscent, with 1 loculus aborting and the other with 1 or rarely 2 seeds, or in F. indica dehiscent or indehiscent, with (4–)8(–18) seeds; stigmas linear, unequal. Two species, F. indica Willis, south-western India and F. metzgerioides (Trimen) Willis, Sri Lanka, southern India. 43. Griffithella (Tulasne) Warming Fig. 122A–D Griffithella (Tulasne) Warming, Overs. Kong. Danske Vidensk. Selsk. Skr. VI, 11(1):13, 65 (1901).

Roots variable, star-shaped or ribbon-like, when ribbon-like, then up to 1 cm wide, green to red, usually closely attached to the rocks but some-

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times cup-like and then attached only by central part; stems simple, short, arising endogenously along lateral margins or from upper surface of root, with 2–6 leaves. Leaves imbricate, scale-like, 3–4 mm long, often caducous; leaf bases ± hooded, overlapping. Spathella broadly funnel-shaped, 2–3 mm long, splitting irregularly at tip into several teeth, the torn parts appearing fimbriate. Flowers solitary; pedicel ±3 mm long at anthesis, 4 mm or more long in fruit; tepals 2, one on each side of andropodium; stamens 2; andropodium 1.5–2 mm long, as long or longer than ovary; filaments 0.5–0.7 mm long; pollen in dyads. Capsules narrowly ovoid, 2.5 mm long, smooth;

valves unequal, the larger persistent; stigmas linear. Seeds ±250, ±0.2 mm long. One species, G. hookeriana (Tulasne) Warming, southern India. 44. Hanseniella C. Cusset

Fig. 122E–K

Hanseniella C. Cusset, Bull. Mus. Natl Hist. Nat. Paris IV, 14, B, Adansonia 1:36 (1992); M. Kato, Acta Phytotax. Geobot. 55:133–165 (2004), rev.

Roots crustose, green, irregularly lobed or branched, lobes ± 4 mm long; stems short, simple, scattered on upper surface of root. Leaves on juvenile or submerged stems linear, simple in irregular rosettes; leaves on flowering or emergent stems imbricate, scale-like, of two kinds, arranged in 4 rows; 2 rows scale-like and entire, ±1.5 mm long; remaining 2 rows 2-lobed, 1.25–1.75 mm long, with the sinus half or more as long as leaf, the lobes ± equal and bluntly rounded. Spathellas ellipsoidal, thick, with 2 or 3 ridges, rupturing irregularly at tip. Flowers solitary; pedicel 2–3 mm long, barely holding flowers above spathella; tepals 2, 1 each side of andropodium, linear-triangular, almost reaching top of ovary; stamens 2, borne on an andropodium, much exceeding ovary; pollen in dyads. Capsules ellipsoidal, somewhat flattened, borne on a ± 0.8 mm long gynophore; valves equal, each with 3 main ribs, in H. heterophylla sometimes with up to 3 fainter additional ribs; stigmas linear. Seeds 8–12, relatively large, 0.6–0.9 mm long. Two species, H. heterophylla C. Cusset and H. smitinandii M. Kato, both from northern Thailand. Molecular data of Kita and Kato (2004b) indicate a close relationship with Hydrobryum. 45. Hydrobryum Endlicher

Figs. 104C, 123A–D

Hydrobryum Endlicher, Gen. Pl. 1375 (1841), M. Kato, Acta Phytotax. Geobot. 55:133–165 (2004), rev. Polypleurella Engler (1927), pro parte. Euhydrobryum Koidzumi (1931). Hydroanzia Koidzumi (1935). Synstylis C. Cusset (1992).

Fig. 122. Podostemaceae-Podostemoideae. A–D Griffithella hookeriana. A Creeping root with two fruiting shoots (2 mm). B Flowering shoot (1 mm). C Young cup-shaped root (2 mm). D Persistent empty capsule valve (1 mm). E–K Hanseniella heterophylla. E Shoot with unopened spathella (1 mm). F Fragment of root bearing tufts of juvenile leaves (3 mm). G Shoot with capsule (1 mm). H Rosette of juvenile leaves (1 mm). I Two-lobed ‘ventral’ leaf (1 mm). J Flower (1 mm). K Placenta with seeds (0.5 mm). (Orig. Cook)

Roots crustose, irregularly lobed, 1–10(–30) cm in diameter; stems scattered on upper surface of root; vegetative shoots very short, rosette-like; flowering stems simple, very short. Leaves of vegetative stems 2–8, tufted, in 2 rows, linear, up to 12 mm long; leaves of flowering stems imbricate, scale-like, 2–8, in 2 rows, overlapping, enlarged at base, tips linear and caducous or lacking. Spathellas boat-shaped, opening irregularly at tip or splitting down one

Podostemaceae

side, thin, smooth. Flowers solitary, terminal, subsessile, remaining within the leaves; tepals 2 (rarely 1, 3 or 4), linear, 1–1.5 mm long; stamens 1 or 2(3), borne on andropodium at least as long as filaments; pollen in dyads. Capsules shortly pedicelled, ± ellipsoidal, sometimes laterally flattened; valves equal, each with 5 or 6(–9) ribs; styles short or 0; stigmas linear to cuneate, entire, toothed or lobed. Seeds 8–60, elliptic-patelliform,

337

surface granular. About 12 species, north-eastern India, Nepal, Bhutan, southern Central China, North Vietnam, Thailand and southern Japan, ten species in Thailand. The genus Synstylis was based on Polypleurella micranthera Engler; we are convinced it belongs in the genus Hydrobryum. Diplobryum is also very close to Hydrobryum. 46. Polypleurum Warming

Figs. 104I, 123E, F

Polypleurum Warming, Overs. Kong. Danske Vidensk. Selsk. Skr. VI, 11(1):464 (1901). Podostemum auctt. Ind., non A. Michaux (1803).

