BotanicalJournal of the Linnean Society, 78: 3 11-32 1. With 4 figures
Julie
1979
Byugate phyllotaxis in Rhizophoreae
(Rhizophoraceae)
P. B. TOMLINSON AND D. W. WHEAT
Haruard University, Haruard Forest, Petersham, M A 01366
Accepted for publication February 1979
Phyllotaxis in the inangrove genera of Rhizophoraceae is shown to be bijugate, the angle between
orthostichies always less than 90D and in some species close to one half the Fibonacci angle (68.8O).
The saiiie leaf arrangement occurs in both orthotropic shoots with extended internodes and in the
crowded terminal rosettes of those branches which develop plagiotropy by apposition growth, and
can be interpreted as an adaptive architectural feature in relation to mutual leaf shading.
KEY WORDS: - Rhizophoraceae - tree architecture - phyllotaxis - bijugy.
CONTENTS
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introduction
Matcrials and Methods
Observations
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Discussion
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Ackiiowledgetiients
Kclcrrtices
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INTRODUCTION
A knowledge of phyllotaxis has important consequences in at least two
disciplines. In anatomy it is a pre-requisite for understanding the internal
vascular system in the shoots of plants, because leaf arrangement closely
determines the course and interconnection of vascular bundles. In ecology, leaf
arrangement is a factor in the photosynthetic strategy of a plant, since the
primary arrangement of leaves can determine maximum light interception. In
comparative studies of the shoot system of certain Rhizophoraceae we have
lbund it necessary to revise current statements about their phyllotaxis. The
phyllotaxis is usually described as decussate but is in fact bijugate, and the
dif’ferencehas important morphological consequences.
The Rhizophoraceae is a small tropical family of 16 genera and about 120
species (Airy-Shaw, 1974). The most familiar species are found in the four genera
of mangroves, Bruguiera, Ceriops, Kandelia, and Rhizophora. The latter is pantropical arid the main constituent of most mangrove communities. These genera
lbrrn the natural tribe Rhizophoreae (van Vliet, 1976) and our observations are
317
0024-4074/79/0403 1 7-05/$02.00/0
0 1979 The Linnean Society of London
P. B. rOMLINSON AND D. W. WHEAT
318
largely concerned with these taxa in relation to studies o n the biology of
mangroves. Apart from Anzsophyha (and related genera with apparently
tiistichous leaves, sometimes segregated as a family Anisophylleaceae) the
Rhizophoraceae have opposite stipulate leaves. Descriptions frequently refer to
this arrangement as decussate (e.g., Ding Hou, 1958, for the family; Salvoza,
1936, for Rhizophora; Graham, 1964, for Rhizophora; Lewis, 1956, for Cassipoured.
Schmidt ( 19031, in a little-cited monograph, noted the non-decussate phyllotaxis
of this group, although he provided no quantitative data. A characteristic feature
of Khizophora and some species in related genera (e.g., Bruguiera gymnorrhiza Lam.)
is the development, as illustrated by Schmidt, of terminal rosettes of leaves on the
distal parts of axes which are plagiotropic by apposition (Hallt?, Oldeman &
Tornlinson, 1978). Gill & Tomlinson (1969) described these shoots as decussate
but with a marked tendency for the leaf pairs to be arranged in a progressive
spiral. This statement requires explanation.
MATERIALS AND METHODS
Shoots of all genera of Rhizophoreae including most species, were examined
i n the field and laboratory as part of a survey of the morphology, floral biology,
taxonomy and geography of mangroves which is being conducted in South
Florida and the South Pacific (cf. Gill & Tomlinson, 1969, 1971; Tomlinson,
1978; Tomlinson, Primack & Bunt, 1979; Tomlinson 8c Womersley, 1976).
Dissection of fresh material or of fixed shoots was done at Harvard Forest and
at the Australian Institute of Marine Science, Townsville, Queensland. Most
microscopic observations were made with a Wild M-5 stereomicroscope, but
freehand sections of buds were made for observations with a compound
microscope. Photography of specimens illuminated with high intensity fibre
optics (Figs 1-41 was done with macro-lenses o n a bellows extension fitted to a
camera back.
0 BS ERVATI 0 NS
Nodes in all genera of Rhizophoreae consist of a pair of opposite foliage leaves
below a pair of stipules inserted at right angles to the leaves of the same node.
Leaf blades and stipules are roiled distally and are imbricate, always interdigitating in the same way (cf. Gill & Tomlinson, 1969; Fig. 1 1 ) . The stipule of
the youngest expanded leaf pair encloses all younger developing primordia
in such a way that it forms the conspicuous terminal 'bud', even though the
shoots are essentially indeterminate and without bud-scales (Gill & Tomlinson,
197 1). Stipules fall when the next-youngest internode elongates. Within the
Figures 1-4. Rhizophoreae (Rhizophoraceae). Shoot apices with older leaves and enveloping stipules
renioved (all x 131. Fig. 1. Kandelza candel. Fig. 2 . Eruguiera exarislata. Fig. 3. Rhzzophora mangle. Fig. 4.
