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2Institut für Systematische Botanik der Universität Zürich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland; and 3Institut für Pharmazie der Johannes Gutenberg-Universität Mainz, Saarstrasse 21, D-55099 Mainz, Germany
Received for publication April 2, 1998. Accepted for publication November 30, 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: basipetal bract inception • inflorescence • morphogenesis • Mourera fluviatilis • Podostemaceae • polystemonous flowers • seedling morphology • terminal leaf • water plants
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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... the appearance of the flowering plant in the rapids is fascinating, but so strange that there will scarcely be found a formation on earth which can be compared with it.(Went, 1929)
Mourera fluviatialis Aublet occurs in a relatively large area in northeastern South America: southeastern Venezuela, Guyana, Surinam, French Guiana, and northern Brazil (van Royen, 1953
; Velasquez, 1994
). It seems that Mourera fluviatilis is less seasonal in its flowering period than most other Podostemaceae. Flowering and fruiting individuals are found nearly throughout the year: from (May to) August to November in Guyana and Surinam, from July to February in northern Brazil (van Royen, 1953
). Grubert (1974)
observed flowering and fruiting plants of M. fluviatilis in the Rio Caroní (Venezuela) from October to January, i.e., in the first 4 mo of the dry period that normally lasts until March. The short stem and the cabbage-like leaves of the adult plant are fixed to the rock by claw-shaped holdfasts (Went, 1926
, 1929
). Roots with endogenous daughter shoots have not been observed in M. fluviatilis.
Investigations on M. fluviatilis go back more than 220 yr. Aublet (1775)
described it as the first species of what later became the family Podostemaceae. Since then many studies have been published on the taxonomy, morphology and ecology of this spectacular member of the Podostemaceae (e.g., Tulasne, 1852
, 1852–1853
; Warming, 1888
, 1890
, 1899
; Matthiesen, 1908
; Went, 1910
, 1926
; Engler, 1930
; van Royen, 1953
; Schnell, 1967
, 1969
, 1998
; Grubert, 1974
, 1975
, 1976
, 1991
; de Granville, 1977
). Important results from earlier publications on Mourera are summarized here. This paper complements those of Rutishauser and Grubert (1994) as well as Rutishauser (1995)
where the vegetative architecture was described with special emphasis on foliage leaves. This study focuses on the development of the inflorescences, flowers, and seedlings of M. fluviatilis. Various structural idiosyncrasies will be described: e.g., double-sheathed (dithecous) leaves and bracts, which are not known in angiosperms except for Podostemaceae; raceme-like inflorescence with terminal leaf and basipetal bract inception; polystemonous flowers with introrse and extrorse anthers. Mourera is thought to be a primitive genus within Podostemaceae (Schnell, 1969
, 1994
). The molecular data and cladograms presented by Les, Philbrick, and Novelo (1997
, 1998) seem to verify Schnell's hypothesis. Thus, a better knowledge of the developmental morphologies of M. fluviatilis and allies is needed for phylogenetic reconstruction of the family.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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20 km south of San Félix (October 1972–March 1973). Ecological data from the site and phenological aspects of the life cycle of M. fluviatilis are described by Pannier (1960)
, Gessner and Hammer (1962)
, Grubert (1970
, 1974
, 1975
, 1976
) and Schnell (1998)
. During the last two decades the collection site at the lower Rio Caroní has been destroyed to a considerable degree due to hydroelectric power plants and industrial pollution (Grubert, 1991
). The material used for this study was fixed and preserved in ethyl alcohol (70%). For scanning electron microscopy the dissected specimens were critical-point dried and sputter-coated (Au-Pd). A few specimens were cut with a razor-blade prior to critical-point drying. The micrographs were taken with a Cambridge S4 scanning electron microscope. Voucher specimens (pressed and liquid fixed) are housed at MZ (Mainz) and Z (Zürich).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The raceme-like inflorescences are in anthesis when the basal vegetative parts with the cabbage-like leaves remain submerged in as much as 35 cm of water. Elongate peduncles keep the flowers well above the water level (Figs. 1, 3). However, in rivers that have a dry season, M. fluviatilis is annual with shorter leaves and smaller inflorescences. Grubert (1974)
found dwarf plants in shallow water. They had a mean leaf length of 11.6 cm and mean inflorescence length of 15.4 cm. The plants may continue to flower and fruit until the rocky substrate is already slightly above water level. Vigorous plants may produce up to 11 inflorescences arising one by one from a short stem. Inflorescences have 40–90 flowers along the two flanks of their flattened axis (Fig. 2; Rutishauser and Grubert, 1994
). When the inflorescence presents the first (= most distal) flowers, inflorescence axis and peduncle normally have not yet reached their mature size. They may add several centimetres in length until the most proximal flowers are in anthesis.
