Botanical Journal of the Linnean Society, 2002, 139, 255–273. With 3 figures Developmental morphology of Saxicolella amicorum and S. submersa (Podostemaceae: Podostemoideae) from Ghana K. GABRIEL AMEKA1, EVELIN PFEIFER2 and ROLF RUTISHAUSER2* Department of Botany, University of Ghana, P.0. Box LG 55, Legon, Accra, Ghana Botanischer Garten und Institut für Systematische Botanik, Universität, Zollikerstr. 107, 8008 Zurich, Switzerland 2 Received February 2002; accepted for publication April 2002 Saxicolella (six spp.) is a podostemoid genus occurring in tropical west Africa (Cameroon, Ghana, Nigeria). Taxonomically used characters such as root (with holdfasts), pollen (dyads in many Podostemoideae), capsules (with ribs) and seeds are demonstrated and discussed. This paper deals with the structure and development of two species, which are endemic to rivers in southern Ghana: Saxicolella amicorum J.B.Hall and Saxicolella submersa (J.B.Hall) C.D.K.Cook & Rutish. (syn. Polypleurum submersum J.B.Hall). Saxicolella amicorum has simple, one-flowered stems up to 3 cm long, whereas S. submersa has branched, many-flowered stems up to 25 cm long. Vegetative shoots can reach 12 cm (S. amicorum) and even 50 cm (S. submersa) in length. The latter species was previously placed in the Asian genus Polypleurum because the long floating axis was misinterpreted as a root which would be typical for Polypleurum. The long floating axis of S. submersa develops exogenous leaves and is actually a stem. Both S. amicorum and S. submersa have various features in common: vegetative parts (roots, stems, leaves) are elongate and very thin (diameter less than 1 mm); prostrate roots are narrow ribbons (twice as wide as thick); endogenous shoots in opposite pairs along the root; leaves usually simple and filiform; leaf bases with two attached ear-like stipules; spathella club-shaped to ellipsoidal; erect flowers with a solitary stamen; ovary ellipsoidal to fusiform, bilocular; capsules nearly isolobous, with three prominent ribs per valve (i.e. eight ribs per capsule including sutural ribs). Evolutionary dynamics of the root structures in African Podostemoideae such as Saxicolella include: formation of green prostrate ribbons as a result of dorsoventral root flattening; reduction of root caps; occurrence of adhesive hairs and exogenous holdfasts which are disk- or finger-like. Structural diversity and developmental patterns in the Ghanaian Saxicolella species are compared with other African Podostemoideae. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273. ADDITIONAL KEYWORDS: African Podostemaceae – aquatic angiosperms – developmental patterns – holdfasts – Polypleurum – silica bodies – stipules – systematics – water plants. INTRODUCTION The family Podostemaceae (including Tristichaceae of some authors) occurs on all continents except Antarctica and Europe. They are mainly restricted to tropical streams, rivers, waterfalls and cataracts with distinct seasonality, where they grow usually attached to rocks or other solid substrata. Hence they are haptophytes (Cook, 1996). All members of the family are rheophytes too (van Steenis, 1981). The vegetatively growing plants are completely submerged Corresponding author. E-mail: rutishau@systbot.unizh.ch in swiftly running water during the rainy season. Emergent flowers and fruits are formed when the water recedes during the dry season characterized by low rainfall. BIODIVERSITY AND BIOGEOGRAPHY The Podostemaceae are the largest family of strictly aquatic flowering plants (Cook, 1999). Most of the c. 280 species and many of the 46 genera are endemic to small geographical areas such as a single river or a country (Cook, 1996; Ameka, 2000). Species richness is highest in tropical America (van Royen, 1951, 1953, © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 255 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 1 256 K. G. AMEKA ET AL. THE GENUS SAXICOLELLA ENGLER Saxicolella was described by Engler (1926). Saxicolella is the third largest genus among the African Podostemaceae after Ledermanniella (44 species) and Macropodiella (six species). There are six Saxicolella species known, all occurring in tropical west Africa: S. amicorum in Ghana, S. flabellata (G. Taylor) C. Cusset in Nigeria and Cameroon, S. laciniata (Engl.) C. Cusset, S. marginalis (G. Taylor) C. Cusset ex Cheek and S. nana Engl. all in Cameroon, and S. submersa in Ghana according to Hall (1972), Lebrun & Stork (1991), Cusset (1987), Cook (1996), and Cheek, Onana & Pollard, 2000). Saxicolella amicorum and S. submersa (syn. Polypleurum submersum) were described as new species from Ghana in a paper by Hall (1972). The present developmental and morphological studies of the isotype material indicate that this latter species belongs in Saxicolella (Cook & Rutishauser, 2001). DEVELOPMENTAL MORPHOLOGY OF AFRICAN PODOSTEMOIDEAE There is a renewed interest in the study of comparative and developmental morphology of the Podostemaceae as exemplified by the work of Vidyashankari (1988), Rutishauser & Huber (1991), Sehgal, Mohan Ram & Bhatt (1993), Philbrick & Novelo (1995), Mohan Ram & Sehgal (1997), Rutishauser (1997), Jäger-Zürn (1997, 2000a, 2000b), Imaichi, Ichiba & Kato (1999), Rutishauser et al. (1999), Rutishauser & Grubert (2000), Uniyal & Mohan Ram (2001) and others. These studies have increased our knowledge and understanding of the plant form of Asian and Neotropic species. Morphological and developmental studies are lacking among the African taxa, except for Jäger-Zürn’s (2000c) contribution on Sphaerothylax abyssinica (Wedd.) Warm. The aim of the present and subsequent papers is to elucidate the architecture and developmental morphology of the Ghanaian and other African Podostemaceae (Ameka, 2000). It is hoped that this will stimulate further work on the African Podostemaceae by other botanists. PODOSTEMACEAE AS MORPHOLOGICAL MISFITS: FUZZINESS OF ORGAN CATEGORIES Podostemaceae are highly modified and many of them resemble algae, liverworts or mosses. The architecture of all Podostemaceae is anomalous compared with that of most other angiosperms, including aquatic forms. For example, a characteristic feature of aquatic angiosperms is the presence of aerenchyma (Sculthorpe, 1967). This tissue is lacking in the Podostemaceae. The modified morphologies of Podostemaceae are probably due to their haptophytic habit and their evolutionary histories in river rapids. Despite progress made in studies on architecture and comparative morphology of Podostemaceae members outside Africa, some morphological problems are yet to be resolved. For example, there is disagreement among contemporary botanists over interpretation of the vegetative body in the Podostemaceae. The vegetative body of Podostemaceae can be described as partially homologous with the classical root–shoot model (CRS model) that applies to most other angiosperms (e.g. Rutishauser, 1997; Jäger-Zürn, 2000a). Structural terms such as ‘root’, ‘shoot’, ‘stem’ and ‘leaf ’ do not necessarily imply a 1 : 1 correspondence (total homology) with organ categories of typical angiosperms. The terms ‘root’, ‘shoot’, ‘stem’ and ‘leaf ’ should be recognized as fuzzy sets, as organ categories with fuzzy borderlines which allow the acceptance of intermediates (Rutishauser, 1995, 1997). Another group of Podostemaceae students (e.g. Cusset & Cusset, 1988; Mohan Ram & Sehgal, 1992; Schnell, 1994) prefers to use the neutral term ‘thallus’ for the creeping structures which are called ‘root’ in the present paper. Herein we interpret the ‘root’ as an organ giving rise to endogenously formed ‘shoots’ whereas the ‘shoot’ is defined as a ‘stem’ that carries ‘leaves’ (except