Botanical Journal of the Linnean Society, 2002, 138, 63–84. With 30 figures
Comparative studies in the morphology of
Crenias weddelliana and Maferria indica with
reference to Sphaerothylax abyssinica
(Podostemaceae: Podostemoideae)
IRMGARD JÄGER-ZÜRN*
Hainerbergweg 61, D-61462 Königstein, Germany
Received May 2001; accepted for publication August 2001
The scope of morphological plasticity of vegetative structures among Podostemoideae (Podostemaceae) is documented for Crenias weddelliana, a neotropical species, Maferria indica, a palaeotropical species, and Sphaerothylax abyssinica, from Kenya, and compared with related taxa. The study highlights intrinsic characters of the widely
enigmatic plant body of many species of the subfamily Podostemoideae. These include dorsiventrality of shoots
occurring irrespective of gravity, incurvate distichy and one-sided spirodistichy correlated with shoot dorsiventrality, asymmetric leaves, and several types of positioning of the two prophylls and inflorescence structures. The homogeneity of hairs of the ‘Zeylanidium olivaceum type’ established on the subulate leaves of some Indian species is of
taxonomic value. The latter also applies to the stipella (not stipule) on the asymmetric compound leaf in New World
species. The morphological data represent a framework of features consistent for the subfamily. © 2002 The
Linnean Society of London, Botanical Journal of the Linnean Society, 138, 63–84.
ADDITIONAL KEY WORDS: aquatic plant – asymmetric leaf – compound leaf – distichy – dorsiventrality of
shoots – hairy leaf – hapters – incurvate distichy – inflorescence – prophyll – ramification – root-borne shoots –
spirodistichy – stipella
INTRODUCTION
Species of the widespread aquatic flowering plant
family Podostemaceae (c. 48 genera, c. 270 species) are
rheophytes, mainly occurring in the tropics. Fastened
to rocks in swift running rivers, Podostemaceae grow
submerged except for their flowering and fruiting
stages. At the beginning of the seasonal low water
level of rivers, they seemingly shift from an aquatic
to aerial life. These plants depend on the seasonal
change of the water level, as flowering and seed
dispersal take place only above the water.
Among water plants with special adaptations to
aquatic conditions, Podostemaceae have been considered enigmatic in terms of the structure of the plant
body. However, comparative morphology, i.e. analyses
of homologous structures, has proven fruitful in interpreting often intricate structures (Jäger-Zürn, 1997,
*E-mail: [email protected]
1999; 2000a,c). Comparative morphology can reveal an
understanding of the often complex and abnormal (relative to other angiosperms) structures of Podostemaceae, in addition to helping sort out the genetic
vs. environmental bases of variation. Our understanding of structures of many species remains superficial,
being based on previous descriptions (Warming, 1881,
1882, 1888, 1889; Willis, 1901/02ab, 1882; Matthiesen,
1910; Went, 1910, 1926; Hammond, 1936, 1937; van
Royen, 1951; 1953, 1954; Arekal & Nagendran, 1974).
Recently, analysis of vegetative and floral structures of
mature plants has been accomplished for 13 (of about
260) species of Podostemoideae, which is the largest
of the two (or probably three: see Kita & Kato, 2001)
subfamilies: Mourera fluviatilis Aublet (Rutishauser
& Grubert, 1994, 1999), Marathrum rubrum Novelo &
Philbrick, M. schiedeanum (Chamisso) Tulasne, M.
tenue Liebmann, Vanroyenella plumosa Novelo &
Philbrick (Rutishauser et al., 1999), Apinagia multibranchiata (Matthiesen) van Royen (Rutishauser &
Grubert, 2000), Zeylanidium olivaceum (Gardner)
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Engler (Jäger-Zürn, 2000a,b), Zeylanidium subulatum
(Gardner) C. Cusset (Jäger-Zürn, 1994, 1999; 2000b;
as Podostemum subulatum), Polypleurum munnarense
Nagendran & Arekal (Jäger-Zürn, 2000d as Podostemum munnarense (Nagendran & Arekal) Mathew
& Satheesh, but recent data (Philbrick, unpubl.) suggest the removal of this species to Polypleurum; see
Nagendran & Arekal, 1981), Sphaerothylax abyssinica
(Weddell) Warming (Jäger-Zürn, 2000c), Hydrobryum
japonicum Imamura (Ota, Imaichi & Kato, 2001),
and Willisia selaginoides (Bedd.) Warming ex Willis
(Uniyal & Mohan Ram, 2001), Hydrobryopsis sessilis
(Willis) Engler (Uniyal, 2001). Each of the species
investigated so far reflects the basic morphological
‘bauplan’ of Podostemoideae, illustrating specialization
of roots, ramification, inflorescence and leaf structure.
Even so, studies of additional species are needed to
further elucidate the remarkable range of variation in
the family. The degree of structural variation that
occurs in Podostemaceae is only now beginning to be
revealed.
The goals of this paper are to present detailed
comparative morphological data and interpretation
for Crenias weddelliana (Tulasne) C. D. K. Cook & R.
Rutishauser (syn. Mniopsis weddelliana Tulasne;
see Cook & Rutishauser, 2001) and Maferria indica
(Willis) C. Cusset as compared with Sphaerothylax
abyssinica (Weddell) Warming.
MATERIALS AND METHODS
The material of Crenias weddelliana has been taken
from the collection of Prof. Dr Wilhelm Troll, accessioned into the herbarium of the Department of
Special Botany of the University of Mainz, Germany.