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25% are scattered in the central cylinder and 75% in the cortex (Fig. 11: black arrows; Mildbraed, 1904
). The upper portion of the peduncle becomes the inflorescence axis. The number of scattered vascular bundles is gradually reduced in the inflorescence axis while moving from the most proximal to the most distal flower. The central cylinder also contains laticiferous tubes (Fig. 12: white arrows). Thus, milky sap extrudes from the fresh peduncle when it is cut (Grubert, 1974
; see Steude [1935]
for similar observations in M. aspera). The peripheral zone of the peduncle consists of chlorenchymatous multicellular warts (diameter 100–500 µm, Fig. 11: white arrows). Vascular bundles supply the warts. Similar warts also cover the inflorescence axis (Fig. 20), the bracts (Fig. 28), and the upper surface of the foliage leaves (see below).
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; Rutishauser, 1995
). Most foliage leaves prior to inflorescence formation possess a single sheath with two wings, which wrap around younger leaves or a primordial inflorescence. Such monothecous (single-sheathed) leaves are shown in Figs. 4–5 (e.g., leaf II), Fig. 6 (leaf IV), and Fig. 9 (leaf L). The tip and marginal lobes of the young leaf blades are coiled towards the upper side. The outer (= abaxial) leaf margin (arrows in Figs. 6, 9) continues to grow basipetally clearly below the inner (= adaxial) leaf insertion area. Thus, the leaf insertion area becomes asymmetrical (Rutishauser and Grubert, 1994
). Initiation of the inflorescences at the tip of the prostrate stem is correlated with the formation of a few foliage leaves that are dithecous (double-sheathed). A typical situation is illustrated in Figs. 4–5. All leaves (either monothecous or dithecous) are arranged in the same plane as the two young inflorescences (J1/J2). Leaves I/II/IV and V are monothecous, whereas the central leaf III is dithecous. Thus, inflorescence J1 is positioned in the gap between leaves II and III. Initiation of new leaves (IV/V) and a new inflorescence (J2) is repeated in the gap between the leaves I and III.
An early developmental stage of a dithecous foliage leaf (Lx in Figs. 13–14) shows its position next to a primordial inflorescence (J). The lower (= ventral) wings (lW/lW') of the two sheaths are confluent with the primordial blade margin. The upper (= dorsal) sheath wings (uW/uW') are initiated as separate bulges. The right sheath, consisting of the wings uW and lW (Fig. 13), faces the primordial inflorescence (J), whereas the left sheath with the wings lW' and uW' (Fig. 14) is occupied by a new leaf primordium (Lx + 1).
A young dithecous leaf (L) with coiled blade lobes is illustrated in Fig. 19. Only the upper wings (uW/uW') of both sheaths are observable from above. The sheaths are quite unequal, associated with an asymmetrical insertion of the dithecous leaf (L). The bigger sheath with its upper wing (uW) faces towards a young and curved inflorescence (J), whereas the smaller sheath with ist upper wing (uW') encloses a new foliage leaf (black arrow in Figs. 19–20).
Dorsiventral symmetry and early development of inflorescences including terminal bract
The inflorescence leaves are called bracts because their blade is much shorter, or lacking, as compared to foliage leaves. Inflorescences of M. fluviatilis have a terminal bract with a blade of 2 cm length or more (Figs. 3–4, 22: tB). The young inflorescence is slightly dorsiventral due to its horizontal to ascending position at the tip of the prostrate stem. In developing inflorescences there are some differences between the lower (= ventral) side that originally faces the rock and the upper (= dorsal) side. For example, the terminal bract of young inflorescences is coiled towards the upper side (Figs. 7–8: tB). It is also the upper side of the prostrate stem towards which the margins of the adjacent foliage leaves are coiled (Fig. 6: black arrows). An inflorescence of Mourera fluviatilis starts development in horizontal position and turns up afterwards. This negative geotropism was shown by the following experiment. When a still young but already nearly vertical inflorescence is layed down into horizontal position, it turns up again to vertical position (Schnell, 1967
, 1998
; Grubert, 1974
).
A developing inflorescence first forms the terminal bract, which is provided with a primordial blade (tB in Figs. 9, 15–18). The terminal bract is dithecous, with two sheaths in lateral positions. Due to the horizontal position of the young inflorescence (Fig. 22), both sheaths of the terminal bract each consist of an upper (uW/uW') and a lower wing (lW/lW') (Figs. 16–18, 24). Only the lower sheath wings are confluent with the blade margins, similar to those of the foliage leaves (Figs. 13–14).
