J . Linn. SOC.(Bot.),59, 378, p .

229 229
With 1 plate and 45 text-figures
Printed i n &eat B7itain
July, 1965

The significance of the leaf epidermis in the taxonomy of the

Combretaceae
I. A general review of tribal, generic and specific characters*
BY CLIVE A. STACE
Department of Botany, University of Manchester
(Accepted fw publication November, 1964)

(Communicated by $. W . Exell, F.L.S.)

CONTENTS
PAGE
Introduction: Materials and methods . . 229
Epidermal characters of the Combretaceae . . . 230
Venation . . 230
Domatia . . 231
Hydathodes and related structures . . 231
Epidermal cells . . 231
Leaf margin . 232
Stomata . . 232
Trichomes . . 232
Cuticular membrane . . 234
Generic surveys . . 234
1. Strephoneim . . 235
2. Cmbretum . . 236
3. Pteleopsis . . 236
4. Quisqualis . . 238
5. Guiera . . 239
6. Thiloa . . 240
7. Cabpyxis . . 240
8. Terminalia . . 241
9. Bucida . . . 244
10. Buchenavia . . 244
11. Ramatuella . . 245
12. Conocarpus . . 246
13. Anogeissus . . 246
14. Fi'inetia . . 247
15. Calycoptel.is . . 247
16. Lumnitzera . . 248
17. Lagumuhl.ia . . 248
18. Macropteranthes . . 249
Key to the epidermides of the genera of Combretaceae . 249
Discussion . . 250
Acknowledgements . . 251
References . . 251

INTRODUCTION : MATERIALS AND METHODS

Since Exell's admirable survey of generic limits in the Combretaceae (Exell, 1931)
considerable numbers of new species have been discovered, and much work has been
* This paper represents a modified portion of a thesis accepted for the Ph.D. degree in the University
of London.
 230 CLIVE A. STACE
done in new and unexploited fields of investigation. This, together with a careful re-
appraisal of the longer established data, has resulted in a better understanding of the
family which it is desirable to express in taxonomic terms. The present series of two
papers sets out to present a resume of the evidence accrued from a fairly intensive
study of the leaf epidermis and trichomes.
The material for this investigation consisted almost solely of specimens from the
herbarium of the Department of Botany, British Museum (Natural History), and
embraced all the genera and subgeneric groups of the family, amounting to about 250
species. The amount of material of each species examined varied from 1 to about 20
specimens according to the availability of leaves and the variability of the epidermal
characters observed.
The bulk of the routine examinations was carried out on cuticular preparations
obtained exactly as detailed previously (Stace, 1965), but in many caaes these were
supplemented by epidermal peels, surface and vertical sections cut freehand or with
a freezing microtome, cellulose acetatelgentian violet films (North, 1956), and in the
case of trichomes by whole mounts. About 1100 permanent cuticular preparations are
deposited in the Department of Botany, British Museum (Natural History), representing
about half the number that were originally examined.
The terminology applied to epidermal characters follows that of Stace (in press), and
the tribal and generic classification is based upon that of Engler t Diels (1899), aa modi-
fied by Exell (1931). I n this system the family is divided into the 2 subfamilies
Strephonematoideae, containing the single genus Strephonema, and Combretoideae,
consisting of 4 tribes: Combreteae, with the genera Combreturn, Pteleopsis, Quisqualis,
Guiera, T h i h and Cabpyxis; Terminalieae, with the genera Terminalia, Bucida,
Buchenavia, Ramatuella, Conocarpw and Anogeissus; Calycopterideae, with the genus
Calywpteris (Getonia);and Laguncularieae, with the genera Laguncularia, Lumnitzera
and Macropteranthes. Two genera have been described since Engler & Diels’ work:
Terminaliopsis (Danguy, 1923), which Exell included under Terminalia; and Pinetia
(Gagnepain, 1916), a distinct new genus related to Anogeissus in the Terminalieae.
Thus 18 genera, placed in 5 tribes and 2 subfamilies, were used as a starting point
for the investigation. The above classification is based upon morphological characters of
the flowers, fruits and vegetative shoot, but a knowledge of these is not essential for
an understanding of the present paper.

EPIDERlldrLL CHARACTERS OF THE COMBRETACEAE

Venation
Since the epidermis above and below the midrib, veins and venules is usually modified
in various ways, and the cuticular membrane bears an impression of the epidermal cells,
the pattern of leaf venation can in most cases be studied on cuticular preparations. All
members of the Combretaceae possess simple entire leaves with a pinnate venation
system whose ultimate venules join up to form a venule reticulum, so that there are
few major taxonomic features concerned with the venous organization. There are a
number of examples, however, particularly in the genera Combretum, Termimlia,
Buchenavia and Anogeissus, of species which can be identified with the aid of their
distinctive venation patterns, usually relating to the numbers and direction of the
lateral veins, size and shape of the areolae, and the prominence of the venule reticulum.
The degree to which the venous system is represented on the epidermis depends upon
the development of the vein extension which connect the two (Wylie, 1943), and this
in turn is to some degree related to the development of layers of water-storage tissue in
 The signijmnce of the leaf epidermis in the taxonomy of the Combretaceae 231
the leaf. I n the 3 genera of the Laguncularieae the lateral venous system is scarcely or
not a t all visible on the epidermis, but this is not true of any other genus of the family.
I n a number of cases useful diagnostic characters at the specific level are found in the
shape and size of the modified epidermal cells lying over the venous system.