Sphaerothylax abyssinica was collected in 1960 by
Professor Dr Werner Rauh, Heidelberg, Germany,
near Nyeri, Kenya. Maferria indica was collected from
the Cittar river at Courtallam, South India, in 1968
by the author. Voucher specimens of the two species
are with the author. Plants were fixed in FPA
(formaldehyde/propionic acid/ethanol). Serial sections
were made from paraffin embedded material and
stained with Safranin Fast Green and Haematoxylin
(Delafield’s), respectively. Illustrations are camera
lucida drawings.
RESULTS
Species of subfamily Podostemoideae are characterized by vigorous growth of secondary (i.e. root-borne)
shoots arising from the flanks of flattened roots.
Shoots become more or less upright, while roots in contrast show plagiotropic creeping on rocks. This basic
structure of Podostemoideae is modified by either
favouring roots (which, for example, become promi-
nent broadened crusts with small shoots arising from
the root surface, as in Zeylanidium olivaceum) or
shoots (with the roots remaining more or less threadlike, for example in Z. subulatum). Crenias weddelliana and Maferria indica belong to the second type
and correspond to typical members of Podostemoideae.
Sphaerothylax abyssinica develops elongated shoots
as well as small secondary shoots on crustose roots
and thus corresponds to both types (Jäger-Zürn,
2000c).
CRENIAS
WEDDELLIANA
Crenias weddelliana develops numerous, about 1-cm
long branched or unbranched secondary shoots along
the flanks of ribbon-shaped roots (Fig. 1). Shoots are
dorsiventral and distichously foliated and correspond
to the bauplan of Podostemoideae. Instead of being
opposite at an angle of 180°, leaves are initiated in a
divergence angle of about 130°, opening toward one of
the two sides of the stem, which ensue from the distichous foliation of the shoot (Fig. 2). This side is called
the ‘front side’ hereafter. The other side, separated by
the distichous position of leaves is called the ‘reverse
side’ of the shoot (see below).
Leaves are pinnate to pinnatilobed (Fig. 3). Whereas
leaves arising lower on the stem are simple
(Fig. 1A–C), subsequent leaves appear forked, tripartite or pinnate. The compound structure is evident on
upper, still involute young leaves (Fig. 3A–E). They
show two or more pinnae on either side of the leaf
margin. The number of young pinnate-shaped lobes is
the same along both leaf margins. Both margins and
young pinnae are equal in shape at first. Later, pinnae
of the leaf margin that points towards the reverse side
of the shoot elongate into rounded lobes (Fig. 3F).
Pinnae pointing to the front side of the shoot develop
dissimilarly, although the ontogeny of pinnatilobed
leaves is the same on both margins. The lowermost
pinna of the leaf margin (facing the front side of a
shoot) does not elongate, but remains in a basal position and appears “descended” to the leaf base (Fig. 3FG). A pinna in this position is called a stipella because
of its resemblance to stipules. However, stipules are
distinguished from stipellas in being a part of the leaf
base and characterized by precocious development.
That is not the case in C. weddelliana. Each foliage
leaf of C. weddelliana develops one stipella (Fig. 3H).
Stipellas lack a vascular bundle, whereas each pinna
is traced by a vascular strand. Stipellas thus illustrate
the asymmetry of leaves and the bilateral symmetry
(dorsiventrality) of shoots in C. weddelliana. The compound leaf structure is seen by the major apical lobe
and the two (or more) lobes in flanking positions at
either side of the bifacial leaf (Fig. 3F–G). When leaves
are mature, the two lobes that face the reverse side of
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Figure 1A–D. Crenias weddelliana, root-borne shoots. A–B, two shoots arising from a root, seen from their front sides
(A) and reverse sides (B). C, shoot with tuberous hapters and a shoot-borne root. D, flowering shoot with two young fruits;
note stipella on the front-side leaf margin. f = fruit, h = hapter, r = root, stl = stipella. Scale bar = 2.5 mm.
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Figure 2A–L. Crenias weddelliana. Serial cross-sections of a vegetative shoot (front side orientated upward) showing
the incurvate distichous foliation, made obvious by the vascular leaf traces; note the position of the vascular strand of
the shoot axis (A–D), the apical furrow (asterisk) and the asymmetrical sheathing leaf base bearing a stipella. a = axial
vascular strand of the shoot, stl = stipella. Scale bar = 500 mm.
Figure 3A–J. Crenias weddelliana, leaf development. A–E, young compound pinnate leaves. D and E, same leaf (D) in
natural orientation and (E) spread; note developing pinnae on both margins. F–G, mature pinnate leaves with a stipella
at the leaf base. H–I, distichously foliated root-borne shoot, seen from the front side (H) and the reverse side (I) showing
the asymmetric leaf base with a stipella toward the front side. stl = stipella, p = pinna. Scale bar = 1 mm in A–E; 2.5 mm
in F–I.
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the stem develop into large pinnae, compared with
those of the opposite leaf margin, which are usually
smaller. Leaf blades are bifacial (not subulate)
throughout (Figs 4A–H, 7). Each pinnate lobe
possesses a vascular bundle.
Dithecous leaves, i.e. leaves provided with two
sheaths at the leaf base, occur at branching points
(Fig. 4I; 5D–G). One sheath of the dithecous (doublesheathed) leaf faces the mother shoot as usual, the
second sheath occurs on the reverse (dorsal, abaxial)
side of the leaf base. The second sheath, in this way,
envelops the young branch which arises in a subfoliar
position relative to the ‘subtending’ leaf (Fig. 4I; 5F).