Basipetal initiation and morphology of lateral inflorescence bracts
The lateral bracts of the inflorescence are arranged in two rows along the flanks. The bracts are peculiar with respect to their order of initiation. Following the inception of the terminal bract, all lateral bracts are initiated in a basipetal order along the two inflorescence flanks (Figs. 22–23). In Fig. 17 the young inflorescence is seen from the upper side, with three lateral bracts (B1 > B2 > B3) on the right side and three lateral bracts (B1' > B2' > B3') on the left side of the terminal bract (tB). The basipetal bract inception continues until there are 20–45 bracts per row. A later stage of inflorescence development shows the region of the youngest (= most proximal) bracts along one flank. Four of them are labeled according to their initiation order (Fig. 21: B20–B23). The more distal region of such a young inflorescence is already densely covered with warts (Figs. 19–20).
All lateral bracts are dithecous and 5–13 mm long (Figs. 27–29). Contrasting with the terminal bract they have only a rudimentary blade; either a small lobe, which is coiled upward during development (Fig. 28: *), or a crest (Fig. 25: *). The bract blades, if prominent, are laterally flattened (ensiform), i.e., the blades are oriented in the plane that is defined by the lance-shaped inflorescence (Rutishauser and Grubert, 1994
). The two sheaths of all lateral bracts can be labeled as distal (d) and proximal (p) because they are oriented towards the inflorescence tip and base, respectively. The left and right wings of each sheath may be labeled as upper (u) and a lower one (l), when we refer to the young inflorescence that is horizontal or ascending (Figs. 22–23). Combining the four wing positions (d/p and u/l), the distal sheath of a lateral bract consists of a distal upper wing (duW) and a distal lower wing (dlW), whereas the proximal sheath of a lateral bract consists of a proximal upper wing (puW) and a proximal lower wing (plW; Figs. 25–29). The wings of the distal sheath have a smooth margin or nearly so, whereas the wings of the proximal sheath have a fringed margin. Adjacent sheaths of neighboring bracts overlap each other as follows (Fig, 30): The proximal sheath wings (puW/plW) of the more distal bract partially enclose the distal sheath wings (duW/dlW) of the more proximal bract.
Arrangement and initiation of flowers and spathellas
All flowers of an inflorescence are inserted in the same two rows as the bracts (Figs. 22–23, 30). Each gap between two adjacent bracts is occupied by a single flower (F). The flowers of an inflorescence are initiated clearly after the inception of the neighboring bracts (Figs. 21, 31). Contrasting with typical cymose inflorescences of angiosperms there is a terminal leaf (tB) and not a terminal flower at the end of the young inflorescence (Fig. 17). All flowers between the bracts repeat the basipetal initiation order of the bracts. They develop and open in a basipetal order (Fig. 2).
Each flower is protected by a tubular cover (spathella), as is typical for the subfamily Podostemoideae (Rutishauser, 1997
). The spathella of Mourera fluviatilis arises as a two-lobed collar resembling two connate prophylls (Sp in Figs. 32–34). The spathella consists of about three cell layers and lacks vascularization (Fig. 35).
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).
Development of fruits and seeds
The most distal flowers (dF) of an inflorescence (Fig. 2) may have developed into nearly ripe capsules (with stamens and tepals shed) when the mid-level and the more proximal flowers (pF) are in anthesis or still in bud stage. About 4 d after anthesis the green ovary turns brown and develops six or eight ribs (Grubert, 1974
). This happens due to shedding of the peripheral parenchymatous layers of the ovary wall except the six (= 2 x 3) sclerenchymatous vascular bundles and the two suture margins (similar to other Podostemoideae; Rutishauser, 1997
). The ripe capsule (length 5–13 mm, diameter 2–3 mm) has nearly the same length as the ovary during anthesis. There are 2400 ovules per flower, arranged in two locules and separated by a thin septum (Fig. 41; Rutishauser and Grubert, 1994
). Most ovules have the potential to develop into seeds. Thus, a vigorous plant with five inflorescences and a mean of 85 ripe capsules per inflorescence may produce up to one million seeds. The period from anthesis until seed dispersal lasts 24–30 d. During this time the inflorescence sheds its bracts and outer parenchymatous layers of the axis and peduncle. Thus, only the sclerenchymatous and lignified central cylinder remains. Ripe capsules dehisce by two equal and persistent valves, each with three ribs. The tiny seeds are wind dispersed, at least up to 3–4 m according to field experiments (Grubert, 1974
; Schnell, 1998
).