Roots usually ribbon-like or sometimes threadlike, usually lower part closely attached to rock with upper part free, or sometimes entirely attached to rock; free parts usually repeatedly forked, up to 50 cm long, rather tough, sometimes resembling Fucus; holdfasts often branched; stems short, developed endogenously at sometimes almost regular intervals along or near margin of root, bearing 2–8 or rarely more leaves; vegetative stems 0; flowering stems unbranched, less than 5 mm long. Leaves imbricate, scale-like, entire or lobed, with or without a caducous, elongate apical appendage. Spathellas sessile, ovoid to clubshaped, opening irregularly at tip. Flowers solitary, pedicellate; pedicel up to 1 cm long in fruit; tepals 2, 1 each side of andropodium or stamen, flattened, subulate; stamens 2(1), when 2, then borne on an andropodium; pollen in dyads. Capsules ellipsoidal, 2–3 mm long, sometimes laterally somewhat flattened; valves equal and persistent, each with 3, 5 or 7 ribs; style short or 0; stigmas linear or subconical. Seeds up to 200 or more. About eight species, Sri Lanka, India and Thailand. P. munnarense (Nagendran & Arekal) Mathew & Satheesh belongs to Polypleurum. 47. Thawatchaia M. Kato, Koi & Y. Kita Fig. 123G–K Fig. 123. Podostemaceae-Podostemoideae. A–D Hydrobryum japonicum. A Fragment of a crustose root with juvenile-leaved shoots (1 mm). B Tuft of juvenile leaves (3 mm). C Flowering shoot (1 mm). D Capsule with two equal valves (1 mm). E, F Polypleurum stylosum. E Seaweed-like root with marginal flowering shoots (1 cm). F Flowering shoot (2 mm). G–K Thawatchaia trilobata. G Fragment of crustose root bearing juvenile-leaved shoots (3 mm). H Three-lobed leaf (1 mm). I Shoot with spathella splitting (1 mm). J Flower emerging from spathella (1 mm). K Young capsule (1 mm). (Orig. Cook)

Thawatchaia M. Kato, Koi & Y. Kita, Acta Phytotax. Geobot. 55:66 (2004).

Roots crustose, green, irregularly lobed; stems very short, simple, scattered on upper surface of root; fertile stems appressed to or sometimes strongly oblique to root surface or rarely ascending, 2–3 mm long. Leaves on juvenile (submerged) stems linear, 2–5, in 2 ranks, in small rosettes, sheathed at base; leaves of flowering stems imbricate, scale-like, arranged in 4 rows; 4–6 per row, upper ones 3-lobed

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or uppermost one sometimes 2-lobed with a lateral lobe reduced, 1.5–3 mm long; lobes acute, the median usually somewhat longer than the laterals. Spathellas ellipsoidal, thin, not ridged, rupturing irregularly at tip. Flowers solitary; pedicel 2–2.5 mm long, barely holding flowers above spathella; tepals 2, 1 each side of andropodium, linear-triangular, almost reaching top of ovary; stamens 2, borne on andropodium, exceeding ovary; pollen in dyads. Capsules ellipsoidal, somewhat flattened; valves equal, each with 3 or 4 ribs; stigmas linear. Seeds 14–18(–22). One species, T. trilobata M. Kato, Koi & Y. Kita, northern Thailand. 48. Willisia Warming

Fig. 124A–C

Willisia Warming, Overs. Kong. Danske Vidensk. Selsk. Skr. VI, 11(1):58 (1901). Mniopsis Mart. (1823 or 1824) pro parte, nom. illegit.

Roots usually ribbon-like or crustose and sometimes irregularly lobed or branched, 2–3 cm in diameter; stems arising along or near root margin, dimorphic; vegetative shoots caducous as the water level falls, simple or rarely branched, up to 50 cm long, almost leafless below, above with numerous, up to 8 cm long, filamentous leaves; flowering stems densely crowded, simple, rigid, erect, 2–10 cm long, closely covered with leaves. Leaves of flowering stems in 4 or 6 distinct rows, imbricate, scale-like, some entire, 2 rows with 2 scale-like, lateral teeth and a hair-like but caducous tip. Spathellas urn-shaped, forked at tip into 2 stiff teeth, distal part may fall off as a cap or it may persist in cleistogamous flowers until seeds are ripe. Flowers solitary, terminal, sessile; tepals 2, 1 each side of andropodium; stamens 2, borne on andropodium; pollen in dyads. Capsules smooth or middle nerve of each valve forming a rib; the larger valve persistent; stigmas linear. Seeds ± 80. Two doubtfully distinct species, W. arekaliana Shivamurthy & Sadanand, W. selaginoides (Beddome) Warming ex Willis, both south-western India. 49. Zeylanidium (Tulasne) Engler Figs. 104B, 124D–H Zeylanidium (Tulasne) Engler in Engler & Prantl, Nat. Pflanzenfam. ed. 2, 18a:61 (1928); sensu C. Cusset, Bull. Mus. Natl Hist. Nat. Paris IV, 14, B, Adansonia 1:28 (1992). Podostemum auctt. Ind., non A. Michaux (1803). Hydrobryopsis Engler (1928).