Similar structures have been described from Zeylan-
idium subulatum from India and Sphaerothylax
abyssinica from Kenya (Jäger-Zürn, 1994, 1999;
2000c), and occur widely in many other Podostemoideae (see Rutishauser, 1997; Rutishauser & Grubert,
1994, 1999, 2000; Rutishauser et al., 1999).
Not only the shape of leaves but also the structure
of the shoot axis indicates dorsiventrality of shoots as
seen in cross-sections (Fig. 6). Leaf traces are mostly
at an angle of about 130° resulting in incurvate distichy (Figs 6, 8). The incurvate distichy is a consequence of the dorsiventrality of shoots; leaves, too,
are asymmetrical in shape. Leaves are obliquely orientated, with the margin pointing toward the reverse
side of the shoot detached lower on the stem (Fig. 2).
Figure 4A–I. Crenias weddelliana. A–H, serial cross-sections of a foliage leaf showing sheath and stipella (A–C) and the
partition of the pinnate lamina, each pinnate lobe has a vascular bundle. I, cross section of two upright shoots arising side
by side from a root with their reverse sides adjacent to each other thus demonstrating the asymmetry of shoots independently from the force of gravity; also see the subfoliar position of two young branches enveloped by the additional sheath
of the dithecous leaf which is still fused to the shoot axis. br = branch (stippled), sh = sheath, stl = stipella. Scale
bars = 500 mm.
Figure 5A–G. Crenias weddelliana. Serial cross-sections of a branched vegetative shoot (front side orientated upward)
showing the position of the branch at the reverse (dorsal) side of the dithecous leaf (E); see the vascular strand which is
common to the dithecous leaf and branch, diverging in C; note the incurvate distichy of leaves as well as the establishment of four more leaves on the main shoot after branching. a = axial vascular strand of the shoot, br = branch, c = common
vascular strand, d = dithecous leaf, r = root, stl = stipella. Scale bar = 500 mm.
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MORPHOLOGY OF SOME PODOSTEMACEAE
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Figures 6–8. Crenias weddelliana. Fig. 6. Incurvate distichy of a vegetative shoot (cross-sections) and the apical meristem area; note stipellas at the front side leaf margins. Fig. 7. Cross-section of pinnate leaves. Fig. 8. Close-up view of the
apical meristem area and the vascular leaf traces in incurvate distichous position. a = apical meristem of the shoot axis,
stl = stipella, v = vascular strand. Scale bar = 500 mm in Figs 6 & 7; 200 mm in Fig. 8.
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MORPHOLOGY OF SOME PODOSTEMACEAE
The margin toward the front side, provided with
a stipella, makes the dorsiventrality readily visible
(Fig. 6). It is worth mentioning that the dorsiventrality of the shoot axis occurs independently of gravity.
This is shown on two closely aligned root-borne shoots
(Fig. 4I): although gravity was applied equally to these
adjacent shoots, they are mirror images of each other
in terms of the location of the diverging leaves traces
(about 130°) and orientation of the stipella. As the consequence, the terms ‘upper’ and ‘lower side’ (or ‘dorsal’
and ‘ventral’ side, respectively) commonly used for
shoots of the Podostemoideae, have been dropped
herein in favour of the terms ‘front side’ and ‘reverse
side’.
The apical meristem of vegetative shoots is tiny
and developed as an apical furrow (Fig. 8). The
youngest leaves are not fused around the apex in
the form of a pseudo-stem but become detached soon
after initiation (Fig. 2E–J). A primordium obviously
exhausts the major part of the apical meristem.
Only before initiation of the next primordium is
the apex visible as a circular unilayered meristem
(Fig. 8).
In floriferous shoots, dorsiventrality is indicated
by the position of floral organs. Stamens (or the
androphore) and the ovary are perpendicularly orientated relative to the distichous position of leaves. The
ovary turns to the front side of the shoot, whereas
the stamina face the reverse side. The two carpels of
the ovary are in the median position. The carpel next
to the androecium is smaller than the other, and is
located higher than the carpel on the front side of the
shoot (Fig. 18L, which is the same in Maferria indica,
and Fig. 23, in Sphaerothylax abyssinica).
Branching of C. weddelliana occurs in the same
manner as in other members of Podostemoideae
(Jäger-Zürn, 1994, 1999; 2000c): branch position is
subfoliar; the subtending leaf is above the branch
instead of below it. The leaf associated with branching is dithecous. In C. weddelliana, branching occurs
not only at flowering but also in the vegetative condition (Fig. 5). It is noteworthy that the dichasial
ramification mode is not regularly established in C.
weddelliana. Branching occurring in connection with
the two uppermost leaves (i.e. as ‘subtending’ leaves,
or as dithecous leaves, respectively) is named
‘dichasial’. Dichasial branching is found in other
Podostemoideae. In some instances, branches in C.
weddelliana develop also in connection with leaves
positioned lower on the stem. Two to several leaves are
found between the point of branching and the (apical)
flower. Consequently, in some specimens of C. weddelliana, the inflorescence is not cymoid. In many floriferous shoots, the cymoid type also occurs with the last
leaf being dithecous and ‘bearing’ a branch (Fig. 4I).
The leaf of the opposite orthostichy can be monothe-
71
cous (with one (adaxial) sheath only); this leaf consequently lacks a branch.
Young branches (Fig. 5A, B) show that the vascular
strand is shared by the branch and leaf at their base.
The vascular strand diverges into two, below the point
on which the branch becomes visible as a group of
meristematic cells.
A multitude of creeping roots develops many
root-borne shoots which grow densely in a caespitose
manner. The endogenous initiation of root-borne
shoots from the flanks of the root takes place from the
vascular strand. Adventitious (i.e. shoot-borne) roots,
arise on the stem between lower leaves (Figs 1C, 5A).