Seedling growth
Once the seed gets wet its outer testa forms a mucilage that sticks to the rock (Gessner and Hammer, 1962
; Grubert, 1970
, 1974
, 1976
). Seedlings of M. fluviatilis show two entire threadlike cotyledons (Figs. 42–44, 55), followed by entire or forked filamentous leaves, which arise from the plumular pole (Figs. 45–53). Seedling leaves possess only one tiny vascular bundle inside the filamentous segments (Fig. 54). The base of the seedling leaves may or may not be provided with sheath lobes (Fig. 56: arrows). An obvious shoot meristem is not observable. A new seedling leaf (IV in Figs. 57–58) is initiated in a lateral position from the base of the next older leaf (III). The primary seedling axis (formed by the plumule) becomes the creeping prostrate stem of the mature plant. The radicular pole of the hypocotyl is covered by adhesive hairs, i.e., rhizoids (Rh), and produces exogenously a claw-shaped holdfast (H) that fixes the young plant to the rock (Figs. 42–48). Thus, in M. fluviatilis there is no elongate root arising from the hypocotyl, contrasting with many other Podostemoideae (Went, 1926
; Rutishauser, 1997
). Foliage leaves of young plants show a broadened blade portion, which is dissected along the margin into narrow lobes (Figs. 49–50).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Engler, 1930
). These three genera were included in the tribe Mourereae by van Royen (1951
, 1953)
. Here we will refer to these genera as the Mourera group. Beyond the Mourera group, the comparison will also include other genera, among them the three largest New World genera: Apinagia (50 spp.), Marathrum (25 spp.), and Rhyncholacis (25 spp.). They belong to a seemingly natural group, which is labeled here as the Apinagia group. Most information on these taxa comes from the following literature: Tulasne (1852
, 1852–1853
); Warming (1882
, 1888
, 1890
, 1899
, 1901
); Goebel (1893)
; Mildbraed (1904)
; Matthiesen (1908)
; Went (1910
, 1926)
; Engler (1930)
; Steude (1935)
; Accorsi (1951)
; van Royen (1951
, 1953)
; Schnell (1967
, 1969
, 1998)
; Cook (1996)
; Novelo and Philbrick (1997)
; Tur (1997)
; Rutishauser, Novelo, and Philbrick (1999)
.
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; Schnell and Cusset, 1963
; Grubert, 1976
; Rutishauser and Grubert, 1994
; for M. aspera, see Tur [1997]
). The circinate ultimate segments of the seedling leaves in M. fluviatilis (Figs. 51–53), however, closely resemble the marginal fimbriae of the cabbage-like foliage leaves of adult plants (Rutishauser, 1995
). Both are forked and provided with hairs along the concave sector of the coils. Foliage leaves of young plants already show a broadened blade region with fimbriate lobes along the margin (Figs. 49–50; Went, 1926
).
Mourera fluviatilis has the longest leaves of the Mourera group (up to 2 m long) (Went, 1926
; van Royen, 1953
). Adult leaves of M. alcicornis and M. aspera (Fig. 61) are pinnatisect or entire with a length up to 9 cm and up to 35–100 cm, respectively (Warming, 1888
; Tobler, 1933
; Steude, 1935
; van Royen, 1953
; Tur, 1997
). Mourera fluviatilis is the only species with vascularized prickles on the adult leaves. These multicellular prickles (up to 3 cm long), as well as chlorenchymatous warts with a diameter of <1 mm, arise from the upper leaf surface (Schnell, 1967
, 1969
, 1994
, 1998
; Rutishauser and Grubert, 1994
; Rutishauser, 1995
). Both prickles and warts are lacking in seedling leaves of M. fluviatilis. Foliage leaves of young plants, however, possess chlorenchymatous warts but lack vascularized prickles (Figs. 49–50; Went, 1926
). Mourera fluviatilis is a member of the Mourera group. Foliage leaves of M. alcicornis and M. aspera have epiphyllous chlorenchymatous warts but lack vascularized prickles. All other members of the Mourera group seem to lack both warts and prickles also in foliage leaves of adult plants. Leaves of these species are repeatedly forked or pinnatisect, as is typical for M. glazioviana, M. schwackeana (Fig. 64), M. weddelliana (Fig. 59), and Lonchostephus elegans (Fig. 65; Tulasne, 1852
, 1852–1853
; Warming, 1899
; Troll, 1941
; van Royen, 1953
). The 10–30 cm long adult leaves of Tulasneantha monadelpha are repeatedly forked and provided with a prominent and slightly flattened petiole up to 16 cm long (Engler, 1930
; van Royen, 1953
).
There are no obvious shoot meristems in young and adult plants of M. fluviatilis (Hammond, 1937
; Rutishauser and Grubert, 1994
; Rutishauser, 1995
). Easily observable shoot meristems are also lacking in both seedlings and adult plants of many other Podostemoideae (Rutishauser, 1997
). According to van Royen (1953
, p. 9) the "stem" in Mourera spp. is "formed by the fusion of the leaf-bases." Such a view fits with the phytomeric model for the description of shoots in other flowering plants (Rutishauser and Sattler, 1985
; Brutnell and Langdale, 1998
; Scanlon and Freeling, 1998
). This model postulates the shoot being composed of phytomers (stem segments), each of which comprises a leaf with its node and internode. Induction of leaves directly from leaves is also known in other flowering plants, e.g., in a maize mutant as described by Schichmas, Schneeberger, and Freeling (1997)
.