Roots thread-like, subcylindrical and forked, or ribbon-like and pinnately lobed, lobes sometimes

Fig. 124. Podostemaceae-Podostemoideae. A–C Willisia selaginoides. A Crustose root with one vegetative and two young fertile shoots (2 cm). B Flowering shoot (1 mm). C Persistent empty capsule valve (1 mm). D–H Zeylanidium. D–F Z. olivaceum. D Crustose root with six fruiting shoots (5 mm). E Flowering shoot (2 mm). F Crustose root with vegetative shoots (5 mm). G, H Z. lichenoides. G Ribbon-like root with young fertile shoots (5 mm). H Spathella emerging from leaves (2 mm). (Orig. Cook)

overlapping or foliose, 1–10(–30) cm diameter and irregularly lobed; stems simple, short or somewhat elongate, simple, scattered on upper surface of root or in the sinuses of root lobes; erect structures, up to 3 cm long, stalked below and terminating in photosynthetic filaments may also arise from upper surface of root; flowering stems erect or rather prostrate, with scale-like leaves. Leaves of vegetative stems thread-like, (0.5–)2–5(–30) cm long; leaves of flowering stems imbricate, scale-like, those at base terminating in a caducous, threadlike tip, those below flowers rounded. Spathellas ovoid or boat-like, with an apical beak, opening at tip or by a longitudinal slit, remaining embedded in surrounding leaves or carried well above leaves. Flowers subsessile or pedicellate; tepals 2, one

Podostemaceae

each side of andropodium or stamen; stamens 2 or rarely 1, when 2, then borne on an andropodium; pollen in dyads. Capsules ellipsoidal to subglobose, 2–5 mm long; valves unequal, the larger one persistent; each valve smooth or with 3 ribs; stigmas slightly unequal, conical to linear, sometimes slightly flattened and fan-like. Seeds ± 40 in Z. sessilis (Willis) C.D.K. Cook & R. Rutishauser. Five or six species, Sri Lanka, southern, western and north-eastern India, Myanmar.

Selected Bibliography Ameka, G.K., Pfeifer, E., Rutishauser, R. 2002. Developmental morphology of Saxicolella amicorum and S. submersa (Podostemaceae: Podostemoideae) from Ghana. Bot. J. Linn. Soc. 139:255–273. Ameka, K.G., Clerk, C.G., Pfeifer, E., Rutishauser, R. 2003. Developmental morphology of Ledermanniella bowlingii (Podostemaceae) from Ghana. Pl. Syst. Evol. 237:165–183. Ancibor, E. 1990. Anatomia de las especies Argentinas de Podostemum Michaux (Podostemaceae). Parodiana 6:31– 47. APG II 2003. See general references. Battaglia, E. 1987. Embryological questions. 11. Has the debated case of Podostemaceae been resolved? Annali Bot. (Roma) 45:37–64. Bezuidenhout, A. 1964. The pollen of the African Podostemaceae. Pollen Spores 6:463–478. Burkhardt, G., Schild, W., Becker, H., Grubert, M. 1992. Biphenyls and xanthones from the Podostemaceae. Phytochemistry 31:543–548. Burkhardt, G., Becker, H., Grubert, M., Thomas, J., Eicher, T. 1994. Bioactive chromenes from Rhyncholacis penicillata. Phytochemistry 37:1593–1597. Capers, R.S., Les, D.H. 2001. An unusual population of Podostemum ceratophyllum (Podostemaceae) in a tidal Connecticut river. Rhodora 103:219–223. Cario, R. 1881. Anatomische Untersuchung von Tristicha hypnoides Spreng. Bot. Zeitung 39:25–33, 41–48, 57– 64, 73–82, pl. I. Chase, M.W., Fay, M.F., Savolainen, V. 2000. Higher-level classification in the angiosperms: new insights from perspective of DNA sequence data. Taxon 49:685–704. Cheek, M. 2003. A new species of Ledermanniella (Podostemaceae) from western Cameroon. Kew Bull. 58:733–739. Cheek, M., Onana, J., Pollard, P. 2000. The plants of Mount Oku and the Ijim Ridge. Royal Botanic Gardens, Kew. Collinson, M.E., Boulter, M.C., Holmes, P.L. 1993. Magnoliophyta (Angiospermae). In: Benton, M.J. (ed.) The fossil record, 2. London: Chapman and Hall. Connelly, W.J., Orth, D.J., Smith, R.K. 1999. Habitat of the riverweed darter, Etheostoma podostemonae Jordan, and the decline of riverweed, Podostemum ceratophyllum, in the tributaries of the Roanoke River, Virginia. J. Freshwater Ecol. 14:93–102. Cook, C.D.K. 1996a. Aquatic plant book, 2nd revised edn. The Hague: SPB Academic.