Endogenous branching as well as regeneration of roots
has also been observed. Roots are provided with a
prominent, although asymmetric, root cap on their
upper side. Many rounded or tuberous hapters (holdfasts) arise from the base of root borne shoots. Hapters
fasten the plant body to the substratum. In contrast
to roots, hapters lack a vascular supply.
MAFERRIA
INDICA
Maferria indica is endemic to South India (Figs 9, 10).
It was first described (on the basis of dried fruiting
plants on rocks) as Farmeria indica by Willis
(1901/02a,b: 403–404). Our knowledge was enhanced
by more detailed descriptions of the plant body (Arekal
& Nagendran, 1974) and the protandrous flowers
(Mathew & Satheesh, 1997). Cusset (1992) separated
this species from the genus Farmeria and established
the monotypic genus Maferria C. Cusset.
Maferria indica is characterized by a strongly
branched root system (Fig. 11). Roots creep in looping motion superficially on rocks, and fasten to the
substratum by prominent discoid hapters which are
cortical outgrowths of roots (Fig. 11C–D). A well developed root cap is always found (Figs 11B, 13–15). The
slimy root cap cells clearly develop from the apical root
meristem (Fig. 15) and in this way confirm the presence of a typical, although small, root cap. Roots are
slightly flattened and semicircular in shape, as seen
in cross section, with the rounded side turned to the
substratum (Figs 12, 16). The dorsiventral roots
develop numerous unbranched secondary shoots along
their flanks. Root-borne shoots are initiated near the
root tip and arise endogenously in connection with the
vascular strand of the root (Figs 16, 17).
The root-borne shoots are foliated in distichous
order (Fig. 18K–N). The two orthostichies correspond
to the longitudinal axis of the roots from which the
shoots arise (Fig. 11E–F). Leaves of the two orthostichies arise in a divergence angle slightly smaller
than 180° (Fig. 18K, O–P). The divergence angle of
successive leaves on the shoot axis changes as the
shoot grows. The two first leaves at either side of the
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Figures 9, 10. Maferria indica. Habit of root-borne shoots growing in caespitose manner. r = root. Scale bar = 3 mm.
distichously foliated shoot are nearly opposite. For
subsequent leaves, the angle is reduced from 180°,
pointing toward the front side of the shoot. The phyllotactic pattern changes in the course of foliation
(Fig. 18O–P). The phyllotaxy of subsequent leaves
resembles spirodistichy, but contrary to typical
spirodistichy, the contact parastichies are one-sided in
M. indica, and turn only to the front side of the shoot.
The divergence angle of subsequent shoots thus attenuates more and more. The spathella, enveloping and
protecting the flower bud, appears to be a single leaf
(as seen in a cross section), which is nearly in a
perpendicular position to the distichous phyllotaxy
(Figs 23, 24). The spathella appears to be included
with the spirodistichy of leaves as a member of the
two contact parastichies (Fig. 18O–P). Dorsiventality
of shoots is thus accentuated by the one-sided spirodistichous arrangement of leaves.
The shoot apex is tiny and difficult to observe. Only
few one-layered meristem cells exist representing the
apical growing centre. The shoot tip is developed as an
apical furrow, surrounded by the youngest leaves. Due
to the incurvate distichy, i.e. the one-sided spirodistichy, the subulate grass-like leaves develop asymmetric sheathing leaf bases.
Leaf sheaths develop into a subulate grass-like
blade (Fig. 18E–J). One-celled hairs of the ‘Zeylanidium olivaceum type’ sometimes occur (Figs 19–22).
The hairs (up to 100 mm long) develop from specialized
epidermis cells, the trichoblasts, which differ by dense
cytoplasm. They are constricted at the epidermal
surface, but a cell wall is not established. The nucleus
of the trichoblast cell moves into the hair. Whereas
other epidermal cells possess chloroplasts, trichoblasts and hairs are free of them.
Flowers of M. indica resemble those of many species
of Podostemoideae (Fig. 18A). The bicarpellate ovary
and stamen are perpendicularly positioned relative to
the distichous foliation, with the ovary toward the
front side of the shoot (Fig. 18M, N). The axis of symmetry of the flower is marked by the carpel position
(in the median line within the ovary) as well as by the
stamen, which are perpendicular to the two orthostichies. The position of stamen and ovary mark the two
sides of the shoot (Figs 23, 24). As distichy corresponds
to the longitudinal direction of roots, the ovary faces
the root surface, whereas the single stamen denotes
the reverse side of the shoot. As the stamen and the
two carpels are in one line, that carpel next to the
stamen is smaller, because it is shifted up against
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Figure 11A–D. Maferria indica. A, branched roots with root-borne (secondary) shoots, seen from above and from below;
note the discoid hapter on the lower side. B, part of a branched root system with root-borne shoots, one of them developing a shoot-borne (adventitious) root, note its root cap. C–D, hapters developed from roots, each attached to a stone. E–F,
shoot with distichously arranged subulate leaves. E, reverse side. F, front side. c = root cap, h = hapters, r = root, s = shoot.
Scale bar = 5 mm in A; 2.5 mm in B–D; 1 mm in E–F.
the other carpel (Fig. 23). Both carpels terminate in
elongated slender stigmas with a smooth epidermis.