Holdfasts and roots in the Mourera group
The prostrate stems and leaf bases of M. fluviatilis and other congeneric species (e.g., M. aspera) are fixed to the rock by highly polymorphic outgrowths of up to 4 cm length (Warming, 1888
; Went, 1910
, 1926
, 1929
; Tobler, 1933
; Troll, 1941
, fig. 1841; Accorsi, 1951
; Grubert, 1974
, 1975
, 1991
). These claw-shaped to tendril-like organs are called holdfasts (= hapterons). According to Went (1910
, 1926)
they show thigmotactic growth. Because they arise as exogenous outgrowths from the stem and leaf bases any homology with roots is normally denied.
Most Podostemoideae possess elongate creeping roots with root-borne shoots (Rutishauser, 1997
; Rutishauser, Novelo, and Philbrick, 1999
). Mourera fluviatilis, however, lacks both creeping roots and root-borne shoots (Went, 1926
). Plants of M. fluviatilis may be able to produce vegetative propagules after leaf fragmentation, similar to M. aspera (Tobler, 1933
; Napp-Zinn, 1988
). Nothing is known with certainty about the presence or absence of elongate roots in other members of the Mourera group. Warming (1899)
mentioned for M. schwackeana that the shoot arises from a root. Warming (1888
, fig. 5), Accorsi (1951
, fig. 22), and Tur (1997
, fig. 4b) described and illustrated prostrate axes of two kinds in M. aspera: thick ones with leaf scars (diameter 
1.5 cm) and thin ones without leaf scars (diameter 3 mm). According to Warming (1888)
these thin prostrate axes of M. aspera are roots that endogenously form lateral shoots. It is unclear why Accorsi and Tur did not use again the term root. Outside the Mourera group there seem to be only a few taxa of New World Podostemoideae that lack elongate creeping roots, e.g., Castelnavia princeps and Rhyncholacis carinata (= Rh. macrocarpa) (Goebel, 1889
; Warming, 1882
, 1899
; Mildbraed, 1904
; Troll, 1941
, p. 2338; van Royen, 1954
).
The Podostemoideae bauplan
Plant construction in the Mourera group can be understood as an elaborated version of what is found in other Podostemoideae. Prostrate, horizontal shoots are found in New World Podostemoideae such as Marathrum, Oserya, Rhyncholacis, and Vanroyenella (Rutishauser, 1995
, 1997
; Rutishauser, Novelo, and Philbrick, 1999
). They all have dithecous (double-sheathed) and monothecous (single-sheathed) leaves. Dithecous leaves (with two leaf sheaths each) normally terminate a shoot module while the leaves below are monothecous (with only one sheath each). Warming (1890)
called the dithecous leaves "mother leaves" because they stand between two "daughter leaves," which are adjacent to both sheaths and arise as first members of two new modules (sympodial units). Both daughter modules can produce again some monothecous leaves prior to a terminal dithecous leaf. This type of sympodial organization may be called stem bifurcation. It was called dichotomous branching by Warming (1888
, 1890)
, Engler (1930)
, and Rutishauser (1997)
, although it is not identical to true dichotomous branching, which is the division of an apical meristem into two equal daughter apices (Fisher, 1976
; Wagenitz, 1996
). Stem bifurcation is associated with the occurrence of dithecous leaves in many Podostemoideae (Rutishauser, 1997
). Stem bifurcation leads to the formation of two new modules (sympodial units) from within both sheaths of the dithecous leaf. Modules without monothecous leaves occur when dithecous leaves are developed subsequently (e.g., in Marathrum spp.; Rutishauser, Novelo, and Philbrick, 1999
).
In most New World Podostemoideae genera (including Apinagia, Marathrum, Oserya, Podostemum, Rhyncholacis, and Vanroyenella) and various Old World Podostemoideae there is a developmental pattern that we refer to as the Podostemoideae bauplan (Cusset, 1992
; Jäger-Zürn, 1995
; Rutishauser, 1997
; Rutishauser, Novelo, and Philbrick, 1999
). The characteristics of the Podostemoideae bauplan are as follows. (a) Shoot buds are formed endogenously along a prostrate creeping root, if the root is not lacking as in Mourera fluviatilis. (b) Seedling axes or root-borne shoot buds produce main stems, which are either short and totally adherent to the rock, or elongate and fixed with a basal holdfast only. Monothecous leaves with distichous phyllotaxis are formed as long as there is no shoot branching. (c) Most Asian Podostemoideae have unbranched shoots with a terminal flower. Many American Podostemoideae, however, show stem bifurcation, which is correlated with the occurrence of a dithecous leaf at the end of the main stem. (d) Axillary shoot branching is lacking. There are no daughter shoots that arise from the distal axils of the monothecous (single-sheathed) leaves, as is typical for most other angiosperms. (e) New modules (sympodial units) repeat the growth behavior of the main shoot axis, with the possible formation of additional monothecous leaves prior to another dithecous leaf and the next stem bifurcation. (f) One or both sheaths of a dithecous leaf may be occupied by a flower or a flower fascicle, as is observable in several American Podostemoideae.