Domatia
The major types of phyllodomatia, small pits or pockets of unknoan significance
found on the leaves of a wide range of woody dicotyledons, have been classified by
Stace (1966), and in the Combretaceae all 4 types are present. Basolaminar domatia
revoluta are found in all species of Strephonema, but in no other genus; primary-axillary
domatia marsupiformia (Pl. 1, fig. 1) are found in various species of all 6 genera of the
Combreteae, 3 of the 7 genera of Terminalieae, and in Calycopteris; primary-axillary
domatia lebetiformia (Pl. 1, fig. 2 ) are found in the genera Terminalia (one-fifth of the
species), Corncurpus (all 3 taxa) and Buchenuvia (1 of the 24 species) of the Terminalieae;
and domatia fasciculata are scattered in a few species of one or two genera, their
occurrence being of doubtful constancy and significance. In addition the small marginal
depressions present in Lumnitzera have been described as domatia, and as such would
fall into the third group above. Within the marsupiform and lebetiform groups the size
and shapes of the domatia have proved to be valuable specific criteria in the genera
Terminalia and Buchenmia.
Domatia have very rarely been used by taxonomists, although they are of considerable
systematic significance in many cases. In the Combretaceae the occurrence of t h e
various types of domatia ties in quite well with Engler & Diels’ classification; and in
several genera they are important diagnostic features. The need to investigate their
possible use in other families is therefore emphasized. They are best examined by means
of cuticular preparations, but much can be deduced by a study of whole leaves with a
dissecting microscope.
Hydathodes and related structures
I n the genera Lumnitzera and Lagunculuria large stomata surrounded by radiating
rows of epidermal cells are found scattered over the epidermides, and these have been
described as water-stomata. I n many cases the stoma appears t o fall out, leaving a
jagged hole with the characteristically modified epidermal cells around it. Sometimes
such areas, which are often referred t o as hydathodes, develop unassociated with
stomata.
Whilst the presence of these structures is of interest and taxonomic significance they
are of limited value in identification as similar jagged holes have been found in various
species of other genera, notably Terminalia, where they are almost certainly not
homologous with those of the former 2 genera. I n other cases they merely represent
the site of wounds or of fungal infection. I n the genera Conocarps and Nacropteranthes
they are of very spasmodic occurrence and there their nature is quite obscure, although
they are undoubtedly not caused by external agents.

Epidermal cells
The various features of those epidermal cells not modified due to their proximity to
veins, stomata, trichomes, hydathodes or the leaf margin are sometimes of considerable
systematic value, and have been reviewed by Stace (1965). Those found most useful
in the Combretaceae include the cell shape, particularly with regard to the number of
anticlinal walls per cell and the presence of secondary anticlinal divisions, the type
and degree of anticlinal cell-n-all undulation, the presence of thin areas in the outer
wall of the epidermal cells, and the presence and types of papillae on the outer wall.
232 CLIVEA. STACE
These characters have with few exceptions been found to be significant only at the
specific level. Strephonema, Laguncularia and Guiera, however, are all distinguishable
on their epidermal cell-shape alone.

Lea.. m r g i n
The epidermal cells a t the leaf margin are modified in various ways, usually, like
those over the veins, being elongated or squarish and arranged in parallel rows. This
situation is almost universal in the Combretaceae, but in Laguncularia the marginal
epidermal cells are not arranged in such a regular manner. Elsewhere in the family,
however, the epidermal cells a t the leaf margin provide very few diagnostic characters.