L'e7iup.s tugal.
L,, Youngest leaf pair (possible younger leaf primordia were ignored); L,, L,, successively older
leaf pairs; S, and S, stipules associated with leaf pairs L, and L,; C, colleters. Lines show the
dorsiventral planes of the first, second and third pairs of leaves, estimated by eye, the method used
lor measuring angular divergence between successive leaf pairs.
BlJ IJGA-IT P HYLLOTAXIS 1N R H I 2 0 PHO REAE
319
320
P . B. TOMLINSON AND D. W. WHEAT
Table 1
Species
Kandelia candel (L.)Druce
Rhizophora mangle L.
Bruguiera exan'rtata Ding Hou
Cenops tagal [Perr.) C. B. Roxb.
No. of
buds
examined
Mean divergence
angle between
pairs of
leaves'
3
3
7
5
79.70
81.7O
69.6O
70.0°
Standard
error of
the mean
2.8O
1.70
1.002
3.701
lSignificantly less than 90° in all examples at the 95% level.
'Not significantly different from 68.8O a t the 95%level.
terminal bud there is a maximum of three further pairs of leaves plus the stipule
primordia, as noted for Rhizophoramangle L. by Gill & Tomlinson (1971). In other
genera there may be fewer; Ceriops tagal (Perr.) C . B. Roxb. for example,
consistently has only two fwther visible nodes within the oldest stipule pair.
Colleters (club-shaped glands) are abundant on the inner surface at the base of
the stipules and are apparently the source of mucilaginous (e.g., Ceriops) or fluid
(e.g., Rhizophora) secretions. Primack & T o m h s o n (1978) noted that these
secretions in Rhizophora stylasa Griff are sugary and attractive to birds.
Measurement of the angle between leaves of successive pairs cannot be made
precisely because there is no exact mid-point to either the stem or the leaf
prirnordia, and this must therefore be estimated by eye. Further, usually only two
sets of measurements can be made on a single bud because of the small number
of bud components. However, the flat shallow cone of the apical region does
facilitate microscopical observation (Figs 1-4). The primary leaf arrangement in
all shoots examined consists of pairs of leaves with successive pairs succeeding
each other at an angle less than 90° j.e., the phyllotaxis is bijugate.
Representative values for four different taxa are listed in Table 1. These show that
the angle between orthostichies is not 90°, but some value statistically
significantly less than this. Only the figures for Bruguiera and Ceriops fall close to
a theoretical half-Fibonacci angle of 68.8O, a value which might be expected in
strict bijugy.
DISCUSSION
The bijugate condition in the tribe Rhizophoreae seems a constant and
primary feature of shoot construction and has important consequences in the
architecture of' the tree. In those examples such as Bruguiera gymnorrhiza which
conform to Aubreville's rnodel (Hall6 & Oldeman, 1970; Halli., et al., 1978) and
develop plagiotropic branch complexes by apposition growth, the congested
rosettes of leaf pairs maximize their photosynthetic ability by minimizing the
amount of mutual shading, especially where there is a n approximation to the
half-Fibonacci angle. The situation is similar in trees like Rhizophora (Attims's
model) except that plagiotropy is achieved gradually by progressive reclination
of essentially orthotropic shoots (cf. Halle, et al., 1978: 53).
Bijugy has been thought most common in congested systems with short
BIJUGATE PHYLLOTAXIS IN RHIZOPHOREAE
32 I
internodes, such as rosette plants (Cutter, 1964)and this is supported by the configuration of outermost shoots in the trees we studied. Though the Rhizophoreae
have long internodes on trunk axes and on initially orthotropic branch axes,
bijugy remains a constant feature. O n elongated shoots the arrangement
simulates a decussate system and presumably confers appropriate (but unknown)
benefits.
The consequences of this leaf arrangement in the vasculature of the shoot is
that there are no precise orthostichies and the median traces of alternate leaf
pairs are not vertically superposed. Preliminary observation shows that the
'twisting' of the vascular system accommodates the morphological displacement
and median leaf traces do, in fact, unite with traces at alternate nodes above and
below.
We have not examined other Rhizophoraceae in detail, but it seems likely that
the bijugate condition characterizes all members of the family with opposite
leaves.
ACKNOWLEDGEMENTS
Extensive field observation on natural populations of Rhizophoreae in
Australasia were made possible by grants from the National Geographic Society
(1973, 1976) and the National Science Foundation ( I N T 76-24479) to P. B.
Tomlinson. Facilities provided by J. S. Bunt, Australian Institule of Marine
Science, Townsville, Queensland and the Assistant Director, Division of Botany,
Office of Forests, Lae, Papua New Guinea are gratefully acknowledged. The
material of Kandelia candel was supplied by P. Chai, Department of Forestry,
Kuching, Sarawak.
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