As noted by Mathew & Satheesh (1997), the uppermost of the two to six leaves of a shoot is regularly provided with ‘a leaf-like appendage’ at the base of the
dorsal (i.e. reverse) side (Figs 18B–D, 24). That leaf is
dithecous in shape, and comprises a distinct vascular
strand in contrast to the other foliage leaves. The
strand diverges into two bundles, one of which enters
the appendage, while the smaller becomes the vascu-
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Figures 12–17. Maferria indica. Fig. 12. Transverse section of a root. Fig. 13. Longitudinal section of a root. Figs 14 &
15. Root tips. Fig. 14. TS showing the apical root meristem above the slimy root cap cells. Fig. 15. Close-up view of Fig. 13,
showing root cap cells developing from the apical root meristem. Figs 16 &17. Endogenously developing young root-borne
shoots, linked to the vascular strand of the root from inception. Scale bar = 200 mm in Figs 12, 13, 16 & 17; 100 mm in Figs
14 & 15.
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Figure 18A–P. Maferria indica. A, root-borne flowering shoot, showing one of the distichously arranged leaves with two
appendages at the reverse side. B–D, cross-sections of sheathing dithecous leaves with one or two appendages on the dorsal
side. E–J, serial cross-sections of two successively originated leaves showing the bifacial sheathing base (E & F) and the
subulate blade (one of them stippled) (G–J); note the irregular shape. K–N, serial cross-sections of a floriferous shoot (from
below upwards) terminated by a flower, showing the position of floral organs: the ovary facing the front side, the stamen
the reverse side; note the slight sheath-like cavity of a dithecous leaf which, however, lacks a branch or appendage. O–P,
diagrams of two actual examples of shoots showing slight spirodistichous phyllotaxic pattern; the contact parastichies
pointing towards the front side to the middle line of the shoot with the spathella. ap = appendage, d = dithecous leaf,
g = gynoecium, l = leaf, sh = sheath, st = stamen. Scale bars = 500 mm.
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Figures 19–22. Maferria indica. Figs 19–21. Sections of leaves provided with hairs of the ‘Zeylanidium olivaceum type’;
note the constriction of the hair (but not a cell wall) at the leaf surface, the position of the nucleus within the hair (Fig.
21), and the trichoblast cells in LS, visible by their dense cytoplasm (Fig. 20). Fig. 22. Trichoblasts seen in transverse
section of the epidermal layer. t = trichoblast. Scale bar = 10 mm in Figs 19–21; 100 mm in Fig. 22.
lar bundle of the dithecous leaf. As the presence of a
dithecous leaf marks a branching event in Podostemoideae, the appendage, being located at the branch
position, certainly represents a rudimentary branch.
The grass-like appendage clearly represents the first
leaf of that branch. This phenomenon occurs regularly
in the uppermost leaf and occasionally in both upper
leaves (Fig. 18A–D). A visible appendage is, however,
not always established. In some instances, the respective foliage leaf is dithecous, i.e. with a sheathing
cavity at the reverse side of the leaf, but without an
appendage (Fig. 18M–N). In addition, in some leaves
a slight cavity occurs on the reverse side of the leaf,
but an appendage is lacking; this type of leaf differs
from others by the presence of a distinct vascular
strand which other leaves of M. indica usually do not
develop. Lastly, other leaves show two ‘appendages’
arising from the reverse (dorsal) side of the uppermost
leaf. These examples show the ability in M. indica to
develop a branch, but further growth is arrested in
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Figures 23, 24. Maferria indica. Subsequent cross-sections of the distichously foliated floriferous shoot (front side
orientated upwards) with a dithecous leaf (Fig. 23) developing an appendage (= prophyll a of a branch) (Fig. 24).
ap = appendage, d = dithecous leaf, g = gynoecium, l = locule, sp. = spathella, st = stamen. Scale bar = 500 mm.
development. The interpretation of arrested branching in M. indica seems developmentally related to the
regular branching pattern seen in root-borne shoots of
Sphaerothylax abyssinica (see below).
SPHAEROTHYLAX
ABYSSINICA
Root-borne shoots of Sphaerothylax abyssinica resemble secondary shoots of M. indica (Figs 25, 26).
As in M. indica, root-borne shoots of S. abyssinica
usually develop only one flower. Rarely, a second
flower occurs in S. abyssinica, associated with a rudimentary branch at the opposite side of the main shoot.
Most secondary shoots in S. abyssinica remain
unbranched.
The small secondary shoots of S. abyssinica are
distichously foliated with a divergence angle of 180°
(Fig. 25). A dithecous leaf occurs in S. abyssinica
which develops a prominent sheathing base, i.e. the
sheath facing the (mother) shoot axis. At the base of
the reverse side, the dithecous leaf possesses neither a branch nor a second sheath (Fig. 25B). The vascular strand of the dithecous leaf diverges into two
bundles and indicates the existence of the branch
which is represented soon after by its first leaf,
prophyll a (Figs 25C–E, 27–30). The additional
sheath of the dithecous leaf then becomes visible. The
apical branch meristem is faintly recognizable as a
group of meristematic cells (Figs 28–30). The meristem gives rise to the second prophyll b higher up on
© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 138, 63–84
78
I. JÄGER-ZÜRN
Figure 25A–E. Sphaerothylax abyssinica. Serial cross-sections of a distichously foliated floriferous shoot, the front side
indicated by the position of the ovary, the reverse side by the stamens; note the dithecous leaf and the subfoliar branch
position at the reverse side of the leaf (B–E). b = branch, d = dithecous leaf, g = gynoecium, st = stamen. Scale bar = 100 mm.
the branch (Fig. 30). Both prophylls are fused to the
additional (second) sheath of the dithecous leaf. The
process of branching occurs in the same manner in
M. indica.
The ovary and stamen in S. abyssinica are in the
median line of the shoot and thus perpendicular to the
distichous foliation (Figs 25, 26). The single stamen or
the two stamens point to the reverse side, the ovary
to the front side of the shoot. In this way, the dorsiventrality of shoots and the position of ovary and
stamen relative to the shoot axis are maintained, but
neither incurvate distichy nor spirodistichy occur.