Stomata
In the Combretaceae the stomata provide many important taxonomic characters
concerning a. wide range of structural and distributional features. In the majority of
cases, however, these are of systematic value only at the species level, although there are
of course a number of exceptions to this. Aspects of stomatal structure which have
proved important in various genera are the degree and pattern of thickening of the
guard-cell walls; the distribution of cuticular thickenings on the outer and inner guard-
cell walls, particularly regarding the stomatal ledges; the degree of sunken-ness of the
guard-cells in the epidermis; the shape of the guard-cells in surface view, notably a t the
stomatal poles; and the stomatal size.
The orientation of the stomata, the frequency per unit area or expressed as the
stomatal index, and the distribution of stomata on the 2 epidermides have also been
found to be of value in various groups of the family. Stomata are found on the upper
epidermis to a similar degree to the lower epidermis, for example, only in the genera
Lurnnitzera, Laguncularia, Macropteranthes, Conmarpus, and a very few species of
Anogeissus, Combreturn and Terrninalia.
Of much greater importance a t the generic level is the presence of subsidiary cells,
modified epidermal cells adjacent to the stomata. On this criterion 4 types of stoma
are usually recognized: 1 (anomocytic) lacking true subsidiary cells (Pl. 1, fig. 3), the
other 3 possessing them in differing arrangements. In the Combretaceae only 1 genus
does not possess anomocytic stomata, that being Streplwnemu in which the stomata are
paracytic (Pl. 1, fig. 5), the 2 subsidiary cells lying on either side of the guard-cells and
parallel to them. In addition secondary differentiation of apparent subsidiary cells
can occur within the anomocytic group, and this is the caw in Lurnnitzera (Pl. 1, fig. 4)
and Lagunculuria. Here the adjacent epidermal cells are arranged in a ring of 3-5
around the stoma and are relatively narrow in the radial plane, such a situation having
been described as cyclocytic (Stace, in press). The taxonomic significance of these 3
stomatal groups in the Combretaceae is obvious.

T r i c k
I n the Combretaceae the trichomes provide by far the most important taxonomic
characters of the epidermis, and in many cases are as valuable as any of the other
features of the plant.
Three main types of trichome are to be found in the Combretaceae. Except for a
few cases all the non-glandular trichomes are of a similar basic structure (Text-figs. 1-7),
often being known as ‘Combretaceous hairs’ (‘Combretaceen Haare’ ; Heiden, 1893).
These are long, straight, sharply-pointed, unicellular hairs with very thick walls (the
lumen often being virtually absent) and a t the base a peculiar conical internal com-
partment (Pl. 1, fig. 6) occupying usually only a fraction of the total hair length. The
 The signi$cunce of the leaf epidermis in the t a x o i m y of the Combretaceae 233

Text-figs. 1-1 2 . Son-Glandular Trichomes of the Combretmeae. Fig. 1 , compartmented

hair of Conocarpus erectus var. sericeus. Fig. 2, compartmented hair of C u k r a senegalemis.
Fig. 3, base of compartmented hair of Buche.navia capitata. Fig. 4, base of compartmented
hair of B. reticulata. Fig. 5 , bage of Compartmented hair of Strephonema mannii. Fig. 6, base
of similar hair o f S . mannii, but lacking internal compartment. Fig. 7, base of compartmented
hair of Macropteranthes kekutickii inserted in epidermis. Figs. 8, 9, non-compartmented hairs
of Quisqualw hemii. Fig. 10, non-compartmented hair of Macropteranthes leichhardtii. Fig.
11, two-armed hair of Strephonemu sericea, one arm not h e w n in full. Fig. 12, two-armed
hair of S. polybotryum.

base of the hair, which is often somewhat bulbous a t the position of the internal com-
partment, is narrowed into a peg-like foot which is inserted between 3 or more cells of
the epidermis (Text-fig. 7 ) . The precise form of the compartmented hairs is often of
systematic value at the specific or even generic level (e.g. Cuiera), but of greater im-
portance still is the fact that these hairs are found in every genus of the Combretaceae,
234 CLIVE A. STACE
and, except in extremely few species of one or two genera, in every species.Moreover, such
trichomes are elsewhere known only in the distant family Cistaceae and in a few species
of the Myrtaceae. Thus microscopic examination of the leaf indumentum is frequently of
great value in placing or rejecting sterileherbarium specimensin or from the Combretaceae.
Kon-glandular hairs of other types are relatively extremely rare in the Combretaceae.
Presumably aberrant types are not infrequently encountered in a few genera, but in
some species they are constant in occurrence and thus of greater significance. In
Macropteranthes leichhardtii F. Muell. and Quisqwlis hem2 (Engl. & Diels) Exell, for
example, thin-walled, blunt-ended, simple, unicellular hairs (Text-figs. 8-10) are found
mixed with the compartmented hairs, yet are absent elsewhere in these genera. I n
Strephonema 4 of the 5 species possess two-armed unicellular hairs which are usually
compartmented but in one species are not (Text-figs. 11,12), whilst the other species has
typical one-armed compartmented hairs (Text-figs.5,6).
Glandular trichomes of the Combretaceae are of 2 basic types: ‘stalked glands’ (Pl. 1,
fig. 8; Text-figs. 28-44), in which there is a multicellular head of 2 or more cells in all 3
dimensions (found typically in the genera Combreturn, Cabpyxis, Quisqwlis and Cono-
carpus); and ‘scales’ (Pl. 1, fig. 7; Text-figs. 13-27), in which the head consists of a
multicellular plate only 1 cell thick (found in the genera Combreturn, Guiera, Thiloa and
Calyqteris). I n both types the stalks are usually relatively short and uniseriate-celled,
although there are rare exceptions to this. In addition Lagunculuria possesses extremely
distinctive glands of a third type which a t once distinguish this genus from all the
others (Text-fig. 45). I n this case the multicellular glands are apparently sessile but
sunken in very deep small-apertured pits found scattered on both epidermides. The
types of glandular trichomes found in the various taxa of the Combretaceae are of
great diagnostic importance a t the tribal, generic and specific levels.
Other characters found to be of taxonomic value are the shape and arrangements of
the trichome-base cells and the distribution of trichomes over the epidermides. In the
genus Combreturn, for example, the compartmented hairs are always accompanied by
either scales or stalked glands (or very rarely both). Scales are almost always much more
abundant on the non-venous areas than over the veins, whilst the opposite is true of
the stalked glands. I n 3 species (C. roxburghii Spreng., C . platypetalurn Welw. and C .
trifoliaturn Vent.) which possess stalked glands, however, the latter are distributed
mainly in the non-venous areas and thus provide a valuable diagnostic character.