for rosulate shoots which seem to consist of leaves only because the stem is short). The fuzziness of podostemaceous organs will not be discussed in this paper. MATERIAL AND METHODS This work is based on the study of fixed and preserved plant materials deposited in the Ghana Herbarium (GC) and Kew Herbarium (K). The following specimens were used: Saxicolella amicorum J.B.Hall, synonym: Aulea amicorum (J.B. Hall) C. Cusset, nomen illeg., as listed in Lebrun & Stork (1991): Ghana, Western Region, © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 1954; Philbrick & Novelo, 1995). Tropical Africa is a second centre of diversity (Engler, 1928; Schnell, 1967; Cusset, 1987; Cook, 1996). Few taxa, however, extend to temperate regions. In Ghana there are four members of Podostemaceae. Three Podostemoideae taxa, namely Ledermanniella bowlingii (J.B. Hall) C. Cusset, Saxicolella amicorum J.B. Hall and Saxicolella submersa (J.B. Hall) C.D.K. Cook & Rutish. are endemic to three and two rivers, respectively, in southern Ghana, whereas Tristicha trifaria (Bory ex Willd.) Spreng. (Tristichoideae) is widespread in the country (Ameka et al., 1994). SAXICOLELLA FROM GHANA Ankasa Resource Reserve, Ankasa River. Ameka no. 113, November 21, 1998 (GC). RESULTS ROOTS AND HOLDFASTS Root architecture of S. amicorum and S. submersa is shown in Figures 1–17. The root tips of S. submersa have rudimentary caps (Figs 9–11). In S. amicorum we could not observe intact root tips. The roots of both species are thread-like, though slightly flattened (diameter 0.2–0.5 mm). Transverse sections of S. amicorum roots clearly show them as narrow and ribbonlike (about twice as wide as thick), with an outline which is planar towards the substratum and convex on the dorsal side. There is a central bundle with a few prosenchymatous vascular cells with xylem and phloem not distinguishable (Figs 3–5). Silica bodies, as typical for many Podostemaceae, are found in some epidermal and hypodermal cells of the dorsal (upper) root side whereas they are restricted to a few epidermal cells of the ventral (lower) root side (Fig. 4). The roots (as seen in cross-sections) of S. submersa are similar to those of S. amicorum. They are attached to the substratum by adhesive hairs which arise from the ventral side of the roots, perhaps in combination with bacterial slime (Figs 1,4,15,17; Jäger-Zürn & Grubert, 2000). Additional means of fixing podostemaceous roots to the substratum are holdfasts (also called haptera). The holdfasts of Saxicolella are often disklike. In S. submersa we found a few roots that had finger-like holdfasts (2 mm long). The holdfasts are produced exogenously from the root flanks and occur in opposite pairs (Figs 16,17,31). In S. amicorum the exogenous formation of the holdfasts is less obvious (Figs 6–8). The distance between consecutive pairs of holdfasts along the root is usually less than 5 mm, rarely up to 10 mm. Endogenous shoot buds originate from the root flanks, usually in opposite or subopposite pairs (Figs 1,2,12,13,28). They are positionally associated with the holdfasts (Figs 13–17,27). In S. submersa the shoots are directed upwards and the finger-like holdfasts point downwards. SHOOTS AND THEIR POSITION ALONG ROOTS Stem and leaf features of both Ghanaian Saxicolella species are shown in Figures 18–33, 43 and 44. Vegetative shoots are simple, unbranched and up to 12 cm in length in S. amicorum (Fig. 18); they are elongate, branched and up to 50 cm in S. submersa (Figs 43 and 44). The stems of both species are terete in transverse sections, with diameters of 0.4–0.8 mm (Figs 24,29). There is a prominent central strand of vascular tissue with no obvious differentiation into xylem and phloem elements. An additional weak bundle (leaf trace) may derive from the central vascular bundle and enter a leaf (Figs 23,24). In S. submersa cortical cells with thickened walls surround the central vascular tissue (Fig. 29). The stem epidermis of both species contains silica bodies, each one completely filling a cell. The surface of the silica bodies contains several holes that occur only on the side that is facing the stem periphery (Figs 25,26,30). After floral induction the shorter vegetative (sterile) shoots of both Ghanaian Saxicolella species are converted into reproductive (fertile) ones by the development of terminal flowers. The vegetative shoots of both species are usually longer than the reproductive ones. Roots may produce short reproductive shoots (<1 cm) with a single terminal flower (Figs 34,42). Saxicolella submersa has branched shoots. The reproductive lateral shoots arise in the axils of the alternately arranged leaves along the main stems (Figs 43,44,48). Flowers develop apically on these, often short, branches. LEAVES AND STIPULES The leaves of both Ghanaian Saxicolella species are green, thread-like and usually simple. They are inserted along the stem in a distichous order, with internode lengths of 6 mm or less (Figs 18,37,43,44). © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 Saxicolella submersa (J.B. Hall) C.D.K. Cook & Rutish., synonyms: Polypleurum submersum J. B. Hall; Aulea submersa (J.B.Hall) C.Cusset, nomen illeg., as listed in Lebrun & Stork (1991): Ghana, Eastern Region, Kwahu Nteso, Asuboni River. Hall & Bowling no. 38532, January 17, 1968 (material received from liquid isotype collections at GC and K). Thirty years later G. Ameka and M. Cheek (pers. comm.) could not find it again in the river Asuboni. We have to assume that it is extinct here. Additional sterile material for comparison (probably also belonging to S. submersa) was collected in Wli Falls, Ghana, by Ameka s.n., 3.xii.1997. The plant specimens used were fixed and preserved in 70% ethanol or formalin–acetic acid–ethanol (FAA). Preserved material stored in 70% ethanol was used for light and scanning electron microscopy (SEM). For microtome sections, specimens were embedded in Kulzer’s Technovit (2-hydroethyl methacrylate), as described in Igersheim (1993) and Igersheim & Cichocki (1996), and sectioned with a Microtom HM 355 rotary microtome and conventional microtome knife type C and D. The mostly 7 mm thick sections were stained with ruthenium red and toluidine blue (Weber & Igersheim, 1994). The permanent slides of the microtome sections are deposited at the Institute of Systematic Botany of the University of Zurich (Z). 257 258 K. G. AMEKA ET AL. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 Figures 1–8. Saxicolella amicorum. Root architecture and endogenous shoot formation (Ameka GC 113). Fig. 1. Young root portion, seen from below: thread-like but slightly flattened. Arrows point to nearly opposite pair of bulges due to formation of endogenous shoot buds. Asterisk denotes adhesive hairs on ventral root surface. Scale bar = 200 mm. Fig. 2. Another young root portion, seen from dorsal side. Left shoot bud with first coiled leaf (L). Right endogenous bud (arrow) still inside the root cortex. Scale bar = 250 mm. Figs 3 and 4. Cross-sections of young root. Note adhesive hairs on ventral root surface and bacterial slime. Arrows point to central vascular tissue. A hypodermal cell containing a silica body is marked with an asterisk. Scale bars = 60 mm. Fig. 5. Close-up of root cross-section with vascular tissue in the region of the asterisk (xylem and phloem not obvious). Scale bar = 50 mm. Figs 6 and 7. Basal portions of endogenous shoot pair (X/X¢) that have arisen from the root (R). Arrow points to disk-like holdfast as anchorage of shoot pair. Note distichous arrangement (1–3) of leaves that already have been shed. Scale bars = 500 mm. Fig. 8. Another root portion (R), with endogenously formed shoot. Only one (right side) shoot of the opposite pair is observable. Arrow points to disk-like holdfast. L = basal portion of filamentous leaf. Scale bar = 500 mm. SAXICOLELLA FROM GHANA 259 © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 Figures 9–17. Saxicolella submersa. Root architecture and endogenous shoot formation. (Hall & Bowling GC 38532). Fig. 9. Dorsal view of young root, with tip (asterisk) and an opposite pair of endogenous shoot buds (arrows). Scale bar = 500 mm. Figs 10 and 11. Lateral and dorsal view of root tip (same as shown in Fig. 9). The structure labelled by an asterisk may be interpreted as rudimentary root cap. Scale bars = 250 mm. Fig. 12. Dorsal view of root portion (R) with opposite pair of endogenous shoot buds (arrows), close-up of Fig. 9. Scale bar = 200 mm. Fig. 13. Lateral view of root portion (R) with endogenous shoot bud (root cortex ruptured). Note initial exogenous holdfast (Hx) associated with the location of the shoot bud. Scale bar = 200 mm. Figs 14 and 15. Two views of root (R) with endogenous shoot buds inside bumps of root cortex (arrows). Note outgrowing exogenous holdfast (Hx). Ventral root surface with adhesive hairs (T, most of them already dropped). Scale bars = 200 mm. Figs 16 and 17. Ventral views of two older root portions (R), with pairs of elongated fingerlike holdfasts (Hx/Hx¢) as exogenous outgrowths of the root flanks. Endogenous shoot buds with first leaves (L) protruding from cortex. Scale bars = 250 mm. 260 K. G. AMEKA ET AL. Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 SAXICOLELLA FROM GHANA 261 䉳 Figures 18–26. Saxicolella amicorum. Stems and leaves. (Ameka GC 113). Fig. 18. Distal shoot portion showing five leaves (1–5) which are distichously arranged. Arrows point to indistinct stipular lobes at leaf bases. Scale bar = 500 mm. Fig. 19. Close-up of leaf tip (same as shown in Figs 21 and 22). Scale bar = 100 mm. Fig. 20. Leaf insertion area (leaf 4 in Fig. 22). Arrow points to weak vascular bundle. Scale bar = 100 mm. Figs 21 and 22. Two views of the same shoot tip with three uppermost leaves (1–3). Arrow points to stipular appendage present only on one side of leaf 2, covering youngest visible leaf. Scale bars = 500 mm. Fig. 23. Cross-section of leaf. Note few narrow cells in vascular bundle position (arrow) and absence of silica bodies. Scale bar = 80 mm. Fig. 24. Cross-section of stem, with central vascular bundle and inconspicuous vascular branch (arrows). Note a few epidermal cells with silica bodies (asterisk). Scale bar = 100 mm. Figs 25 and 26. Close-ups of silica bodies in stem epidermis. Scale bars = 20 mm and 25 mm, respectively. SPATHELLAS AND arranged in clusters. The clusters are due to reduced internode length of the main axis between the short branches (Figs 46,47). As typical for all Podostemoideae each flower bud is totally enveloped by a membraneous non-vascularized cover which is called a spathella. The spathellas of Saxicolella are ellipsoidal to club-shaped and have a smooth surface (Figs 34–38, 42–48). Each spathella consists of 3–5 cell layers (Figs 40,41). The spathellas of S. submersa (length c. 3.5 mm) are bigger than those of S. amicorum (length c. 2.5 mm). Saxicolella flowers are erect in the spathella (Figs 49,61,62). In S. amicorum anthesis occurs when the spathella is slightly above the water surface and exposed to air. Shortly before anthesis the spathella splits irregularly at the tip (Figs 36–38). Unfortunately we could not observe the reproductive biology of S. submersa in the field. Hall (1972) reports that ‘the flowers of this species, unlike those of the majority of Podostemaceae, open below the surface of the water’. The specific name ‘submersa’ draws attention to Hall’s field observation which needs to be verified. In the isotype material of S. submersa we found only two flowers with a slightly dehisced spathella (Fig. 62). Most flowers were either still covered by the spathella (Fig. 61) or at fruiting stage (Fig. 71). TEPALS Saxicolella flowers have two (rarely one) linear tepals, inserted one on either side of the filament (Figs 40,50–52,63–65). They are shorter than the ovary and filament. Tepal lengths in both species varied from 0.4 to 1.2 mm. FLOWERS The flowers of Saxicolella are small, bisexual and zygomorphic. They consist of a single stamen, two inconspicuous tepals, and a superior ovary with two stigma lobes and many ovules. In S. amicorum the flowers are solitary and subsessile at the end of unbranched shoots. The flowers in S. submersa, however, are usually found on short reproductive branches which are produced by elongated stems. The terminal flowers of various S. submersa shoots were ANDROECIUM The androecium in Saxicolella consists of a single stamen with a filament and a two-lobed anther (Figs 50,61). We observed filament lengths up to 5 mm in both species. The anther length in both species is c. 1 mm. The introrse anthers are attached to the filament in a versatile position (Figs 54,66). Anther lobes consist of two pollen sacs each which open © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 Mature leaves in S. amicorum are 0.5–1.8 cm long and strap-like with a width of 0.5–0.8 mm. Saxicolella submersa leaves are 4–16 cm long with strongly elongate upper portions which are thin and thread-like (diameter 0.2–0.3 mm; Figs 31,32). The leaves are sometimes bifid in S. amicorum, with two elongate filaments arising from the leaf base (Figs 36,39). Trifid leaves in S. amicorum specimens, as rarely found by Hall (1972), were not observed by the authors. The leaf base is transversely flattened having a crescentshaped outline (Fig. 20). Higher up, the filamentous leaves are flattened in the median plane, similar to ensiform leaves of Acorus and Iris (Figs 21,22). Leaf cross-sections of both Saxicolella species show a weak central vascular bundle consisting of a few narrow cells only. The large parenchyma and epidermis cells contain chloroplasts. Silica bodies as found in stem and root are absent in the leaf (Fig. 23). Young filamentous leaves of both species may carry short-lived hairs along one side, as shown for S. submersa in Figure 33. The leaf tips are provided with somewhat papillate epidermal cells (Fig. 19). Stipular teeth or lobes are often present at the leaf bases in both species (Figs 18,21). The uppermost leaves of reproductive short shoots, at the base of the terminal flower, typically have two stipular teeth attached to the leaf base. They are more conspicuous in S. submersa (Figs 45,47) than in S. amicorum (Figs 35–39, see also figures in Hall, 1972). The stipular lobes of the basal and mid-level leaves are usually less prominent and may be absent on one side of the shoot (Figs 18,21,22). 262 K. G. AMEKA ET AL. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 Figures 27–33. Saxicolella submersa. Stems and leaves. (Hall & Bowling GC 38532) Fig. 27. Root portion (R), seen from above, with opposite pair of stems (X/X¢) and disk-like holdfast (Hx). Scale bar = 1 mm. Fig. 28. Another root portion (R) with pair of stems (X/X¢) and associated holdfasts (Hx/Hx¢) fused into one disk. Scale bar = 1 mm. Fig. 29. Stem crosssection. Arrow points to epidermis with thick cuticula. Some cortical cells have thick walls. Vascular tissue in stem centre with narrow cells, xylem and phloem not distinguishable. Scale bar = 100 mm. Fig. 30. Periphery of stem cross-section, showing silica bodies in epidermal cells. Scale bar = 30 mm. Figs 31 and 32. Ventral and dorsal view of mother root (R) with endogenous lateral root (Rn). Note pair of exogenous holdfasts (Hx) and short endogenous shoot (Xn) with uppermost leaf (L) continuing into filiform blade. Scale bars = 1 mm, 0.5 mm, respectively. Fig. 33. Filiform blade of mature leaf, covered with hairs along one sector. Scale bar = 330 mm. SAXICOLELLA FROM GHANA longitudinally at the stomium to release pollen. The pollen grains are tricolpate and arranged in dyads (Figs 55,67,68). GYNOECIUM CAPSULE AND SEEDS The nearly mature capsules of both species are narrow ellipsoidal or fusiform. They have the same shape and nearly the same size as the ovaries during anthesis. Capsule lengths were 1.6–2.9 mm in S. amicorum and 2.4–3.9 mm in S. submersa. The capsule of both Ghanaian Saxicolella species is shortly stalked, with a pedicel of 1–2 mm. In S. submersa there is a gynophore of up to 1 mm length (see also Hall, 1972). The dehiscing capsules consist of two equal or subequal persistent valves; each valve has three ribs and two marginal sutures (Figs 58,71). The seeds of both species are nearly ovoid, c. 0.3 mm long, brown to reddish-brown in colour and with reticulate markings on the surface (Figs 57,72). Two to 25 seeds per capsule occurred in S. amicorum whereas S. submersa capsules contained 13–41 seeds. The capsule is ribbed whereas the ovary is smooth. The appearance of capsule ribs is part of a decay process of the ovary wall. During anthesis the ovary wall consists of four cell layers and groups of thin fibre strands along eight sectors (Figs 41,59,60). The inner epidermal cells are transversally elongated whereas the inner hypodermal cells are longitudinally elongated. Only the inner two cell layers (becoming filled with a dark content) and the fibre strands persist at fruit maturity. The outer two layers, consisting of ± isodiametric cells, detach and fall during capsule development. DISCUSSION VEGETATIVE STRUCTURES Roots and holdfasts The prostrate roots of Podostemaceae fix the plants to the hard substratum by adhesive hairs and multicellular holdfasts (Rutishauser, 1997). Hall (1972), who described the two Ghanaian Saxicolella species, used the term ‘prostrate thallus’ instead of ‘root’. As done in earlier papers on Podostemaceae (see Rutishauser, 1997), we prefer the term ‘root’ for the creeping organs attached to the rock. This family shows an amazing diversity of root types. They all are dorsoventrally flattened and widened to some degree. They vary from thread-like (nearly cylindrical) to clearly ribbon-like and further to foliose (i.e. crustose and disk-like). In Saxicolella the roots are filiform or narrow ribbons (width less than 1 mm) in S. amicorum, S. laciniata and S. submersa, whereas foliose roots are found in S. flabellata, S. marginalis and S. nana (‘thalloide foliacée’ according to Cusset, 1987). Hall (1972; fig. 2/1) reported roots up to 3 mm broad for S. submersa. Our observations do not support this interpretation; we observed narrower (< 1 mm wide) roots. Root cap development and structure in Saxicolella and other Podostemaceae are largely rudimentary. The variation in root tip and cap structure of some American and Asian taxa has been demonstrated by Rutishauser (1997). For example, the root tip of Podostemum ceratophyllum from North America has a prominent but clearly asymmetrical cap, whereas Farmeria metzgerioides from southern India carries only a rudimentary root cap. Additional basal outgrowths, called holdfasts, stick the plants to the solid substratum. In many Podostemaceae the holdfasts are disk-like. Finger-like holdfasts, as described in S. submersa, are also known from Indotristicha ramosissima and Podostemum ceratophyllum (Rutishauser & Huber, 1991; Rutishauser, 1997). They can arise as exogenous outgrowths from the root flank (as typical for Podostemum and Saxicolella), or they can be formed from endogenous buds inside the root cortex (as typical for Indotristicha). Shoots and their position along roots The endogenous origin of shoots from roots, as observable in Saxicolella, seems to be typical for all Podostemaceae (Rutishauser & Huber, 1991; Ameka, 2000). Ribbon-like roots usually arise from the root flanks in opposite pairs as found in S. amicorum and S. submersa. Vegetative shoots are short and rosulate (a few millimeters high) in S. marginalis and S. nana (Engler, 1928; Cusset, 1987). They are well developed with elongated stems in S. amicorum (unbranched, up to 12 cm long), S. laciniata (rarely branched, up to 10 cm long), S. flabellata (branched, up to 20 cm long) and S. submersa (branched, up to 50 cm long). The reproductive shoots of the latter four species are often shorter than their vegetative shoots. There is axillary branching, at least in S. submersa, with lateral shoots arising in leaf axils. Axillary branching is typical for most angiosperms (Bell, 1991). © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 The gynoecium of both Saxicolella species consists of a shortly stalked ellipsoidal ovary and two linear stigmas (Figs 40,41,50–53,63,64). Inside the undehisced spathella the stigma lobes may be appressed to the ovary and even coiled to some degree (Figs 64,69). No distinct pollen receptive site on the stigma was observable. Stigma length varied from 0.5 mm to 1.5 mm in both S. amicorum and S. submersa. Placentation is axile (Fig. 70). The ovary has two equal or subequal locules separated by a thin septum (Figs 41,56,57,71). 263 264 K. G. AMEKA ET AL. Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 In many Podostemoideae, however, it was replaced by other branching types, especially stem bifurcation associated with double-sheathed leaves (dithecous) leaves. Double-sheathed leaves and stem bifurcation are correlated evolutionary novelties of many Podostemoideae, including the putatively basal taxa such as Apinagia, Marathrum and Mourera (see, e.g. Rutishauser & Grubert, 1994, 1999, 2000; Rutishauser, Novelo & Philbrick, 1999; Kita & Kato, 2001). Double-sheathed leaves and stem bifurcation may be seen as synapomorphies of the Podostemoideae (Rutishauser, 1997). Both features occur in some African taxa (e.g. Sphaerothylax abyssinica) and in a single Asian member (Zeylanidium subulatum, © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 SAXICOLELLA FROM GHANA 265 Figures 42–48. Saxicolella submersa. Reproductive shoots and spathellas. (Hall & Bowling GC 38532). Fig. 42. Dorsal view of root (R) with opposite pair of endogenous short shoots, right one reproductive, with terminal flower in spathella (Fc). Scale bar = 1 mm. Figs 43 and 44. Two views of elongated stem portion (X) with lateral short branch ending with terminal flower in spathella (Fc). Arrows point to scar of subtending leaf (dropped). Note distichous arrangement of leaves 1–5 along short branch. Scale bars = 1 mm. Fig. 45. Upper portion of reproductive branch with terminal flower in spathella (Fc). Note uppermost leaf with stipular tooth (arrow). Scale bar = 0.5 mm. Fig. 46. Reproductive shoot with stem (X) and four flowers in spathellas (Fc) at the end of branchlets. Filamentous leaves already dropped except for scale-like bases. Scale bar = 1 mm. Figs 47 and 48. Another reproductive shoot, seen from two sides, with three flowers in spathellas (Fc) at the end of branchlets. Note one of the uppermost leaves with stipular teeth (arrow). Scale bars = 1 mm. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 䉳 Figures 34–41. Saxicolella amicorum. Reproductive shoots with terminal flower in spathella. (Ameka GC 113). Fig. 34. Part of prostrate root (R) with two short lateral reproductive shoots (X/X¢). The right one has a terminal flower in unruptured spathella (Fc). Scale bar = 500 mm. Figs 35 and 36. Two views of another terminal flower enclosed in spathella (Fc) which is slightly split (asterisk). Arrows point to stipular appendages attached to leaf base. Leaves a–d below spathella with distichous phyllotaxis. Leaf b forked at base with two filamentous segments. Scale bar = 500 mm. Figs 37 and 38. Two views of another shoot tip with terminal spathella (Fc) ruptured and exposing the flower. Note uppermost four leaves a–d (tips removed) with attached stipular teeth. Scale bars = 500 mm. Fig. 39. Another reproductive shoot tip with spathella base (Fc). Uppermost leaves a–e with distichous phyllotaxis. Leaf d forked at base with two segments. Scale bar = 500 mm. Fig. 40. Cross-section through basal zone of spathella (Fc), covering flower bud with stamen filament (씹f), two tepals (P) and gynophore (씸s). Scale bar = 160 mm. Fig. 41. Cross-section through mid-level zone of spathella (Fc) and bilocular ovary. Arrows point to septae separating the two slightly unequal locules, each with several ovules. Scale bar = 250 mm. 266 K. G. AMEKA ET AL. Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 SAXICOLELLA FROM GHANA 267 syn. Podostemum subulatum) of this subfamily (Jäger-Zürn, 2000b, 2000c; Cook & Rutishauser, in press). Similar to all Asian Podostemoideae (except one) we could not find double-sheathed leaves in the two Saxicolella species from Ghana. The remaining Saxicolella species have yet to be studied in this respect. Molecular and cladistic analyses may show if the loss of double-sheathed leaves and (more rarely) the return to axillary branching are evolutionary reversals that happened more than once in the evolution of the non-American Podostemoideae. Leaves and stipules Simple (often linear) leaves are found in S. marginalis, S. nana and S. submersa. Simple, bifid (or rarely trifid) leaves with strap-like (narrowly lanceolate) segments are present in S. amicorum. More complex leaves occur in S. laciniata (laciniate with filiform ultimate segments) and S. flabellata (fan-shaped). Saxicolella submersa is the only member of the genus with filamentous leaves exceeding a length of 20 mm. Short-lived hairs, as occasionally observable along one leaf sector in S. submersa, can be found in many Podostemoideae (Rutishauser, 1997). Both Ghanaian Saxicolella species as well as S. marginalis can have stipules that are attached to the leaf base. The uppermost leaves below the terminal flower especially are each provided with two stipular teeth or lobes (Engler, 1928; Taylor, 1953; Cusset, 1987). Anatomical aspects: silica bodies and vascular tissue Silica bodies in peripheral cells of long-lived parts such as roots and stems are frequently found in Podostemaceae. Among the Podostemaceae in Ghana, silica bodies occur in S. amicorum, S. submersa and Tristicha trifaria but seem to be absent in Ledermanniella bowlingii (Ameka, 2000). The silica bodies have a protective function against mechanical injury and also prevent the plant from collapse during short periods of desiccation (Engler, 1928; Metcalfe & Chalk, 1950). According to Bezuidenhout (1964) they may also protect the plant against grazing animals. Since silica bodies of similar shape are present in most Podostemaceae there is little chance to use them as taxonomically valuable characters. The vascular tissue in the organs of S. amicorum and S. submersa is not well developed. The prosenchymatous cells often lack a clear differentiation into xylem and phloem. Ota, Imaichi & Kato (2001), while describing foliose Hydrobryum roots called these strands lacking obvious xylem and phloem elements ‘nonvascular strands’. Typical phloem elements were rarely identified in Podostemaceae (Romano & Dwyer, 1971; Uniyal & Mohan Ram, 2001) whereas xylem elements such as annular-thickened tracheids can be found more often, especially in bigger stems and leaf midribs of various members (Rutishauser & Grubert, 2000). REPRODUCTIVE STRUCTURES Anthesis All non-American Podostemoideae have inconspicuous flowers with one, two (or rarely three) stamens. These taxa are adapted to wind pollination and seem to be more derived than the neotropical genera, Apinagia, Marathrum and Mourera (Kita & Kato, 2001). Several species of these three genera have showy, multistaminate flowers adapted to insect pollination (Bezuidenhout, 1964; Grubert, 1974; Rutishauser & Grubert, 2000). Anthesis above the water surface and wind pollination seem to occur in Saxicolella amicorum but perhaps not in S. submersa. According to Hall (1972) the flowers in S. submersa ‘open under the surface of the water and flowers are pollinated by the current’. To suggest that these flowers are waterpollinated seems precocious until the time when © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 䉳 Figures 49–60. Saxicolella amicorum. Reproductive structures: flowers and fruits. (Ameka GC 113). Fig. 49. Flower bud after removal of spathella (Fc), with tepal (P), stamen (씹), gynoecium (씸). Arrow points to stipular lobe of uppermost leaf. Scale bar = 500 mm. Figs 50 and 51. Two views of flower in anthesis, with anther on long filament (씹f ), ovary with two thread-like stigma lobes. Note presence of single tepal (P) on one side of the filament base. Scale bars = 1 mm, 500 mm, respectively. Fig. 52. Another flower in anthesis, with two tepals (P = tepal). Scale bar = 500 mm. Fig. 53. Stigma lobes, close-up of Fig. 52. Scale bar = 250 mm. Fig. 54. Bipartite introrse anther, close-up of Fig. 50. Scale bar = 250 mm. Fig. 55. Dyad of tricolpate pollen. Scale bar = 10 mm. Fig. 56. Ovary after anthesis, artificially ruptured in order to show young seeds. Scale bar = 500 mm. Fig. 57. Ovary after anthesis, artificially ruptured, with septum (arrow) and ovules on fleshy placenta. Scale bar = 250 mm. Fig. 58. Capsule dehisced only along one suture (due to artifact after critical-point drying). Arrow points to suture which usually also dehisces. Each valve with three ribs (besides rib-like sutures). Scale bar = 250 mm. Figs 59 and 60. Cross-sections of sectors of ovary wall shortly after anthesis. Cells of inner epidermis (e) transversally elongated and with dark staining, cells of inner hypodermis (h) longitudinally elongated, surrounding cortical tissue consists of one layer of parenchyma cells below outer epidermis. Arrows point to rib positions, each one with few longitudinal fibre cells. Scale bars = 100 mm and 50 mm, respectively. 268 K. G. AMEKA ET AL. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 Figures 61–72. Saxicolella submersa. Reproductive structures: flowers and fruits. (Hall & Bowling GC 38532). Fig. 61. Young flower, after partial removal of spathella (Fc); with gynoecium (씸), stamen (씹), and tepal (P). Scale bar = 500 mm. Fig. 62. Flower emerging from ruptured spathella (Fc). Abbreviations as in Fig. 61. Scale bar = 500 mm. Figs 63 and 64. Two views of another flower prior to anthesis, after removal of spathella. Note the two tepals (P). Scale bars = 500 mm. Fig. 65. Needle-like tepal at base of filament (씹f) and slightly stalked ovary (씸). Scale bar = 330 mm. Fig. 66. Anther with introrse thecae. Scale bar = 330 mm. Figs 67 and 68. Dyads of tricolpate pollen, polar and equatorial views. Scale bars = 10 mm. Fig. 69. Close-up of preanthetic stigma lobes after removal of spathella. Scale bar = 330 mm. Fig. 70. Gynoecium of another flower bud, with ovary wall removed in order to show ovules. Arrow points to stigma lobes which are partly covered by the spathella (Fc). Scale bar = 500 mm. Fig. 71. Dehisced eight-ribbed capsule with two equal valves, each one with three ribs (besides rib-like sutures). Arrow points to placenta with septum and mature seeds. Note elongated capsule stalk (씸s). Scale bar = 1 mm. Fig. 72. Two mature seeds. Scale bar = 100 mm. SAXICOLELLA FROM GHANA additional data are available. It is more parsimonious to predict that these plants