Inflorescences of the Mourera group as highly elaborated version of the Podostemoideae bauplan
The inflorescences in Mourera were called racemes or pseudo-racemes ("pseudo-grappes" by Warming, 1888
, 1899
; "Trauben" by Engler, 1930
) because they resemble true racemes. Inflorescences similar to those of Mourera fluviatilis are found in other species of Mourera (Figs. 59, 64), as well as Lonchostephus (Figs. 65–67) and Tulasneantha. Sometimes the inflorescences are branched and compound. For example, in M. alciformis, M. aspera (Figs. 60–61), and M. glazioviana (Fig. 63) they are forked, with a dithecous leaf or bract in the fork between the two arms. The flowers are arranged in two rows along each arm (Warming, 1899
). The outer rows may even continue down to the common stalk of a forked inflorescence in M. aspera and M. weddelliana (Fig. 61; van Royen and Reitz, 1971
). The forked inflorescences are due to stem bifurcation, which may be repeated, leading to complex inflorescences with several raceme-like subunits. In M. alciformis and M. aspera there are branched inflorescences with 2–5 dithecous foliage leaves (VI–X in Figs. 60–61), which separate the inflorescence subunits (Warming, 1888
, 1899
; Matthiesen, 1908
; van Royen, 1953
).
The number of inflorescences per plant varies between one and 11 in M. fluviatilis (Schnell, 1967
, 1994
, 1998
; Grubert, 1974
). Thus, a vigorous plant may produce several inflorescences. The multiplication of inflorescences is due to repeated formation of inflorescence primordia from one or both sheaths of a dithecous leaf (e.g., from leaf III in Fig. 5). There are two daughter modules (sympodial units) that produce a new inflorescence immediately or after the formation of additional leaves (e.g., J1 and J2 in Fig. 5). This type of stem bifurcation may be repeated by the formation of additional dithecous leaves.
Whether there are several separate raceme-like inflorescences as in M. fluviatilis (Fig. 3) or a single complex inflorescence that is forked repeatedly as in M. aspera (Fig. 61) mainly depends on the respective position of intercalary stem elongation, i.e., the site of peduncle formation. In M. fluviatilis the distal arms of the forks elongate considerably (up to 40 cm), whereas all more proximal axes stay short. Thus, all inflorescences arise as separate units from the prostrate stem. In M. aspera the peduncles are formed by elongation of the proximal stem portions below the forks. Thus, the result is a stalked inflorescence with forked subunits and dithecous leaves in the forks (Warming, 1888
; Steude, 1935
). Forked inflorescences in combination with dithecous leaves or bracts were also observed in M. glazioviana and M. weddelliana (Figs. 59, 63; Tulasne, 1852
, 1852–1853
; Warming, 1890
, 1899
; Engler, 1930
).
Size variation and basipetal growth of the inflorescences in the Mourera group
In Mourera and Tulasneantha there are normally over 20 flowers per inflorescence with sequential anthesis in basipetal order. Stalked inflorescences with only 3–6 flowers are found in Lonchostephus, the third genus of the Mourera group (Figs. 65–67; Engler, 1930
). Even M. fluviatilis can produce similar dwarf specimens with few-flowered inflorescences. Schnell (1969)
observed a specimen of M. fluviatilis with only two flowers and a bract between, whereas the other leaves of the slightly elongate inflorescence axis had an obvious blade (Fig. 62).
Inflorescences in Mourera fluviatilis and other members of the Mourera group consist of a terminal dithecous leaf or bract and two lateral rows of dithecous bracts (with reduced blades). The proximal sheath of each lateral bract covers the distal sheath of the next proximal bract (Fig. 30; van Royen, 1953
). The flowers of the inflorescences of M. aspera (Fig. 61), M. fluviatilis, and Tulasneantha monadelpha show basipetal anthesis of the flowers along each row (Warming, 1888
; Engler, 1930
). Further studies are needed to elucidate whether in all members of the Mourera group basipetal anthesis is developmentally correlated with basipetal bract and flower initiation. Such additional studies may also show that in the Mourera group inflorescence development always starts with a dithecous bract in terminal position.