Cuticular membrane
The pattern of cuticular thickening on the stomata has already been mentioned as
providing systematic evidence, and the same is frequently true a t the species level
concerning the thickness of the cuticular membrane over the other epidermal cells,
particularly the trichome-base cells.
The outer surface of the cuticle is in some species furrowed and ridged in a characteris-
tic manner, and this has also been used to advantage as a taxonomic character in the
Combretaceae. Such cuticular ‘striations’are of very characteristic appearance in certain
species of Combreturn, Macropteranthes, Terminalia, Bucida and Quisqualis, for instance.
In Combreturnzenkeri Engl. & Diels the epidermal papillae have a conspicuously echinate
cuticle, a unique feature in the Combretaceae.

GENERIC SURVEYS

In this section under each of the 18 genera are noted those epidermal features which
have been found to be useful in identification or classification, followed by a statement
 The sigiziJicunce of the leaf epidermis in the taxonomy of the Combretaceue 235
on the variability within the genus and an indication of the extent to which specific
delimitation can be made on the basis of epidermal characters alone. Finally an assess-
ment is made of the relevance of the epidermal features to a n understanding of the
intergeneric relationships of each genus.
The number of species present in each genus is given in brackets after the heading;
in cases where a n approximate figure appears a world-wide taxonomic revision of the
genus has not been undertaken in recent years. The geographical range of each genus
is also stated; all the Combretaceae are tropical or (in a very few cases) subtropical.

1. Strephonema ( 5 s p p . , in tropical West Africa)

All 5 species were examined

Midrib and lateral veins discernible on epidermides ; upper midrib primarily composed
of shorter than broad cells ; venule reticulum not represented on epidermides. Epidermal
cells characteristically irregularly shaped, often with very acute angles, with tightly
undulate walls, the undulations sometimes restricted to the outer part of the wall.
Domatia revoluta present in all species, variously developed. Leaves hypostomatic ;
stomata with or without T-pieces (T-shaped thickenings at the stomata1 poles), with
2 paracytic subsidiary cells (Pl. 1, fig. 5 ) .I n all species the subsidiary cells are subdivided
t o some extent so that up to 5 or more of the latter adjoin each stoma. This is particularly
the case in S.mannii Hook. f. (incl. S.tessmannii Mildbr.) and S.gilletii de Wild., where
the paracytic nature of the subsidiary cells is thus partly obscured. The only hairs
present in S.mannii s.1 are typical compartmented hairs, although the internal com-
partment is apparently rudimentary or not present in a few of the hairs of most specimens
(Text-figs. 5 , 6). The typical hairs of the other 4 species, on the other hand, are unicellular,
two-armed, and very short stalked. I n S. gilletii, S. sericea Hook. f. and S. pseudocola
A. Chev. (incl. S.apolloniensis J. J. Clark) the 2 arms of the hairs are very long and
pointed with lumina which extend for a high proportion of their length, and where the
2 arms meet the typical internal compartment is clearly visible extending into each
(Text-fig. 11). I n S. plybotryum Mildbr., however, the 2 arms are in general much
shorter and broader, and the lumen often falls far short of their extremities. Moreover
no internal compartment is to be seen (Text-fig. 12). Some specimens labelled S. poly-
botryum, however, possess two-armed hairs of the same type as in S.sericea, etc.
The latter 4 species are much more densely pubescent than is S.mannii s.l., vhere
hairs are extremely sparsely scattered over the vegetative and floral regions, being most
common on the sepal margins. There is thus a possibility that tS.pical one-armed com-
partmented hairs do exist very sparsely in the 4 species with two-armed hairs, and in
fact in 1 specimen of S.gilletii a few normal one-armed hairs were found on the sepal
margins. Extensive examination of the other 3 species. however, has failed to reveal
their presence.
As a genus Strephonema is quite distinct from the rest of the Combretaceae in its
revolute domatia, characteristic pattern of epidermal cells, paracytic subsidiary cells
and two-armed hairs, none of which is found elsewhere in the family. Indeed, very few
epidermal similarities are to be found between the 2 groups, and in the past Strephonema
has been assigned to several other families. The presence of typically Combretaceous
compartmented hairs in a t least 2 species is thus of great significance, and the two-
armed hairs of the remaining species can easily be visualized as derivatives of the
one-armed type. Heiden (1893) noted similar two-armed hairs in Corncarpus, but this
observation is considered by the writer to be an error, probably of identification. Heiden
also remarked that compartmented hairs with a rudimentary second arm in the form
of a rounded bulge were to be found in various Terminulia species, but these types are
 236 CLrVE A. STACE
common in several genera (Text-fig. 1) and are unlikely to be directly related to the
two-armed hairs of S t r e p h m a .