DISCUSSION
Crenias weddelliana and the four other species of the
genus, as well as species of Podostemum, are a group
of neotropic Podostemoideae of a rather similar
growth form (van Royen 1954; Tur 1997). The Old
World species Maferria indica resembles them in
many respects. Although considerable new insight into
the morphological complexity of Podostemaceae has
been provided, much of our understanding of the
family remains fragmentary. Even so, integration of
the information provided herein with that of the pub-
© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 138, 63–84
MORPHOLOGY OF SOME PODOSTEMACEAE
79
Figures 26–30. Sphaerothylax abyssinica. Fig. 26. Cross-section of a root-borne shoot terminated by a flower and branched in connection with the uppermost (dithecous) leaf. Fig. 27–30. Close-up views of the branching event seen in
serial sections. Note the divergence of the vascular strand into a leaf bundle and a branch bundle (Fig. 27) and the
first leaf (= prophyll a) arising from a group of small axial cells (Figs 28 & 29) as well as subsequent leaves of the branch
(Fig. 30). br = branch, d = dithecous leaf, g = gynoecium, sp. = spathella, st = stamen. Scale bar = 500 mm in Fig. 26; 200 mm
in Figs 27–30.
© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 138, 63–84
80
I. JÄGER-ZÜRN
Table 1. Summary of the distribution of characteristics in certain Podostemoideae
Dorsiventral shoot
Incurvate distichy
Compound leaves
Simple leaves
Hairy leaves
False lamina
Changing phyllotaxis
Distichy perpendicular
Distichy corresponding
180° distichy
Crenias
weddelliana
Maferria
indica
Zeylanidium
subulatum
Zeylanidium
olivaceum
Polypleurum
munnarense
Sphaerothylax
abyssin.
+
+
+
+
+
+
+
+
+
+
+
+
+
+
(+)
+
+
+
+
+
+
+
+
+
Crustose roots
+
+
lished literature reveals several apparent evolutionary patterns. These patterns are presented below with
the aim of establishing a working hypothesis that can
be tested via subsequent morphological and phylogenetic analyses (Table 1).
1 Although secondary (root-borne) shoots turn
upright and are not characterized by a more or
less plagiotropous growth as otherwise occurring
in Podostemoideae, a clear dorsiventrality of shoots
exists in C. weddelliana and M. indica. The dorsiventral symmetry is illustrated by the distichous foliation
of shoots, separating a ‘front side’ from a ‘reverse side’.
The reverse side of floriferous shoots is marked by the
position of one or two stamens, the front side by the
ovary. The floral organs are perpendicularly orientated with respect to the distichous foliation. Such an
orientation is typical in species of subfamily Podostemoideae investigated so far (e.g. Old World species
Maferria indica, Zeylanidium subulatum, Z. olivaceum, Polypleurum munnarense from India, and the
African species Sphaerothylax abyssinica, as well as
Crenias weddelliana from Brazil). Although the two
sides of the more plagiotropously growing secondary
(floriferous) shoots of Z. olivaceum and Z. subulatum
have been named ‘upper side’ (marked by the ovary)
and ‘lower side’ (marked by the stamens) (Jäger-Zürn
1999, 2000a), these designations have been dropped
here as they are not generally applicable for the also
upright growing root-borne shoots. These terms have
been replaced by the designations ‘front side’ and
‘reverse side’. The two sides are further distinguishable by differing leaf margins of the asymmetrical
leaves, which are especially marked in Crenias weddelliana by unilateral stipella development on the
front side of the shoot.
2 Incurvate distichy, brought about by the divergence angle smaller than 180° toward the front side,
+
+
+
Crustose roots
+
is a widespread character among Podostemoideae.
Such a pattern is found in Crenias weddelliana (130°)
and as a horse-shoe shaped arrangement in Zeylanidium subulatum, and similarly also Polypleurum
munnarense and Z. olivaceum from India. Maferria
indica contrasts by one-sided spirodistichy. Whereas
the former species show first and second leaf position
in a narrower divergence angle (about 90° in Z. subulatum) than those of subsequent leaves (the angle of
which is increased), the opposite occurs in M. indica.
In the latter species, the divergence angle is 180°
at first, but decreases in subsequent leaves. Both
spirodistichous contact parastichies are located on the
front side of the shoot (meeting each other), and ensue
a progressively decreasing angle (Fig. 18). In typical
spirodistichy, one of the two contact parastichies turns
to the front side, the second to the reverse side of the
shoot. This is not the case in M. indica, as the direction of the spirodistichous contact parastichies is influenced by the dorsiventrality of the shoot, and both
parastichies turn to the front side. Interestingly, one
or both contact parastichies are traceable to the
middle line of the spathella, which supports the suggestion that the spathella is a single hypsophyll. The
contact parastichies further indicate that the hypsophyll (= spathella) is obviously perpendicular to the
distichous phyllotaxis. The phenomenon of incurvate
distichy is, however, not developed in the African
Sphaerothylax abyssinica.