The inflorescences of the Mourera group may be derived from those of the Apinagia group
Raceme-like inflorescences with basipetal flower initiation seem to be restricted to the Mourera group within the Podostemoideae. The Mourera inflorescences can be better understood when they are compared with members of other New World Podostemoideae, especially with Apinagia from South America. Most Apinagia species possess upright, elongate shoots carrying flowers (e.g., A. multibranchiata from Venezuela, A. riedelii from southeastern Brazil). They are constructed according to the Podostemoideae bauplan. Apinagia riedelii produces sympodial chains ("monochasia") of flowers, each with a single dithecous foliage leaf between two consecutive flowers. This pattern may serve as an evolutionary starting point for the derivation of the Mourera-type inflorescences because also in all members of the Mourera group each module (sympodial unit) consists of a dithecous leaf and a flower. Warming (1888
, 1890
, 1899)
and Engler (1930)
concluded that in the Mourera group two chains ("monochasia") of flowers are fused congenitally and basipetally with the inflorescence axis. Recurrent congenital fusion ("retrocaulescence") may have been the developmental change that resulted in the evolution of the raceme-like inflorescences of the Mourera group. Each dithecous bract (Bx in Fig. 30) wraps a flower with its distal sheath (F) and gives birth to a new module (with Bx + 1 and F) on its proximal side, covered by the proximal sheath of Bx. This hypothesis was accepted by van Royen (1951)
who described the inflorescences of the Mourera group as "two-sided spiciform monochasia." Further developmental studies in Apinagia spp. (e.g., A. multibranchiata, A. riedelii) will help to better understand inflorescence construction in the Mourera group (Rutishauser and Grubert, unpublished data). Further studies may also elucidate the morphological significance of the second outer sheath of the dithecous leaves or bracts in Mourera and other Podostemoideae (Jäger-Zürn, 1995
; Rutishauser, 1997
). There is a certain similarity to the densily packed "hypopeltate" bracts as described by Endress (1975)
in inflorescences of other vascular plants.
Comparison with Cordia (Boraginaceae)
The inflorescences of the Mourera group resemble those of Cordia (Boraginaceae). The Boraginaceae, a sympetalous family of dicotyledons, are not closely related to the Podostemaceae (Troll, 1964
; Uhlarz and Weberling, 1977
; Weberling, 1989
). Similar to Mourera, the inflorescences of Cordia spp. show basipetal initiation of lateral appendages (bracts, flowers), whereas other Boraginaceae are provided with normal monochasia (cincinni) and acropetal flower initiation. Troll, Uhlarz, and Weberling derived the Cordia inflorescences by "folding down" the monochasia (cincinni) and by their congenital fusion with the axis of the inflorescence. They called this hypothetical process "retrocaulescence." In contrast to Cordia and other Boraginaceae, the inflorescences of the Mourera group show a dithecous bract instead of a flower in the terminal position of each raceme-like unit. Thus, inflorescences in the Mourera group seem to be only superficially comparable to the "retrocaulescent" inflorescences of Cordia. It may be also useful to compare the Mourera inflorescences with the spikes of Loranthaceae such as Phoradendron and Dendrophthora. Similar to Mourera inflorescences, the spikes of these genera show basipetal flower inception due to an intercalary meristem (Kuijt, 1959
, 1969
).
Flower biology and meristic variation of stamen number in Podostemoideae: Mourera group and Apinagia group
The inflorescence presents flowers in anthesis for 1–2 wk depending on the total number of flowers that open in basipetal order. The flowers of Mourera fluviatilis consist of a pink pedicel and pink filaments with purplish-brown anthers surrounding a green ovary (Fig. 2), whereas the tepals are inconspicuous. The slightly sweet-scented "brush-flowers" attract bees, mainly Trigona spp. (Went, 1926
). Similar flowers (also pink and scented) are found in Rhyncholacis penicillata, i.e., another podostemad that occurs in the same rapids of the Rio Caroní (Venezuela). Anthesis of both M. fluviatilis and R. penicillata lasts 1 d (Grubert, 1974
). The most proximal flowers of the inflorescences in Mourera fluviatilis may be cleistogamous. Then they are surrounded by their spathella until the capsules are ripe (Engler, 1930
).
The combination of polystemonous flowers consisting of an outer whorl of stamens with introrse anthers and an inner whorl of stamens with extrorse anthers is restricted in Podostemoideae to three species in the Mourera group: Mourera fluviatilis, M. schwackeana, and probably M. weddelliana (van Royen, 1953
). Three other Mourera species (e.g., M. aspera) as well as the sister genera Lonchostephus and Tulasneantha lack extrorse anthers, because the flowers possess a single androecial whorl with 5–14 introrse anthers only (Warming, 1899
; Engler, 1930
; van Royen, 1953
; Tur, 1997
). Anthers with extrorse dehiscence are rare in other Podostemoideae. South American species of Apinagia (section Wentia), as well as Jenmaniella and Oserya (other putative members of the Apinagia group) have flowers with extrorse anthers (Engler, 1930
; van Royen, 1951
, 1954
). Various degrees of congenital fusion of stamen filaments occur in the Mourera group. In M. fluviatilis there are rarely two neighboring filaments that are united at the base (Rutishauser and Grubert, 1994
). This phenomenon is more evident in M. schwackeana where some of the 20–25 stamen filaments in a flower are regularly fused (Warming, 1899
; van Royen, 1953
). In Tulasneantha monadelpha the 6–10 stamens are united into a basal tube (Engler, 1930
).