Figs. 13-27. Scale-Trichomes of the Combretaceae. Figs. 13-16. Calycopterw jloribunda.

Fig. 17, Guiera senegalensis. Figs. 18, 19, Thiloa glaucocarpa, normal scales. Figs. 20, 21, T .
paraguariemk. Fig. 22, T . glaucucarpa, normal scale. Figs. 23, 24, T . glaucocarpa, abnormal
long-stalked scales from midrib. Fig. 25, Combrelurn binderianum. Fig. 26, C. apiculatum.
Fig. 27, C. capituliflorum. Figs. 16 and 22, vertical sections of scales in situ; Figs. 23, 24,
side views of detached scales; the rest vertical views. Camera lucida drawings.

2 . Combretum (Over 600 names but probably only about

250 s p p , throughout the tropi'cs except Australia)
About 150 species were examined.
With regard to most epidermal characters Combretum shows a wide range of structure
which makes i t very difficult to define this large genus. All the species examined, how-
ever, lack hydathodes or similar structures, possess anomocytic stomata, and have
 The significance of the leaf epidermis in the taxonomy of the Combretucem 237
typical compartmented hairs. Domatia are usually absent, though domatia marsupi-
formia or fasciculata are present in a number of species. Besides the compartmented
hairs glandular trichomes are also present. I n about two-thirds of the species these are
scales, and in the rest stalked glands (Text-figs. 35, 4 0 4 ) . I n addition 1 species, C .
apetalum Wall. ex Kurz, possesses both.
The structure and arangements of the scales and stalked glands have been found to
be of the greatest value in the taxonomy of Combretum, and this is the subject of the
second paper in this series. The major scale-types of Combretum, however, are of sig-
nificance t o an interpretation of the other lepidote genera of the Combretaceae. The more
complex scales are of 2 main types: those in which the dividing cell-walls are mostly
or wholly radial (Text-fig. 27) ; and those in which they are both radial and tangential
t o roughly equal degrees (Text-fig. 2 5 ) . I n the former types the cells are thus much
longer and narrower and there are more of them a t the circumference of a scale of a
given size than in the latter types. I n the simpler scale-types the number of dividing
cell-walls is reduced to varying degrees, the simplest types having just 8 cells radially
arranged (Text-fig. 26). Every intermediate stage can be found from the simple eight-
celled types to the complex radial-walled types on the one hand and to the complex
radial-tangential-walled types on the other. I n Combretum the cuticular membrane of
the scale may or may not be raised from the cell-plate.

3. Pteleopsis (About 12 spp., in trop’cul Africa)

Five species were examined.
Midrib, lateral veins and venule reticulum well defined on both epidermides. Epidermal
cells straight- or slightly undulate-walled. Domatia present in only 1 species, and there
marsupiform. Stomata almost confined t o lower epidermis ; rather large and with
usually well-developed T-pieces, anomocytic. Typical compartmented hairs the only
trichomes present’.
The 3 species examined proved easily separable on epidermal characters, and whilst
there is a distinct possibility that the sample taken was not sufficient to cover all degrees
of variation the same is true at the macroscopic level of several species which are im-
perfectly known, and the following key does a t least show the type of interspecific
variation encountered.
1 Hairs present on midrib, veins and venules of both epid., and very sparsely t o quite
frequently in the areolas . . 2
Hairs frequent on midribs and sometimes on major lateral veins of 1. epid., but ex-
tremely sparse or absent elsewhere . . 3
2 Hairs rare in areolae and sometimes absent from those of u. epid.; hair-bases (incl.
poral rims) up to 30 p across on 1. epid. midrib P. my7ti,foZia (Laws.) Engl. & Diels
Hairs frequent in areolae of both epid. : no hair-bases over 15 p across .
P.suberosa Engl. & Diels
3 Marsupifom domatia present: cells of both epid. with straight or almost straight walls
P. aniaoplera (Welw. ex Laws.) Engl. & Diels
Domatia absent : cells of both epid. or of 1. epid. only conspicuously undulate-walled . 4
4 Cells of both epid. undulate-walled; u. epid. cells rarely over 25 p across .
P. hylodendron Mildbr.
Cells of 1. epid. only undulate-walled: u. epid. cells commonly 20-30 p across .
P. diptera Engl. & Diels
Pteleopsis is notable as being the only genus of the Combreteae lacking glandular
trichomes of any type. This Terminalian feature is paralleled by certain macroscopic
characters, e.g. the andromonoecious flowers, which are also not found elsewhere in the
Combreteae. The genus Pteleopsis is not separable from Terrninalia and related genera
on one or a finite number of epidermal characters, although each species is probably
distinguishable from these genera individually.
238 CLIVE A. STACE