339

Cook, C.D.K. 1996b. Aquatic and wetland plants of India. Oxford: Oxford University Press. Cook, C.D.K. 1999. The number and kinds of embryobearing plants which have become aquatic: a survey. Perspectives Pl. Ecol. Evol. Syst. 2:79–102. Cook, C.D.K., Rutishauser, R. 2001. Name changes in the Podostemaceae. Taxon 50:1163–1167. Cusset, G. 1974. Quelques traits remarquables de l’organisation du Thelethylax minutiflora C. Cusset (Podostémacée). In: Actes 99ème Congrès National des Sociétés Savantes, Besançon, 1974, Sciences, fasc. 2, pp. 177–188. Cusset, C. 1978. Contribution à l’étude des Podostemaceae. 5. Le genre Macropodiella Engl. Adansonia II, 17:293–303. Cusset, C. 1980. Contribution à l’étude des Podostemaceae. 6. Les genres Leiothylax, et Letestuella. Adansonia II, 20:199–207. Cusset, C. 1983 (publ. 1984). Contribution à l’étude des Podostemaceae. 7. Ledermanniella Engl. sous-genre Phyllosoma C. Cusset. Bull. Mus. Natl Hist. Nat. Paris V, B, Adansonia 4:361–390. Cusset, C. 1984. Contribution à l’étude des Podostemaceae. 8. Ledermanniella Engl. sous-genre Ledermanniella. Bull. Mus. Natl Hist. Nat. Paris VI, B, Adansonia 3:249– 278. Cusset, C. 1987. Podostemaceae et Tristichaceae. In: Satabié, B., Morat, Ph. (eds) Flore du Cameroun 30:51–99. Cusset, C. 1992. Contribution à l’étude des Podostemaceae. 12. Les genres asiatiques. Bull. Mus. Natl Hist. Nat. Paris IV, B, Adansonia 14:13–54. Cusset, G., Cusset, C. 1988. Etude sur les Podostemales. 10. Structures florales et végétatives des Tristichaceae. Bull. Mus. Natl Hist. Nat. Paris IV, B, Adansonia 10:179– 218. Cusset, G., Cusset, C. 1989. Biogéographie évolutive de Tristicha trifaria (Bory ex Willd.) Sprengel. Bull. Mus. Natl Hist. Nat. Paris IV, B, Adansonia 11:39–70. Davis, G.L. 1966. See general references. Engler, A. 1928. Reihe Podostemales. In: Engler, A., Prantl, K., Die natürlichen Pflanzenfamilien, ed. 2, 18a. Leipzig: W. Engelmann, pp. 1–68, 483–484. [published as volume in 1930] Gessner, F., Hammer, L. 1962. Ökologisch-physiologische Untersuchungen an den Podostemonaceen des Caroni. Intl Rev. Gesell. Hydrobiol. 47:497–541. Goebel, K. 1933. Organographie der Pflanzen, 3. Samenpflanzen, ed. 3. Jena: G. Fischer. Grubert, M. 1970. Untersuchungen über die Verankerung der Samen von Podostemonaceen. Intl Rev. Gesell. Hydrobiol. 55:83–114. Grubert, M. 1974. Podostemaceen-Studien. Teil 1. Zur Oekologie einiger venezolanischer Podostemaceen. Beitr. Biol. Pflanzen 50:321–391. Grubert, M. 1976. Podostemaceen-Studien. Teil 2. Untersuchungen über die Keimung. Bot. Jahrb. Syst. 95:455– 477. Grubert, M. 1991. Ecologia de fanerógamas de saltos tropicales adaptadas en forma extrema. Natúra (Caracas) 91:54–61. Gustafsson, M.H.G., Bittrich, V., Stevens, P.F. 2002. Phylogeny of Clusiaceae based on rbcL sequences. Intl J. Pl. Sci. 163:1045–1054. Hammond, B.L. 1936. Regeneration of Podostemon ceratophyllum Michx. Bot. Gaz. 97:834–845.

340


Hiyama, Y., Tsukamoto, I., Imaichi, R., Kato, M. 2002. Developmental anatomy and branching of roots of four Zeylanidium species (Podostemaceae), with implications for evolution of foliose roots. Annals Bot. 90:735–744. Hutchens, J.J., Wallace, J.B., Romaniszyn, E.D. 2004. Role of Podostemum ceratophyllum Michx. in structuring benthic macroinvertebrate assemblages in a southern Appalachian river. J. N. Amer. Benthol. Soc. 23:713– 727. Imaichi, R., Ichiba, T., Kato, M. 1999. Developmental morphology and anatomy of the vegetative organs in Malaccotristicha malayana (Podostemaceae). Intl J. Pl. Sci. 160:253–259. Imaichi, R., Maeda, R., Suzuki, K., Kato, M. 2004. Developmental morphology of foliose shoots and seedlings of Dalzellia zeylanica (Podostemaceae) with special reference to their meristems. Bot. J. Linn. Soc. 144:289–302. Imaichi, R., Hiyama, Y., Kato, M. 2005. Leaf development in absence of a shoot apical meristem in Zeylanidium subulatum (Podostemaceae): evolutionary implications. Ann. Bot. 96:51–58. Jäger-Zürn, I. 1967. Embryologische Untersuchungen an vier Podostemaceen. Oesterr. Bot. Z. 114:20–45. Jäger-Zürn, I. 1970. Morphologie der Podostemaceae. I. Tristicha trifaria (Bory ex Willd.) Spreng. Beitr. Biol. Pflanzen 47:11–52. Jäger-Zürn, I. 1992. Morphologie der Podostemaceae. II. Indotristicha ramosissima (Wight) van Royen (Tristichoideae). Trop.-subtrop. Pflanzenwelt 80:1–48. Mainz: F. Steiner. Jäger-Zürn, I. 1994. Morphologie der Podostemaceae. IV. Zur Kenntnis der dithekischen Blätter bei Podostemum subulatum Gard. (Podostemoideae). Beitr. Biol. Pflanzen 68:391–419. Jäger-Zürn, I. 1995. Morphologie der Podostemaceae. III. Dalzellia ceylanica (Gard.) Wight (Tristichoideae). Trop.-subtrop. Pflanzenwelt 92:1–77. Mainz: F. Steiner. Jäger-Zürn, I. 1997a. Comparative morphology of the vegetative structures of Tristicha trifaria, Indotristicha ramosissima and Dalzellia ceylanica. Aquat. Bot. 57:71–96. Jäger-Zürn, I. 1997b. Embryological and floral studies in Weddellina squamulosa Tul. (Podostemaceae, Tristichoideae). Aquat. Bot. 57:151–182. Jäger-Zürn, I. 1999. Developmental morphology of the shoot system of Podostemum subulatum (Podostemaceae–Podostemoideae). Beitr. Biol. Pflanzen 71:281–334. Jäger-Zürn, I. 2000a. Developmental morphology of roots and root-born shoots of Podostemum subulatum as compared with Zeylanidium olivaceum (Podostemaceae–Podostemoideae). Pl. Syst. Evol. 220:55–67. Jäger-Zürn, I. 2000b. Crustose root and root-borne shoots of Zeylanidium olivaceum (Podostemaceae– Podostemoideae). Flora 195:61–82. Jäger-Zürn, I. 2000c. The unusual ramification mode of Sphaerothylax abyssinica (Wedd.) Warm. (Podostemaceae–Podostemoideae). Flora 195:200– 227. Jäger-Zürn, I. 2002a. Comparative studies in the morphology of Crenias weddelliana and Maferria indica with reference to Sphaerothylax abyssinica (Podostemaceae). Bot. J. Linn. Soc. 137:63–84.