self-pollinate because selfpollination has evolved hundreds of times in extant angiosperms, including many aquatic members. In some oligostemonous Podostemoideae, self-pollination and even preanthesis cleistogamy within the unruptured spathella is more important than allogamy (e.g. in Podostemum ceratophyllum, Philbrick, 1984). Flower position along shoots and in spathella Saxicolella (Fig. 40; Cusset, 1987). The flowers and capsules of the Ghanaian Saxicolella species are subsessile within their spathellas. The pedicel (i.e. stalk below the spathella insertion), however, may elongate after anthesis up to 1–2 mm. Much longer pedicels (> 5 cm) are more common in New World Podostemoideae with prostrate stems and pedicel insertion close to the substratum (e.g. Marathrum spp., Rutishauser et al., 1999). Tepals and stamens African Podostemoideae genera usually have two subulate or filiform tepals as typical for Saxicolella. Only Stonesia is known to possess three tepals per flower, whereas two or three tepals are recorded for Thelethylax (Cook, 1996). Stamen number is variable in African genera such as Ledermanniella (with one, two or even three stamens), Macropodiella and Winklerella (with two or occasionally three stamens), whereas Letestuella has two or rarely one stamen per flower (Warming, 1899; Taylor, 1953; Cusset, 1987). Saxicolella flowers usually have a single stamen. Hall (1972) recorded one (or rarely two) stamens per flower in S. submersa. In the isotype material of S. submersa examined, however, we found only flowers with one stamen. There are other African genera such as Djinga and Sphaerothylax with uniformly unistaminate flowers (Cusset, 1987; Cook, 1996). Pollen Saxicolella has tricolpate dyads. Bezuidenhout (1964) and Lobreau-Callen, LeThomas & Suarez-Cervera (1998) described the pollen types and pollen wall ultrastructure of several podostemaceous genera including African and Madagascan genera. They recognized three main types: tricolpate pollen in monads or dyads in Podostemoideae, forate (= pantoporate, periporate) monads in Tristichoideae. Ledermanniella is the only genus showing both monads and dyads while all other Podostemoideae genera (including those outside Africa) have always either monads or dyads (Cook, 1996). In a few non-African Podostemoideae there are other types of pollen grains that are tetracolpate or pentacolpate (O’Neill, Osborn & Philbrick, 1997; Rutishauser, 1997). Ovary and capsule The length of filiform stigma lobes in Saxicolella varies from 0.5 to 2 mm. The present investigation shows that S. amicorum and S. submersa possess bilocular ovaries with a septum. Engler (1915, fig. 177E; 1928, fig. 39E) had shown bilocular ovaries in S. laciniata (syn. Pohliella laciniata). Other Saxicolella species such as S. flabellata and S. nana may © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 Flowers are either solitary in a terminal position (S. amicorum), or they occur in clusters, with one flower each at the end of short lateral branches (S. submersa). Flower clusters are also found in S. flabellata, S. laciniata and S. nana. Various inflorescences of African Podostemoideae show dense groups of flowers which are called here ‘clusters’ for lack of a better term. Their developmental morphologies are not fully understood. In Macropodiella macrothyrsa candelabrum-like clusters of up to 12 flowers are arranged as short shoots along the main shoots. Contrasting with Saxicolella inflorescences, the clusters in Macropodiella show double-sheathed bracts between neighbouring flowers and were interpreted as cymose inflorescences by Cusset (1978). According to JägerZürn (2000c) the flower clusters of Sphaerothylax abyssinica are a special kind of cyme that combines with congenital fusion (‘syndesmy’) of consecutive branch orders. More developmental studies are needed in order to show if Jäger-Zürn’s model is valid for other African Podostemoideae, although it does not fit for Saxicolella species. Flower buds of all Saxicolella members are erect in the spathella. Forty-seven percent of the Podostemoideae species in Africa and Madagascar have erect flower buds inside their spathellas (Ameka, 2000). This is in contrast to the inverted flower type in the spathella which is typical for all other African Podostemoideae, including genera such as Ledermanniella, Macropodiella and Stonesia. Inverted flower buds are a unique feature (evolutionary novelty, synapomorphy) of several African and Madagascan Podostemoideae whereas erect flower buds are plesiomorphic because they are typical for all podostemoid members outside Africa and Madagascar including the putatively basal genera of the subfamily (Kita & Kato, 2001). Various Podostemoideae are characterized by a stalked ovary (gynophore). African taxa especially with inverted flower buds in the unruptured spathella show a gynophore: a stalk which separates the ovary from the insertion level of androecium and perianth (e.g. Zehnderia with a gynophore up to 8 mm long; Cusset, 1987). Short gynophores, up to 1 mm long, are found in some African taxa with erect flower buds, e.g. 269 270 K. G. AMEKA ET AL. Ovules and seeds Capsule lengths of c. 2–3 mm and seed numbers of 2–40 per capsule as observed in the two Ghanaian Saxicolella species are found in many podostemoid genera (Philbrick & Novelo, 1997). The number of seeds in Podostemaceae capsules varies from 2 000 to 2 400 in Mourera fluviatilis from South America, to one (or rarely two) in Farmeria metzgerioides from southern Asia (Rutishauser & Grubert, 1994). The seeds of most Podostemaceae have nearly the same size as the ovules; they are small (0.1–0.3 mm long) and predictably dispersed by wind or water. In Polypleurum stylosum there are 1 200 000 seeds per gram and in Griffithella hookeriana 700 000 seeds per gram (Khosla & Mohan Ram, 1993). Similar seed weights seem to occur in Saxicolella (Ameka, 2000). Ornithochory is another possibility for seed dispersal. The sticky seed coat (myxospermy) suggests that the seeds could adhere to the feet of birds walking over the exposed rocks (Philbrick, 1984). Seeds can remain viable for up to 18 months when stored dry (Vidyashankari, 1988; Philbrick & Novelo, 1997). These observations need to be verified for Saxicolella. SAXICOLELLA AS COMPARED WITH THE ASIAN GENUS POLYPLEURUM When Hall (1972) described Saxicolella submersa first as Polypleurum submersum he wrote: ‘It is astonishing that this species should have been discovered at such a great distance from its nearest known relatives.’ According to Hall it resembled most closely the southern Asian species Polypleurum elongatum (Gardner) J.B.Hall. Characters that Polypleurum and Saxicolella have in common Roots with exogenous finger- or disk-like holdfasts occur in both genera. The leaves are entire and linear. This is always so in Polypleurum, but in Saxicolella there is variation depending on the species and growth stage. In both Polypleurum and Saxicolella the flower is in an erect position. The ovary is ellipsoidal to fusiform with two linear stigmas. The capsule of both Polypleurum and Saxicolella is ribbed, opens usually by two equal valves and each valve has three ribs and two rib-like marginal sutures. Characters distinguishing Polypleurum and Saxicolella Clearly in Podostemaceae, at least until now, the genus concept is highly artificial (Cook & Rutishauser, 2001). Nevertheless, we are convinced that Saxicolella submersa does not belong in the genus Polypleurum. Elongated floating structures exist in certain species of both genera. They are, however, roots in Polypleurum and shoots in Saxicolella. The elongated floating structures, up to 50 cm in P. elongatum, are slightly