Figs. 28-45. Glandular Trichomes of the Combretacem. Figs. 28, 29, C a b p y x i s eriantha.
Figs. 30, 31, Quisqualb indica. Fig. 32, Q. latialata. Fig. 33, Q. littoren. Fig. 34. Q. hensic
Fig. 35. Combreturn aculeatum. Figs. 36,_37, Conocarpw erectus. Figs. 38, 39, Thiba gracilia.
Fig. 40, Cotnbre-hm smeathmannii. Fig. 41, C . oxystachyum. Fig. 42, C. cacoucia. Fig. 43,
C. platypterwn. Fig. 44, C . grandi-m. 45, Le-?gxd&.a racemosa. Figs. 35 and 45,
vertical axtions of gGn& in situ, the rest side views of detached glands. Camera lucida
drawings.

4. Quisqualis (17 spp., in tropGxl Asia and tropical South Africa)

Exell (1931) divided Quisqualis into 4 sections*: Combretop7sis ( Q . hensii (Engl. &
Diels) Exell, examined) ; Campybgyne (Q. exannulata (0. Hoffm). Exell, examined) ;
* Exell & Strtce (1964) now consider that Q . henSii is best re-transferred to the genus Cotnbretum,
full reasons for the change being presented in that publication. For the sake of completeness, however,
C. hensii Engl. & Diels is here treated under Quisqualb.
 The signijcance of the leaf epidermis in the i k m m n n y of the Combretuceae 239
Sphalanthus (11 species of which Q. latialata (Engl. ex Engl. & Diels) Exell, Q. littorea
(Engl.) Exell, and Q. prostrata Craib were examined) ; and Quisqmlis (4 species of which
only Q. indica L. was examined).
Midribs and lateral veins always and venule reticulum usually well defined on both
epidermides. Upper epidermal cells straight- to very markedly undulate-walled ; lower
always variously undulate-walled. Domatia often present, always marsupiform. Leaves
hypo- or amphi-stomatic ; stomata without subsidiary cells or conspicuous cuticular
thickenings. Cuticle very strongly striated in Q. hensii, weakly so or not in the other
species. Compartmented hairs and stalked glands (Pl. 1, fig. 8) always present, and in
Q. hensii the young leaves densely covered with thin-walled, non-compartmented, uni-
cellular hairs also (Text-figs. 8, 9). The latter fall off the leaves a t maturity, however.
Q. indica is an extremely variable species, chiefly with regard to the cell-wall undula-
tion, the stomata1 distribution, the abundance of compartmented hairs, the size of the
hair-bases, and the anatomy of the stalked glands. This variation is paralleled by
macroscopic features. Since the range of structure in Q. indica overlaps that of most of
the other less variable and geographically more restricted .species, reliable separation
of species using epidermal characters cannot often be carried out. Q. hensii, however, is
very distinct from all the other species in its possession of non-compartmented hairs and
strongly striated cuticle when the leaves are young, although these characters are not
present on older leaves. It is, however, equally distinct from all species of Combretum.
The structure of the glands of this genus varies considerably. The head may be com-
posed of rather few tiered cells, or of many untiered cells; and the stalks may be short
and uniseriate or long and multiseriate. I n Q. indica the glands (Text-figs. 30,31) always
have multicellular untiered heads, but the stalks may be of either of the above 2 types,
or absent. I n the 4 species examined of sections Sphalanthus and Campylogyne the gland
heads are all paucicellular and tiered, and the stalks short and uniseriate (Text-fig. 33) ;
thus these 2 sections can apparently always be distinguished from section Quisqualis.
Q. hensii possesses glands of the Sphalanthus-type (Text-fig. 34) mixed with long multi-
seriate-stalked Quisqualis-types and some intermediates, and thus is also distinct.
On the basis of trichome structure the 4 sections of Quisqmlis thus form 3 groups.
Quisqmlis as a genus, however, cannot on epidermal characters be delimited from those
species of Combretum which possess stalked glands as well as compartmented hairs, and
indeed many species of Quisgwtlis have been included in Combretum in the past.