Somewhat surprising is the high degree of intraspecific variation in stamen number in M. fluviatilis. There are (14–)22–32(–40) stamens per flower (the less frequent numbers in brackets; Rutishauser and Grubert, 1994
). According to Matthiesen (1908)
, Went (1910)
, and Schnell (1967)
, the flowers with the highest stamen numbers are found in the distal region of the vigorous inflorescences, whereas flowers in the more proximal regions have fewer stamens. Similar variations in stamen number are found in other members of the Mourera group (Warming, 1888
; van Royen, 1953
; Schnell, 1998
). Stamen numbers above 20 are also found in members of the Apinagia group, combined with a remarkable intraspecific variation and stamens in 1–2 complete or incomplete whorls: e.g., Apinagia multibranchiata (Venezuela) with 6–29 stamens per flower (Grubert, 1974
; Rutishauser and Grubert, unpublished data), A. staheliana (Guyana, Surinam) with 8–29 stamens per flower (Went, 1926
; Schnell, 1969
), and Marathrum squamosum (Brazil) with 4–40 stamens per flower (van Royen, 1951
). Polystemonous flowers with 5–25 stamens per flower are also found in Weddellina squamulosa (northern South America). The monotypic genus Weddellina is a very odd podostemaceous member that has to be accepted as an own subfamily (Weddellinoideae) rather than as part of the Tristichoideae (Engler, 1930
; Cusset and Cusset, 1988
; Jäger-Zürn, 1997
; Rutishauser, 1997
).
Affinities of the Mourera group and the Apinagia group
According to van Royen (1951)
the genera Mourera, Lonchostephus, and Tulasneantha belong to the tribe Mourereae (= Mourera group). These three genera are characterized by stalked raceme-like inflorescences. These inflorescences can be interpreted in context with the Podostemoideae bauplan, especially when using Apinagia as an evolutionary starting point (see above). A closer relationship between the Mourera group and the Apinagia group (mainly consisting of Apinagia, Marathrum, and Rhyncholacis) was proposed by Engler (1930)
. He united both groups in the American tribe Lacideae (= Apinagieae), whereas all other genera of New and Old World Podostemoideae were added to the second tribe Eupodostemoneae. The Mourera group and the Apinagia group are held together by various characters, for example: (a) some members of both groups form polystemonous flowers, i.e., flowers with more than one complete stamen whorl; (b) no andropod (Y-shaped androecium) is formed when the stamen number is reduced to two; (c) pollen grains are shed as monads, not as dyads as is typical for most other Podostemoideae genera (Rutishauser, 1995
, 1997
; O'Neill et al., 1997
); (d) several members form large foliage leaves with fimbriate margins or dissected blades; and (e) the upper leaf surface of various members of both groups possess photosynthetic appendages (prickles, warts, or tufts of filaments) when the leaf blade is broad enough.
Molecular and nonmolecular criteria elucidating the phylogenetic position of Mourera and allies
Les, Philbrick, and Novelo (1997
, 1998
) included rbcL sequence data of New World Podostemoideae (e.g., Apinagia, Marathrum, Mourera, and Podostemum) and compared it with some Old World Podostemoideae and members of the smaller subfamily Tristichoideae. The cladograms presented by Les, Philbrick, and Novelo (1997
, 1998
) are nearly identical with the relative placement of the genera within the Podostemaceae: Tristicha was placed as sister to the analyzed Podostemoideae taxa (including Mourera). Mourera was sister to the remaining Podostemoideae. The basal taxa of this clade are uniformly South/Central American in distribution (including Apinagia and Marathrum), whereas Podostemum and all studied taxa from Asia (e.g., Cladopus, Zeylanidium) are more derived. Thus, with respect to rbcL sequence data Mourera can be viewed as the most primitive genus of all Podostemoideae. An ancient position of Mourera was proposed by Schnell (1969
, 1994)
, who based his conclusion on morphological and embryological evidence. With respect to inflorescence evolution, however, the Mourera group appears to be more advanced as compared to some members of the Apinagia group (see above). The polystemonous flowers of Mourera spp., Apinagia spp., and Marathrum spp. with at least one complete stamen whorl may be viewed as a plesiomorphic character in the Podostemoideae, whereas the reduction of stamen number to 1–2 per flower (as found in, e.g., Cladopus, Podostemum, and Zeylanidium) is apomorphic.
The Podostemaceae as molecular misfits
The Podostemaceae have to be regarded as morphological misfits (Bell, 1991
; Rutishauser, 1995
, 1997
). Meanwhile, molecular data for various Podostemaceae genera were presented by Les, Philbrick, and Novelo (1997
, 1998
), as well as Ueda et al. (1997)
. Similar to Ceratophyllaceae (Qiu et al., 1993
; Sytsma and Baum, 1996
) the Podostemaceae turn out to be molecular misfits as<