Jäger-Zürn, I. 2002b. Morphology and morphogenesis of ensiform leaves in Apinagia multibranchiata and Mourera fluviatilis (Podostemaceae– Podostemoideae). Flora 197:394–407. Jäger-Zürn, I. 2003a. The occurrence of apical septum in ovaries of Rhyncholacis, Apinagia, Marathrum and Mourera (Podostemoideae–Podostemaceae): taxonomic implications. Bot. Jahrb. Syst. 124:303–324. Jäger-Zürn, I. 2003b. The architecture of Zeylanidium olivaceum (Podostemaceae) inferred from the structure of the primary shoots. Pl. Syst. Evol. 241:103–114. Jäger-Zürn, I. 2005a. Structural analysis of the dissected ensiform leaves and shoot morphology of Marathrum foeniculaceum (Podostemaceae). Flora 200:229–244. Jäger-Zürn, I. 2005b. Shoot apex and spathella: two problematical structures of PodostemaceaePodostemoideae. Pl. Syst. Evol. 253:209–218. Jäger-Zürn, I. 2005c. Morphology and morphogenesis of ensiform leaves, syndesmy of shoots and an understanding of the thalloid plant body in species of Apinagia, Mourera and Marathrum (Podostemaceae). Bot. J. Linn. Soc. 147:47–71. Jäger-Zürn, I., Grubert, M. 2000. Podostemaceae depend on sticky biofilms with respect to attachment to rocks in waterfalls. Intl J. Pl. Sci. 161:599–607. Jäger-Zürn, I., Mathew, C.J. 2002. Cupula structure of Dalzellia ceylanica and Indotristicha ramosissima (Podostemaceae). Aquat. Bot. 72:79–91. Jäger-Zürn, I., Novelo, R.A., Philbrick, C.T. 2005. Microspore development in PodostemaceaePodostemoideae, with implications on the characterization of the subfamilies. Pl. Syst. Evol. 256:209–216. Johri, B.M. et al. 1992. See general references. Kapil, R.N. 1970. Podostemaceae. In: Proc. Symp. Comparative Embryology of Angiosperms. Bull. Indian Natl Sci. Acad. 41:104–109. Kato, M., Kita, Y., Koi, S. 2003. Molecular phylogeny, taxonomy and biogeography of Malaccotristicha australis comb. nov. (syn. Tristicha australis) (Podostemaceae). Austral. Syst. Bot. 16:177–183. Kato, M., Koi, S., Kita, Y. 2004. A new foliose-rooted genus of Podostemaceae from Thailand with a note on root evolution. Acta Phytotax. Geobot. 55:65–73. Kato, L., de Oliveira, C.M.A., Bittrich, V., Amaral, M.C.E. 2005. Xanthones from Weddellina squamulosa Tul. (Podostemaceae). Biochem. Syst. Ecol. 33:331–334. Khosla, Ch., Mohan Ram, H.Y. 1993. Morphology of flower, fruit and seed in Polypleurum stylosum. Aquat. Bot. 46:255–262. Khosla, C., Shivanna, K.R., Mohan Ram, H.Y. 2000. Reproductive biology of Polypleurum stylosum (Podostemaceae). Aquat. Bot. 67:143–154. Khosla, C., Shivanna, K.R., Mohan Ram, H.Y. 2001. Cleistogamy in Griffithella hookeriana (Podostemaceae). S. African J. Bot. 67:320–324. Kita, Y., Kato, M. 2001. Infrafamilial phylogeny of the aquatic angiosperm Podostemaceae inferred from the nucleotide sequence of the matK gene. Pl. Biol. 3:156–163. Kita, Y., Kato, M. 2004a. Phylogenetic relationships between disjunctly occurring groups of Tristicha trifaria (Podostemaceae). J. Biogeogr. 31:1605–1612. Kita, Y., Kato, M. 2004b. Molecular phylogeny of Cladopus and Hydrobryum (Podostemaceae, Podostemoideae)