5. Guiera ( 1 sp., G. senegalensis Lam., in Africa)

Midrib and lateral veins distinct on both epidermides, but venule reticulum only on
lower epidermis. Upper epidermal cells distinctive, with usually few, straight walls
(usually only 3 or 4 but up to 6) often meeting at very acute angles. Areas in centre of
lower epidermal areolae sunken, with small undulate-walled cells ; non-sunken areas with
cells as on upper epidermis. Domatia present, marsupiform. Stomata almost all in
sunken areas of lower epidermis, small (up to 20 p long) and more or less circular, without
thickenings, anomocytic. Typical compartmented hairs (Text-fig. 2) abundant on upper
epidermis, on non-sunken parts of lower epidermis and on sides of sunken areas, but
sparse in sunken areas. Scales (Text-fig. 17) present in sunken areas, usually only one
per area, filled with very dark glutinous substance secreted between cell-plate and the
raised cuticular membrane, divided by radial walls only, more or less circular, c. 12-20
cells around margin, c. 80-140 p diam.; scale-base conspicuous, the stalk inserted into
the epidermis.
Guiera is a t once recognizable by its distinctive upper and lower epidermal cells, its
numerous very short compartmented hairs, and the scales. I n its possession of the last
Guiera resembles Combretum, Thiloa and Calympteris, and its relationships presumably
lie with these genera. Its scales, however, are quite distinct from any of those in the
17
240 CLIVE A. STACE
latter genera. They resemble those of Combreturn and T h i h rather than those of
Calycopteris in that the stalk is inserted into a pore in the epidermis, but Calywpteris
and Combrdum pro parte in that the cuticular membrane is raised from the cell-plate.

6. Thiloa (3 spp., in tropical S o d America)

Only 2 species were available for full examination.
Midrib, veins and venule reticulum well represented on both epidermides. Epidermal
cells conspicuously undulate-walled. Domatia marsupiformia present, large and con-
spicuous. Stomata almost confined to lower epidermis, without thickenings, anomocytic.
Hairs of all types apparently absent. Scales (Pl. 1, fig. 7) present on both epidermides,
mostly on lower, their cuticular membrane not raised from cell-plate, divided by radial
and tangential walls, rather irregular in shape, c. 15-45 cells around the margin, c 75-150
p diam.; stalks inserted into an epidermal pore, forming a conspicuous scale-base.
The scales of all 3 species were examined, when 2 distinct types were found, corres-
ponding with the 2 major types of scale-division noted in Combreturn. The radial-walled
types were present in T. praqmriensis Eichl. (incl. T . inunduta Ducke), and the radial-
tangential-walled types in T. glauwcurpu (Mart). Eichl. (incl. T. stigmaria (Mart.)
Eichl.) and T. gracilis (Schott) Eichl. (incl. T. nitida Eichl. and T . colombianu Dugand
t Exell). This character is obviously of considerable taxonomic importance in the
genus, although it is not correlated with other useful features such as the presence of
a caruncle on the anthers. The 2 species examined fully, T. gracilis and T . glaucocarp,
appeared almost identical on epidermal characters apart from the greater abundance
of scales in the latter. Also of note is the fact that all specimens fully examined possess
a few scales, on or near the midribs, with very long though basically uniseriate stalks
(Text-figs. 23, 24). These stalks are up to 40 cells and 400 p in length, whereas normal
scale-stalks of this and other genera are up to about 4 cells and 10 p long. In addition
all specimens of T.gracilis s.1. possess stalked glands with globular multicellular heads
and medium to long stalks (Text-figs. 38, 39), these being absent in the other 2 species.
They provide an additional and very useful means of identification. Similar glands
have also been found in a few American species of otherwise scale-bearing Combreturn.
The scales of Thiloa differ from those of Calywpteris in that the stalk is inserted into
an epidermal pore (Text-fig. 22), and from those of both Cuiera and Calycopteris in that
the cuticular membrane is not raised from the cell-plate. The apparent absence of
compartmented hairs from all vegetative parts of the plant is very remarkable, but the
hairs found on the floral disk and interior of the upper hypanthium are of the typical
compartmented type.
Thiloa is undoubtedly closely related to Combreturn, and the epidermal structure
supports this view. It is not possible to separate the 2 genera on one or a combination
of epidermal characters, although the particular combination of features in T . gracilis
and T . gla-rpa have not been seen in Combreturn.