3 The typical distichous phyllotaxic pattern of M.
indica turns to spirodistichy in the course of subsequent leaf development. Change to another kind of
phyllotactic pattern has been observed in Polypleurum
munnarense (Jäger-Zürn, 2000d). The two first leaves
do not share the horse-shoe shaped incurvate distichy
of subsequent leaves, but stay apart. Whereas the
divergence angle of the first and second leaves is 180°
© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 138, 63–84
MORPHOLOGY OF SOME PODOSTEMACEAE
in M. indica, it is greater than 180° in P. munnarense,
opening toward the front side of the shoot. The mode
occurring in P. munnarense has not been found in
other species.
4 Two patterns exist regarding how distichous
leaves of root-borne shoots are orientated relative
to the root from which they arise. In M. indica and
Crenias weddelliana, distichy corresponds to the
longitudinal axis of roots. This orientation is also
reported from Z. subulatum (Jäger-Zürn, 1999), but
also Podostemum mülleri Warm. (Tur, 1997) and P.
ricciiforme (Liebm.) van Royen (Novelo & Philbrick,
1997a, 1997b; Jäger-Zürn, unpubl.). A second pattern
has been found in Polypleurum munnarense with distichous shoots orientated perpendicularly to the longitudinal axis of roots. The front side of shoots thus is
directed to the root tip.
5 Leaf structure distinguishes the New World
species Crenias weddelliana from Maferria indica,
and also from most other species of Podostemoideae from India. In India, subulate grass-like simple
leaves prevail, and some possess ‘Zeylanidium olivaceum type’ hairs on one side of the leaf: M. indica,
Z. subulatum, Z. olivaceum (Jäger-Zürn, 1999; 2000a)
and Z. lichenoides (Jäger-Zürn, unpubl.). Polypleurum
munnarense, though provided with subulate leaves,
lacks hairs. Crenias weddelliana and many other
New World species (van Royen, 1951, 1953, 1954;
Novelo & Philbrick, 1997b; Tur, 1997) develop bifacial
compound leaves. Leaf ontogeny of C. weddelliana
shows pinnae along both leaf margins. Leaf blades are
thus pinnate, not forked. As a peculiarity of C. weddelliana, the lowermost pinna at the front-side leaf
margin becomes a stipella. Similar leaves may occur
in Podostemum mülleri and P. uruguayense depicted
by Tur (1997), although their development has not
been studied in detail. Leaves of C. weddelliana, being
evidently asymmetric, are linked to the Old World
species which also have asymmetrically shaped leaf
bases.
6 Simple leaves in Polypleurum munnarense and
Zeylanidium subulatum develop a deceptive lamina
(i.e. a false blade) as the result of an elongation of the
midrib toward the reverse side of the leaf with the
effect that the false blade is perpendicularly orientated relative to the position of the bifacially originated leaf (Jäger-Zürn, 2000d). The shape of the false
blade of Z. subulatum is enhanced by the production
of hairs on one side. Though M. indica develops hairs
of the same type, a false lamina does not occur on the
more or less square-shaped blades (as seen in transverse section) (Fig. 18E–J). However the position of
hairs on one side of the grass-like blade in M. indica
is similar to that which occurs in Z. subulatum.
7 Ramification in Podostemoideae has been de-
81
scribed as cymose, i.e. dichasial (Jäger-Zürn, 1999,
2000c; Rutishauser & Grubert, 2000). Branching in
connection with flowering results in a triplet of
flowers, also called a module by Rutishauser &
Grubert (2000). Two differing modes of the dichasial
branching pattern exist in Podostemoideae with
regard to the position of prophylls. The transverse
position of the two prophylls, i.e. the usual mode
in dicotyledons, does occur in the African species
Sphaerothylax abyssinica (Jäger-Zürn, 2000c). The
resulting partial inflorescence is either a cincinnus
(= scorpoid cyme) or a bostryx (= helicoid cyme). A
second type is observed in Zeylanidium subulatum
(Jäger-Zürn, 1999). Here, prophyll position on the
branch occurs in the (same) direction of the distichy of
the mother shoot, i.e. prophylls are not transversely
positioned, but in the median line of the leaf that is
connected with branching. Flowering branches are
therefore in one line with the flower of the main shoot
resulting in a rhipidium or a drepanium. Crenias weddelliana belongs to the second type, however it differs
from Z. subulatum in the sequence of the two prophylls. Prophyll a is next to the mother shoot in
Crenias weddelliana, whereas, in Z. subulatum, this
position is occupied by prophyll b. A variety of possible prophyll positions is thus realized in Podostemoideae. In its transverse position (i.e. the common
type), S. abyssinica appears less specialized than the
others.
8 Crenias weddelliana deviates from the ramification mode of other species of Podostemoideae investigated so far in two ways. First, branching is not
confined to flowering shoots, but occurs also in the vegetative stage. Second, branching is not exclusively
dichasial, i.e. in connection with the two uppermost
leaves of a flowering shoot, but occurs also lower on
the stem. In this case, the ramification is racemose, as
it occurs along the main shoot axis. In the vegetative
stage of C. weddelliana, branches occur along a foliated shoot which develops additional leaves after the
branching event. The branch has many leaves. In the
floral stage, the main shoot develops additional leaves
after branching. This ramification mode is therefore
not dichasial (a form of the cymose branching type)
because branches are not directly below the terminal
flower. The dichasial mode is a reduced form of the
racemose pattern. The incidentally occurring racemose (not strictly dichasial) branching of the main
shoot axis in C. weddelliana points to possibly multiflorous elongated inflorescences (e.g. panicles or
thyrsus with flowering branches along a main axis) as
a basic pattern of this species. Consequently, racemose
branching and paniculate inflorescences are perhaps
a basic pattern throughout Podostemoideae. Inflorescences were few-flowered in C. weddelliana in the
© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 138, 63–84
82
I. JÄGER-ZÜRN
material used, thus details concerning the inflorescence type are not clear. Yet, Warming (1881) depicted
many-flowered specimens, already in the fruiting
stage, but inflorescence type could not determined
based on his descriptions. More investigations are
needed. In one case in the present study, the branch,
lower on the stem, was found to grow more vigorously
than the main shoot. This points to a possible basitony
of branches relative to the main shoot. Similarly
foliated branched flowering shoots as in C. weddelliana have been depicted for another species of the
genus, C. scaturiginum (Mart.) C. D. K. Cook & R.