flattened roots without exogenous leaves, i.e. plant structures with only endogenous lateral shoots (including leaves and flowers), as typical for other southern Asian Polypleurum species (Mathew & © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 lack the septum and, thus, have unilocular ovaries, at least during and after anthesis. This may have been the reason that Cusset (1987) segregated the obviously bilocular species S. amicorum and S. submersa in the provisional genus Aulea which was never officially published (see Lebrun & Stork, 1991). In our view locule number alone should not be a reason for creating a new genus for S. amicorum and S. submersa. Developmental studies in all Saxicolella species and other African Podostemoideae with seemingly unilocular ovaries will probably show that the septum stops growth early in the basically bilocular ovary, giving rise to a secondarily unilocular ovary with a seemingly free central placenta during further expansion. This type of secondarily unilocular ovary is known from other angiosperms such as the Caryophyllaceae (Weberling, 1989). The ovary of many Podostemoideae is bilocular, with a prominent central placenta and a thin septum. Unlike Cusset (1972, 1987, 1992) who placed emphasis on the number of loculi, we do not view the presence or absence of the septum as an important taxonomic character. It is often difficult or impossible, without careful microtome sections of young flowerbuds, to decide whether the ovary has one or two loculi (Taylor, 1953). For example, based on microtome sections Jäger-Zürn (2000c) has shown that the gynoecium of Sphaerothylax abyssinica consists of a bilocular ovary (not unilocular as noted by Cusset, 1972). Capsule morphology was traditionally used to classify the subfamily Podostemoideae (Willis, 1902). The mature capsules have nearly the same size as the ovaries during anthesis. In Saxicolella narrow ribs (usually eight per capsule) appear during fruit maturation because the outer cortical layers of the ovary wall are shed. This decay pattern is found in many Podostemaceae with ribbed mature capsules (Rutishauser & Pfeifer, in press). Similarly the pedicel (after slight elongation) loses its outer mainly parenchymatous layers. The capsules of Saxicolella dehisce with two equal or subequal valves, each one persistent and provided with three ribs between the two rib-like sutures. Because Saxicolella capsules are normally described as being isolobous (with two equal valves), the slightly unequal valves found in S. amicorum need further inspection. SAXICOLELLA FROM GHANA Characters distinguishing Saxicolella amicorum and S. submersa Vegetative shoots are up to 12 cm long and not branched in S. amicorum, whereas they are up to 50 cm long and branched in S. submersa. The leaves in S. amicorum are simple or bifid (or rarely trifid) with strap-like segments up to 1.8 cm long. Leaves in S. submersa are simple, linear and filamentous, with a length up to 16 cm. Reproductive shoots of S. amicorum are always short and provided with a single terminal flower whereas S. submersa can (besides short one-flowered stems) also produce branched reproductive shoots with flower clusters. Other characters such as presence vs. absence of a root cap, or presence vs. absence of short-lived hairs along the filamentous leaf segments seem to be less reliable for the distinction of the two species. ACKNOWLEDGEMENTS We thank M. Cheek (Kew), C.T. Philbrick (Danbury CT) for valuable comments on the manuscript. The first author thanks K.A.A. de Graft-Johnson (Water Research Institutes Accra) and J.K. Adomako (Botany Department, University of Ghana, Legon) for their kind and excellent assistance during trips in search of rheophytes in Ghanaian rivers. The first author also thanks for the kind hospitality of the family of B. Isler Rutishauser while he was in Zurich to work on the plates for this paper. Technical assistance (scanning electron microscopy) of U. Jauch (Institut für Pflanzenbiologie der Universität Zürich) is gratefully acknowledged. This paper is part of a research project supported by the Swiss National Science Foundation (grant No.31.63748) to the third author. REFERENCES Ameka GK. 2000. The biology, taxonomy and ecology of the Podostemaceae in Ghana. Unpublished PhD Thesis. Department of Botany, University of Ghana, Legon. Ameka GK, Adomako J, De Graft-Johnson KAA, Cheek M, Swaine M. 1994. Rheophytes of Ghana. In: Van der Maesen, LJG et al., eds. The biodiversity of African plants. Dordrecht, The Netherlands: Kluwer Academic Publishers, 780–782. Bell AD. 1991. Plant form. An illustrated guide to flowering plant morphology. Oxford: Oxford University Press. Bezuidenhout A. 1964. The pollen of the African Podostemaceae. Pollen et Spores 6: 463–478. Cheek M, Onana J, Pollard P. 2000. The plants of Mount Oku and the Ijim Ridge. Kew, London: Royal Botanic Gardens. Cook CDK. 1996. Aquatic plant book. 2nd Revised Edition. The Hague: SPB. Academic Publishing. Cook CDK. 1999. The number and kinds of embryobearing plants which have become aquatic: a survey. Perspectives in Plant Ecology, Evolution and Systematics 2: 79–102. Cook CDK, Rutishauser R. 2001. Name changes in the Podostemaceae. Taxon 50: 2063–2067. Cook CDK, Rutishauser R. in press. Podostemaceae. In: Kubitzki K, ed. Families and genera of vascular plants. Berlin: Springer. Cusset C. 1972. Les Podostemaceae de Madagascar. Adansonia Sér. 2 12(4): 557–568. (published 1973) Cusset C. 1978. Contribution à l’étude des Podostemaceae. 5. Le genre Macropodiella Engl. Adansonia Sér. 2 17(3): 293–303. Cusset C. 1987. Podostemaceae and Tristichaceae. In: Satabié B, Morat PH, eds. Flore du Cameroun. 30: 51–99. Yaounde: Ministère de l’Enseignement Superieur et de la Recherche Scientifique. Cusset C. 1992. Contribution à l’étude des Podostemaceae. 12. Les genres asiatiques. Bulletin du Museum National d’Histoire Naturelle, Paris, Série 4, (Section B, Adansonia, no. 1) 14: 13–54. Cusset G, Cusset C. 1988. Études sur les Podostemales. 10. Structures florales et végétatives des Tristichaceae. Bulletin du Museum National d’Histoire Naturelle, Paris, Série 4, (Section B, Adansonia, no. 2) 10: 179–218. Engler A. 1915. Die Pflanzenwelt Afrikas. Leipzig: W. Engelmann. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 Satheesh, 1997). In S. submersa (as typical for other Saxicolella spp.) the prominent floating structures (up to 50 cm long) are shoots, i.e. plant structures with distichously arranged, exogenous leaves and axillary, exogenous branches. The root-borne shoots in Polypleurum are always short and rosulate whereas the shoots in Saxicolella are elongated, except for S. marginalis and S. nana which have short shoots arising directly from the root. The Saxicolella leaves, especially the uppermost leaves just below the terminal flower, are provided with two lateral stipules. These lateral stipules are lacking in Polypleurum. Two stamens per flower, united into an andropodium, usually occur in Polypleurum. Polypleurum schmidtianum (syn. Polypleurella schmidtiana) is the only exception having one stamen per flower (Cusset, 1992). In Saxicolella (including S. submersa) one stamen per flower is the rule. Hall (1972), however, mentioned that S. submersa rarely has two stamens per flower. Kita & Kato (2001) inferred the phylogeny of the Podostemoideae from nucleotide sequences of the chloroplast matK gene. They found that all Asian Podostemoideae taxa studied form a monophyletic group (with Polypleurum being part of a subclade with Zeylanidium). The two taxa (Endocaulos, Thelethylax) studied hitherto from Madagascar are a sister clade to all Asian Podostemoideae. Molecular data of Saxicolella and all other African genera are not yet available. 