Podostemaceae with implications for their biogeography in East Asia. Syst. Bot. 29:921–932. Kita, Y., Kato, M. 2005. Seedling developmental anatomy of an undescribed Malaccotristicha species Podostemaceae, (subfamily Tristichoideae) with implications for body plan evolution. Pl. Syst. Evol. 254:221–232. Koi, S., Kato, M. 2003. Comparative developmental anatomy of the root in three species of Cladopus(Podostemaceae). Ann. Bot. 91:927–933. Koi, S., Imaichi, R., Kato, M. 2005. Endogenous leaf initiation in the apical-meristemless shoot of Cladopus queenslandicus (Podostemaceae) and implications for evolution of shoot morphology. Intl J. Pl. Sci. 166:199– 206. Léonard, J. 1993. Etude phytosociologique des chutes de la Tshopo (Kisangani–Zaïre). Bull. Jard. Bot. Natl Belgique 62:283–347. Léonard, J., Dessart, P. 1994. Avis de recherche: Torridincolidés (Coleoptera) vivant en symbiose avec Podostémacées (Podostémales). Bull. Ann. Soc. Roy. Belge Entomol. 130:71–76. Les, D.H., Philbrick, C.T., Novelo, R.A. 1997. The phylogenetic position of river-weeds (Podostemaceae): insights from rbcL sequence data. Aquat. Bot. 57:5–27. Lobreau-Callen, D., LeThomas, A., Suarez-Cervera, M. 1998. Ultrastructural characters of the pollen of some Podostemales. Affinities with advanced Rosidae (in French). C. R. Acad. Sci. Paris III, 321:335–345. Mai, D.H. 1985. Entwicklung der Wasser- und Sumpfpflanzen-Gesellschaften Europas von der Kreide bis ins Quartär. Flora 176:449–511. Mathew, C.J., Satheesh, V.K. 1997. Taxonomy and distribution of the Podostemaceae in Kerala, India. Aquat. Bot. 57:243–274. Mathew, C.J., Jäger-Zürn, I., Nileena, C.B. 2001. Dalzellia gracilis – a new species of Podostemaceae (Tristichoideae) from Kerala, India. Intl J. Pl. Sci. 162:899– 909. Mathew, C.J., Nileena, C.B., Jäger-Zürn, I. 2003. Morphology and ecology of two new species of Polypleurum (Podostemaceae) from Kerala, India. Pl. Syst. Evol. 237:209–217. Matthiesen, F. 1908. Beiträge zur Kenntnis der Podostemaceen. Bibl. Bot. 1908:1–55, 9 pls. Mauritzon, J. 1933. Über die systematische Stellung der Familien Hydrostachyaceae and Podostemonaceae. Bot. Notiser 1933:172–180. Metcalfe, C.R., Chalk, L. 1950. See general references. Miyoshi, N., Kato, H. 1982. Pollen morphology by means of scanning electron microscope. 5. Angiospermae (Piperales, Podostemonales). Jap. J. Palynol. 28:7–11. Mohan Ram, H.Y., Sehgal, A. 1992. Podostemaceae – the strange family of aquatic angiosperms. Palaeobotanist 41:192–197. Mohan Ram, H.Y., Sehgal, A. 1997. In vitro studies on developmental morphology of Indian Podostemaceae. Aquat. Bot. 57:97–132. Mohan Ram, H.Y., Sehgal, A. 2001. Biology of Indian Podostemaceae. In: Rangaswamy, N.S. (ed.) Phytomorphology (Recent trends in plant sciences) Golden Jubilee Issue 2001. Delhi: International Society of Plant Morphologists, pp. 365–391.

341

Moline, P., Thiv, M., Ameka, G.K., Ghogue, J.-P., Pfeifer, E., Rutishauser, R. 2006. Molecular phylogeny and morphological evolution of African Podostemaceae – Podostemoideae. Intl J. Pl. Sci. (in press). Murguía-Sánchez, G., Novelo, R.A., Philbrick, C.T., Márquez Guzmán, G.J. 2001. Desarrollo de los verticilos sexuales de Vanroyenella plumosa Novelo & Philbrick. Acta Bot. Mex. 57:37–50. Murguía-Sánchez, G., Novelo, R.A., Philbrick, C.T., Márquez Guzmán, G.J. 2002. Embryo sac development in Vanroyenella plumosa, Podostemaceae. Aquat. Bot. 73:201–210. Noro, T., Suzuki, H., Kanayama, T. 1994a. Phenology and distribution of Hydrobryum japonicum Imamura (Podostemaceae) in the Kaminkawa River, Kagoshima, Japan (in Japanese). J. Jap. Bot. 69:162–166. Noro, T., Suzuki, H., Kanayama, T. 1994b. Water quality at the habitat of Hydrobryum japonicum Imamura (Podostemaceae) in Japan (in Japanese). J. Jap. Bot. 69:167–175. Novelo, R.A., Philbrick, C.T. 1997. Taxonomy of Mexican Podostemaceae. Spec. Issue Podostemaceae, Aquat. Bot. 57:275–303. Odinetz-Collart, O., Tavares, A.S., Enriconi, A. 2001. Response of Podostemaceae aquatic biocenosis to environmental perturbations in central Amazonian waterfalls. Verh. Intl Verein. Limnol. 27:4063–4068. Okada, H., Kato, M. 2002. Pollination systems inferred from pollen-ovule ratio of some species of Podostemaceae. Acta Phytotax. Geobot. 53:51–61. O’Neill, S.P., Osborn, J.M., Philbrick, C.T. 1997. Comparative pollen morphology of five New World genera of Podostemaceae. Aquat. Bot. 57:133–150. Oropeza, N., Mercado-Ruaro, P., Novelo, R.A., Philbrick, C.T. 1998. Karyomorphological studies of Mexican species of Marathrum (Podostemaceae). Aquat. Bot. 62:207–211. Oropeza, N., Palomino, G., Novelo, R.A., Philbrick, C.T. 2002. Karyomorphological studies in Oserya, Vanroyenella and Tristicha (Podostemaceae sensu lato). Aquat. Bot. 73:163–171. Osborn, J.M., O’Neill, S.P., El-Ghazaly, G. 2000. Pollen morphology and ultrastructure of Marathrum schiedeanum (Podostemaceae). Grana 39:221–225. Ota, M., Imaichi, R., Kato, M. 2001. Developmental morphology of the thalloid Hydrobryum japonicum (Podostemaceae). Amer. J. Bot. 88:382–390. Pannier, F. 1960. Physiological responses of Podostemaceae in their natural habitat. Intl Rev. Gesell. Hydrobiol. 45:347–354. Philbrick, C.T. 1984. Aspects of floral biology, breeding system, and seed and seedling biology in Podostemum ceratophyllum (Podostemaceae). Syst. Bot. 9:166– 174. Philbrick, C.T., Bogle, A.L. 1988. A survey of floral variation in five populations of Podostemum ceratophyllum Michx. (Podostemaceae). Rhodora 90:113–121. Philbrick, C.T., Crow, G.E. 1992. Isozyme variation and population structure in Podostemum ceratophyllum Michx. (Podostemaceae): implications for colonization of glaciated North America. Aquat. Bot. 43:311–325. Philbrick, C.T., Novelo, R.A. 1993. A fascinating family of aquatic flowering plants. Aquaphyte 13:1–7.