Rutishauser (as Mniopsis scaturiginum Mart.) by
Warming (1881: plate VI, 1899: 136) and may be
assumed also for the other species of the genus
(Warming 1881, 1882; 1888; 1899). Similar racemose branching occurs, e.g. in Podostemum mülleri
(Tur 1997). This fact points to racemose branching
pattern as common in this group, and is present in
the vegetative as well as the floral stages. If this
holds true, dichasial ramification (resulting in a triplet
of flowers) and the cymoid inflorescence in many
species of the Podostemoideae would then be a depauperate form of a former racemose pattern in the
subfamily.
9 The branch arises higher on the dithecous leaf
in Sphaerothylax abyssinica, but not at its base,
which may suggest that the branch is leaf-borne. Such
an interpretation, however, is not supported by
observations that indicate that the young branch
diverges from the main shoot axis (Jäger-Zürn, 2000c:
215). The branch position in S. abyssinica and C. weddelliana appears as a kind of recaulescence, which is
unusual. The means by which this ‘shifting’ of the
branch on the leaf occurs is not yet understood. Maferria indica presents the same branch position higher
on a dithecous leaf, although only visible as the
‘appendage’, i.e. the first leaf of the branch. The resemblance of branches in secondary shoots of S. abyssinica (which have not yet achieved their full size)
to the dithecous leaf–‘appendage’ complex in M. indica
points to an arrested branch development in the latter.
As a consequence, it can be deduced that the seemingly unbranched one-flowered species in India
evolved from ancestors that were more branched and
with many flowers. The ‘appendage’ should be interpreted as the first leaf of a branch that is arrested in
development.
10 Roots in Podostemaceae are important with
regard to the production of secondary shoots and
clonal growth of these plants. The root system of C.
weddelliana and M. indica is increased by many
lateral roots as well as by regeneration of damaged
roots, and furthermore by the development of shootborne (adventitious) roots. The latter have been suggested for the crustose roots of Zeylanidium olivaceum
(Jäger-Zürn, 2000a: 80) and are confirmed for C. weddelliana as a multitude of roots arising from the
shoot base, as well as for M. indica. Roots originate
endogenously, whereas the accompanying hapters
are outgrowths of the stem or root, respectively, and
differ from roots by the lack of specified vascular
bundles.
CONCLUSION
The dorsiventrality of shoots of Podostemoideae
studied here has been revealed as an intrinsic structure that occurs independently from growth form and
from the force of gravity. It is enhanced by a divergence angle of 130° in Crenias weddelliana or by the
horse-shoe shaped leaf trace arrangement in Zeylanidium subulatum resulting in incurvate distichy as
well as spirodistichy (Maferria indica) in most species
dealt with here. The four Indian species (M. indica,
the previously investigated Z. subulatum, Z. olivaceum and Polypleurum munnarense) are characterized by simple leaves, provided with hairs of the
‘Zeylanidium olivaceum type’, except P. munnarense.
Among this group, Z. subulatum is linked with P.
munnarense by the occurrence of a false lamina which
may also occur in M. indica, but has not been found
elsewhere. P. munnarense, however, differs from all
other species by the orientation of distichous leaves
perpendicularly to the long axis of the root (from which
the root-borne shoots arise) and, further, by the above
mentioned switch of phyllotactic pattern. Interestingly, 180° distichy of the two first leaves links P.
munnarense to M. indica. But M. indica differs from
the other Indian species dealt with herein by flowers
with occasionally one stamen instead of two. We,
consequently, are not able to define clear evolutionary
lines of structural relationships among the Indian
species. There exist a pool of structures which seem
variously combined. The New World species C. weddelliana is linked to the Indian group (especially to Z.
subulatum) by the strong incurvate distichy and the
similar shoot orientation relative to the root. On the
contrary, the compound leaves of C. weddelliana,
Podostemum ricciiforme and other species of this
genus separate them from the Indian species. The
African S. abyssinica is distinguished from all species
referred to here by having straight (180°) distichy
throughout and the transverse position of the two prophylls. The compound leaves of this species, with
scarcely forked pinnae, however, are grass-like as in
the Indian species.
The results point to a morphological plasticity
among the taxa described here. As yet, our knowledge
of the various patterns is fragmentary. Only from
examination of additional taxa can distinct lines of
morphological evolution in the subfamily be deter-
© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 138, 63–84
MORPHOLOGY OF SOME PODOSTEMACEAE
mined. The branching pattern in the taxa described
here represents a kind of recaulescence that occurs on
the ‘wrong’ (reverse) side of the leaf. Such a pattern
represents a basic divergence from that which is otherwise typical in angiosperms. This phenomenon and
the evolutionary process of the (deviating) subfoliar
branch position remain enigmatic.
ACKNOWLEDGEMENTS
The author is very much indebted to Dr C. T.
Philbrick, Associate Professor of Biology, Danbury, CT,
USA, for reading the English manuscript, which considerably improved the quality of the text. The valuable comments of the reviewer are gratefully
acknowledged.
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