271 272 K. G. AMEKA ET AL. of the Podostemaceae in Kerala, India. Aquatic Botany 57: 243–274. Metcalfe CR, Chalk L. 1950. Anatomy of the dicotyledons, Vol. 2. Oxford: Oxford University Press. Mohan Ram HY, Sehgal A. 1992. Podostemaceae – the strange family of aquatic angiosperms. Palaeobotanist 41: 192–197. Mohan Ram HY, Sehgal A. 1997. In vitro studies on developmental morphology of Indian Podostemaceae. Aquatic Botany 57: 97–132. O’Neill SP, Osborn JM, Philbrick CT. 1997. Comparative pollen morphology of five New World genera of Podostemaceae. Aquatic Botany 57: 133–150. Ota M, Imaichi R, Kato M. 2001. Developmental morphology of the thalloid Hydrobryum japonicum (Podostemaceae). American Journal of Botany 88: 382–390. Philbrick CT. 1984. Aspects of floral biology, breeding system, and seed and seedling biology in Podostemum ceratophyllum (Podostemaceae). Systematic Botany 9(2): 166–174. Philbrick CT, Novelo RA. 1995. New World Podostemaceae: Ecological and evolutionary enigmas. Brittonia 47: 210– 222. Philbrick CT, Novelo RA. 1997. Ovule number, seed number and seed size in Mexican and North American species of Podostemaceae. Aquatic Botany 57: 183–200. Romano GR, Dwyer JD. 1971. A demonstration of phloem in the Podostemaceae. Bulletin of the Torrey Botanical Club 98 (1): 46–53. van Royen P. 1951. The Podostemaceae of the New World. Part I. Mededeelingen van hat Botanisch Museum en Herbarium van de Rijks Universiteit te Utrecht 107: 1–151. van Royen P. 1953. The Podostemaceae of the New World II. Acta Botanica Neerlandica 2 (1): 1–21. van Royen P. 1954. The Podostemaceae of the New World III. Acta Botanica Neerlandica 3 (2): 215–263. Rutishauser R. 1995. Developmental patterns of leaves in Podostemaceae compared with more typical flowering plants: saltational evolution and fuzzy morphology. Canadian Journal of Botany 73 (9): 1305–1317. Rutishauser R. 1997. Structural and developmental diversity in Podostemaceae (river-weeds). Aquatic Botany 57: 29–70. Rutishauser R, Grubert M. 1994. The architecture of Mourera fluviatilis (Podostemaceae). Botanica Helvetica 104: 179–194. Rutishauser R, Grubert M. 1999. The architecture of Mourera fluviatilis (Podostemaceae): developmental morphology of inflorescences, flowers and seedlings. American Journal of Botany 86: 907–922. Rutishauser R, Grubert M. 2000. Developmental morphology of Apinagia multibranchiata (Podostemaceae) from the Venezuelan Guyanas. Botanical Journal of the Linnean Society 132: 299–323. Rutishauser R, Huber KA. 1991. The developmental morphology of Indotristicha ramosissima (Podostemaceae, Tristichoideae). Plant Systematics and Evolution 178: 195– 223. Rutishauser R, Novelo RA, Philbrick CT. 1999. Develop- © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 Engler A. 1926. Podostemonaceae Africanae IV. Botanische Jahrbücher für Systematik. Pflanzengeschichte und Pflanzengeographie 60: 451–467. Engler A. 1928. Reihe Podostemales. In: Engler A, Prantl K, eds. Die Natürlichen Pflanzenfamilien 18a: 1–68. 483–484 (Leipzig: W. Engelmann; published as Volume in 1930). Grubert M. 1974. Podostemaceen-Studien. Teil 1. Zur Ökologie einiger venezolanischer Podostemaceen. Beiträge zur Biologie der Pflanzen 50: 321–391. Hall JB. 1972. New Podostemaceae from Ghana with notes on related species. Kew Bulletin 26: 123–136. Igersheim A. 1993. The character states of the Caribbean monotypic Strumpfia (Rubiaceae). Nordic Journal of Botany 13: 545–559. Igersheim A, Cichocki O. 1996. A simple method for microtome sectioning of prehistoric charcoal specimens embedded in 2-hydroxyethyl methacrylate (HEMA). Review of Palaeobotany and Palynology 92: 389–393. Imaichi R, Ichiba T, Kato M. 1999. Developmental morphology and anatomy of the vegetative organs in Malaccotristicha malayana (Podostemaceae). International Journal of Plant Sciences 160(2): 253–259. Jäger-Zürn I. 1997. Comparative morphology of the vegetative structures of Tristicha trifaria, Indotristicha ramosissima and Dalzellia ceylanica (Podostemaceae, Tristichoideae): a review. Aquatic Botany 57: 71–96. Jäger-Zürn I. 2000a. Crustose root and root-borne shoots of Zeylanidium olivaceum (Podostemaceae – Podostemoideae). Part VI of the series ‘Morphology of Podostemaceae’. Flora 195: 61–82. Jäger-Zürn I. 2000b. Developmental morphology of roots and root-borne shoots of Podostemum subulatum as compared with Zeylanidium olivaceum (PodostemaceaePodostemoideae). Part VII of the series ‘Morphology of Podostemaceae’. Plant Systematics and Evolution 220: 55–67. Jäger-Zürn I. 2000c. The unusual ramification mode of Sphaerothylax abyssinica (Wedd.) Warm. (Podostemaceae – Podostemoideae). Flora 195: 200–227. Jäger-Zürn I, Grubert M. 2000. Podostemaceae depend on sticky biofilms with respect to attachment to rocks in waterfalls. International Journal of Plant Science 161: 599–607. Khosla C, Mohan Ram HY. 1993. Morphology of flower, fruit and seed in Polypleurum stylosum. Aquatic Botany 46: 255–262. Kita Y, Kato M. 2001. Infrafamilial phylogeny of the aquatic angiosperm Podostemaceae inferred from the nucleotide sequence of the matK gene. Plant Biology 3: 156–163. Lebrun JP, Stork AL. 1991. Enumeration des plantes à pleurs d’Afrique tropicale. 1. Généralités et Annonaceae à Pandaceae. Genève: Conservatoire et Jardin botaniques de Genève. Lobreau-Callen D, LeThomas A, Suarez-Cervera M. 1998. Ultrastructural characters of the pollen of some Podostemales. Affinities with advanced Rosidae [in French]. Comptes Rendues de l’Academie des Sciences, Série III 321: 335–345. Mathew CJ, Satheesh VK. 1997. Taxonomy and distribution SAXICOLELLA FROM GHANA the Flora of West Tropical Africa. Bulletin of the British Museum, Botany 1: 53–79. Uniyal PL, Mohan Ram HY. 2001. Studies on the morphology and in vitro seed germination in Willisia selaginoides (Bedd.) Warm. ex Willis (Podostemaceae). Flora 196: 370–380. Vidyashankari B. 1988. Seed germination and seedling morphology in Indotristicha ramosissima (Podostemaceae) grown in vitro. Current Science 57 (7): 369–373. Warming E. 1899. Familien Podostemaceae. V. Det Kongelige Danske Videnskabernes Selskabs Naturvidenskabelige og Mathematiske Afhandlinger (Copenhagen) 9: 105–154. Weber M, Igersheim A. 1994. ‘Pollen buds’ in Ophiorrhiza (Rubiaceae) and their role in Pollenkitt release. Botanica Acta 107: 257–262. Weberling F. 1989. Morphology of flowers and inflorescences. Cambridge: Cambridge University Press. Willis JC. 1902. A revision of the Podostemaceae of India and Ceylon. Annals of the Royal Botanic Gardens, Peradeniya 1: 181–250. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 255–273 Downloaded from https://academic.oup.com/botlinnean/article/139/3/255/2433627 by guest on 08 June 2022 mental morphology of New World Podostemaceae: Marathrum and Vanroyenella. International Journal of Plant Sciences 160 (1): 29–45. Rutishauser R, Pfeifer E. in press. Comparative morphology of Cladopus (including Torrenticola, Podostemaceae) from E Asia to NE Australia. Australian Journal of Botany in press. Schnell R. 1967. Études sur l’anatomie et la morphologie des Podostémacées. Candollea 22: 157–225. Schnell R. 1994. Les stratégies végétales. Essai de morphologie évolutive. Paris: Masson. Sculthorpe CD. 1967. The biology of aquatic vascular plants. London: Edward Arnold. Sehgal A, Mohan Ram HY, Bhatt JR. 1993. In vitro germination, growth, morphogenesis and flowering of an aquatic angiosperm, Polypleurum stylosum (Podostemaceae). Aquatic Botany 45: 269–283. van Steenis CGGJ. 1981. Rheophytes of the world. Alphen aan den Rijn: Sijthoff and Noordhoff. Taylor G. 1953. Notes on Podostemaceae for the revision of 273