342


Philbrick, C.T., Novelo, R.A. 1995. New World Podostemaceae: ecological and evolutionary enigmas. Brittonia 47:210–222. Philbrick, C.T., Novelo, R.A. 1997. Ovule number, seed number and seed size in Mexican and North American species of Podostemaceae. Aquat. Bot. 57:183–200. Philbrick, C.T., Novelo, R.A. 1998. Flowering phenology, pollen flow, and seed production in Marathrum rubrum (Podostemaceae). Aquat. Bot. 62:199–206. Philbrick, C.T., Novelo, R.A. 2004. Monograph of Podostemum (Podostemaceae). Syst. Bot. Monogr. 70:1–106. Philbrick, C.T., Novelo, R.A., Irgang, B.E. 2004a. Two new genera of Podostemaceae from the state of Minas Gerais, Brazil. Syst. Bot. 29:109–117. Philbrick, C.T., Novelo, R.A., Irgang, B.E. 2004b. A new species of Ceratolacis (Podostemaceae) from the state of Minas Gerais, Brazil. Novon 14:108–113. Quiroz, F., Novelo, R.A., Philbrick, C.T. 1997. Water chemistry and the distribution of Mexican Podostemaceae: a preliminary evaluation. Aquat. Bot. 57:201–212. Rauh, W. 1937. Die Bildung von Hypokotyl- und Wurzelsprossen und ihre Bedeutung für die Wuchsformen der Pflanzen. Nova Acta Leopoldiana, n.s. 4:396–553. Razi, B.A. 1955. Some aspects of the embryology of Zeylanidium olivaceum and Lawia zeylanica. Bull. Bot. Soc. Bengal 9:36–41. Romano, G.R., Dwyer, J.D. 1971. A demonstration of phloem in the Podostemaceae. Bull. Torrey Bot. Club 98:46–53. Romo Contreras, V., Scogin, R., Philbrick, C.T., Novelo, R.A. 1993. A phytochemical study of selected Podostemaceae: systematic implications. Aliso 13:513–520. Royen, P. van 1951. The Podostemaceae of the New World. I. Proefschrift, P. Harte, Bergen op Zoom, pp. 1–151, 16 pls. Reissued in Med. Bot. Mus. Herb. Rijksuniv. Utrecht 107:1– 151, 16 pls. Royen, P. van 1953. The Podostemaceae of the New World. II. Acta Bot. Neerl. 2:1–21. Royen, P. van 1954. The Podostemaceae of the New World. Part III. Acta Bot. Neerl. 3:215–263. Rutishauser, R. 1995. Developmental patterns of leaves in Podostemaceae compared with more typical flowering plants: saltational evolution and fuzzy morphology. Canad. J. Bot. 73:1305–1317. Rutishauser, R. 1997. Structural and developmental diversity in Podostemaceae (river-weeds). Aquat. Bot. 57:29–70. Rutishauser, R., Grubert, M. 1994. The architecture of Mourera fluviatilis (Podostemaceae). Bot. Helv. 104:179– 194. Rutishauser, R., Grubert, M. 1999. The architecture of Mourera fluviatilis (Podostemaceae). Developmental morphology of inflorescences, flowers and seedlings. Amer. J. Bot. 86:907–922. Rutishauser, R., Grubert, M. 2000. Developmental morphology of Apinagia multibranchiata (Podostemaceae) from the Venezuelan Guyanas. Bot. J. Linn. Soc. 132:299–323. Rutishauser, R., Huber, K.A. 1991. The developmental morphology of Indotristicha ramosissima (Podostemaceae, Tristichoideae). Pl. Syst. Evol. 178:195–223. Rutishauser, R., Moline, P. 2005. Evo-devo and the search for homology (“sameness”) in biological systems. In:

Evolutionary developmental biology – new challenges to the homology concept? Theory Biosci. Spec. Issue 124, 2:213–241. Rutishauser, R., Pfeifer, E. 2002. Comparative morphology of Cladopus (including Torrenticola, Podostemaceae) from East Asia to north-eastern Australia. Austral. J. Bot. 50:725–739. Rutishauser, R., Novelo, R.A., Philbrick, C.T. 1999. Developmental morphology of New World Podostemaceae: Marathrum and Vanroyenella. Intl J. Pl. Sci. 160:29– 45. Rutishauser, R., Pfeifer, E., Moline, P., Philbrick, C.T. 2003. Developmental morphology of roots and shoots of Podostemum ceratophyllum (Podostemaceae– Podostemoideae). Rhodora 105:337–353. Rutishauser, R., Pfeifer, E., Novelo, R.A., Philbrick, C.T. 2005. Diamantina lombardii – an odd Brazilian member of the Podostemaceae. Flora 200:245–255. Savolainen, V., Fay, M.F. et al. 2000. See general references. Schenk, J.J., Thomas, D.W. 2004. A new species of Ledermanniella (Podostemaceae) from Cameroon. Novon 14:227–232. Schnell, R. 1967. Etudes sur l’anatomie et la morphologie des Podostémacées. Candollea 22:157–225. Schnell, R. 1994. Les stratégies végétales. Essai de morphologie évolutive. Paris: Masson. Schnell, R. 1998. Anatomie des Podostémacées. In: Carlquist, S., Cutler, D.F., Fink, S., Ozenda, P., Roth, I., Ziegler, H. (eds) Encyclopedia of plant anatomy: extreme adaptations in angiospermous hydrophytes. Berlin: Borntraeger, pp. 197–283. Schnell, R., Cusset, G. 1963. Remarques sur la structure des plantules de Podostemonaceae. Adansonia II, 3:358– 369. Sculthorpe, C.D. 1967. The biology of aquatic vascular plants. London: Edward Arnold. Sehgal, A., Mohan Ram, H.Y., Bhatt, J.R. 1993. In vitro germination, growth, morphogenesis and flowering of an aquatic angiosperm, Polypleurum stylosum (Podostemaceae). Aquat. Bot. 45:269–283. Sehgal, A., Sethi, M., Mohan Ram, H.Y. 2002. Origin, structure, and interpretation of the thallus in Hydrobryopsis sessilis (Podostemaceae). Intl J. Pl. Sci. 163:891–905. Soltis, D.E., Mort, M.E., Soltis, P.S., Hibsch-Jetter, C., Zimmer, E.A., Morgan, D. 1999. Phylogenetic relationships of the enigmatic angiosperm family Podostemaceae inferred from 18S rDNA and rbcL sequence data. Mol. Phylog. Evol. 11:261–272. Stevens, P.F. 2005. See general references. Suzuki, K., Kita, Y., Kato, M. 2002. Comparative developmental anatomy of seedling in nine species of Podostemaceae (subfamily Podostemoideae). Ann. Bot. 89:755–765. Taylor, G. 1953. Notes on Podostemaceae for the revision of the Flora of West Tropical Africa. Bull. Brit. Mus. Nat. Hist., Bot. 1:53–79. Troll, W. 1941. Vergleichende Morphologie der höheren Pflanzen, vol. 1/3, pp. 2007–2736. Berlin: Borntraeger. Tur, N.M. 1997. Taxonomy of Podostemaceae in Argentina. Aquat. Bot. 57:213–241. Ueda, K., Hanyuda, T., Nakano, A., Shiuchi, T., Seo, A., Okubo, H., Hotta, M. 1997. Molecular phylogenetic position of Podostemaceae, a marvellous aquatic flowering plant family. J. Pl. Res. 110:87–92.

Podostemaceae Uniyal, P.L., Mohan Ram, H.Y. 1994. Karyological studies in some members of Podostemaceae. Aquat. Bot. 47:85– 90. Uniyal, P.L., Mohan Ram, H.Y. 1996. In vitro germination and seedling morphology of Dalzellia zeylanica (Gardner) Wight (Podostemaceae). Aquat. Bot. 54:59–71. Vartak, V.D., Kumbhojkar, M.S. 1984. Palynological study of the family Podostemaceae from Western India. Biovigyanam 10:89–92. Vidyashankari, B. 1988a. Seed germination and seedling morphology in Indotristicha ramosissima (Podostemaceae) grown in vitro. Curr. Sci. 57:369– 373. Vidyashankari, B. 1988b. Developmental biology of Griffithella hookeriana. Ph.D. Thesis, University of Delhi, Delhi. Vidyashankari, B., Mohan Ram, H.Y. 1987. In vitro germination and origin of thallus in Griffithella hookeriana (Podostemaceae). Aquat. Bot. 28:161–169. Wächter, W. 1897. Beiträge zur Kenntniss einiger Wasserpflanzen. Flora 83:381–397. Warming, E. 1881. Familien Podostemaceae, I. Kong. Danske Vidensk. Selsk. Nat. Math. Afd. 2:1–34, pls I–VI.

343

Warming, E. 1882. Familien Podostemaceae, II. Kong. Danske Vidensk. Selsk. Nat. Math. Afd. 2:77–130, pls VII–XIV. Warming, E. 1888. Familien Podostemaceae, III. Kong. Danske Vidensk. Selsk. Nat. Math. Afd. 4:443–514. Warming, E. 1899. Familien Podostemaceae, V. Kong. Danske Vidensk. Selsk. Nat. Math. Afd. 9:105–154. Warming, E. 1901. Familien Podostemaceae, VI. Kong. Danske Vidensk. Selsk. Nat. Math. Afd. 11:1–67. Went, F.A.F.C. 1912. Untersuchungen über die Podostemaceen, II. Verhandl. Konink. Akad. Wetensch. Amsterdam 17:1–19. Went, F.A.F.C. 1926. Untersuchungen über die Podostemaceen, III. Verhandl. Konink. Akad. Wetensch. Amsterdam 25:1–59, 11 pls. Willis, J.C. 1902. Studies in the morphology and ecology of the Podostemaceae of Ceylon and India. Ann. Roy. Bot. Gard. Peradeniya 1:267–465.

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