7. Calopyxis (About 18 spp., endemic to Marlrcgascar)

Only C. eriantha Tul. could be examined.
Midrib, veins and venule reticulum well developed on both epidermides. Epidermal
cells with straight or very slightly undulate walls. Domatia marsupiformia present.
Leaves hypostomatic; stomata without thickenings or subsidiary cells. Typical com-
partmented hairs and stalked glands (Text-figs. 28, 29) present; stalked glands the
more abundant, with short uniseriate stalks and small, paucicellular, few-tiered heads.
Although the genus has been revised recently almost all the species are insufficiently
known, and a further, critical revision is needed.
 The signijicance of the leaf epi&ermisin the taxowmy of the Combretaceue 241
Macroscopic examination and perusal of the literature of other species suggests that
the presence of the stalked glands is a constant generic character. Calopyxis thus falls
close to those species of Combretum which bear stalked glands, and whilst C. erianthu
differs from any species of Combretum examined i t seems unlikely that the 2 genera
are separable as such on epidermal characters.

8. Terminalia (About 400 names, perhaps about 200 spp., pantropical)

Twenty-nine species were investigated microscopically. Mhny taxonomic problems
remain in the genus, and it has never been satisfactorily classified into subgenera and
sections (Exell, 1954).
Like those of the even larger genus Combretum species of Terminalia are extremely
variable with regard to most of their epidermal characters, so that a useful inclusive
description of the genus cannot be given. The stomata, however, are always anomocytic
(Pl. 1, fig. 3), and the only trichomes present are typical compartmented hairs. Domatia
may be absent, or if present either marsupiform or lebetiform. A survey was undertaken
macroscopically on all 160 species of Terminalia available with the following results:
domatia absent in 110, marsupiform in 16 and lebetiform in 34 species.
Of the 29 species investigated microscopically 2 ( T . mollis Laws. and T . suberosa
R. E. Fr.) were identical but the other 27 were easily distinguished on cuticular charac-
ters alone. The 2 former taxa, in fact, together with the epidermally distinct T . torulosa
F. Hoffm., have recently been treated as 1 species (Griffiths, 1959). I n Combretum the
most important taxonomic epidermal characters are the trichomes, the epidermal cells
and stomata being relatively constant in structure, although they do show a considerable
range of variation in the whole genus. I n Terminulia, on the other hand, the only
trichomes to be found are the virtually invariable compartmented hairs, the epidermal
cells and stomata, etc., providing many more taxonomic characters than in Combreturn.
This ‘shift of emphasis’ is paralleled in macroscopic features, for in Combretum the
flowers provide most of the diagnostic characters, the fruits being much less variable,
whilst in Terminalia the opposite is the case.
The 28 of the 29 Terminalia species were easily separated by means of the following 10
characters, in each of which from 2 to 5 categories were recognized:
(i) Cuticular membrane thickness and cuticular JEange development on upper epidermis:
A--Cuticular membrane very thin; cell outlines not or only fragmentarily visible;
B-Cuticular membrane thin; cell outlines faint but most or all visible;
C-Cuticular membrane medium thickness ; cell outlines all conspicuous;
D-Cuticular membrane thick ; cell outlines very conspicuous and broad.
(ii) Undulation of upper epidermal anticlinal cell-walls:
A-Walls very strongly undulate ;
%Walls conspicuously though not very strongly undulate ;
&Walls slightly and variously undulate, some merely curved or even straight;
D-Walls straight or some curved.
(iii) Undulation of lower epidermal anticlinal cell-walls:
The same 4 categories as under (ii).
(iv) Prominence of ve1u)u.s system on upper epidermis:
A-Venule reticulum strongly developed and raised above the areolae ;
B-Venule reticulum always present, never raised, conspicuous or not ;
&Midrib, lateral and lesser veins present, but venules not joining up t o form a
reticulum ;
D-Midrib, major lateral and a few secondary veins visible only.
242 CLIVEA. STAGE
(v) Prominence of venom system on lower epidermis:
The same 4 categories as under (iv).

(vi) Stornatal distribution on upper epidermis:

A-Absent, or sparse alongside and/or on the midrib;
B-Frequent along midrib and major lateral veins, rarely extremely sparse elsewhere ;
&Frequent by venous system and often in the areolae (and then sometimes absent
from the venous system) but always much less abundant than on lower epidermis;
D-Present to an equal or nearly equal extent on both epidermides.

(vii) Type of stomata as seen on cuticular membrane:

A-Epidermal walls of guard-cells invisible to faint; T-pieces more or less absent;
poral walls scarcely thickened; outer stornatal ledge absent;
B-Epidermal walls conspicuous ; T-pieces present ; poral walls somewhat thickened ;
outer stornatal ledge usually present.

(viii) Distribution of hair-bases (average of 2 epidermides) :

A-Extremely sparse, if present confined to midribs and major lateral veins, but
sometimes abundant around the domatia;
B-Frequent on midribs and major lateral veins, absent to very rare elsewhere;
&Frequent to abundant on midribs and veins, quite to very frequent on venules
and sometimes sparsely present on non-venous areas.

(ix) Type of hair-base :

A-Small (rarely over 15 p diam., including poral rims); rims not to fairly well
thickened; adjacent cells unmodified to slightly radially elongated ;
B-Larger (c. 10-50 p diam.); rims usually conspicuous; adjacent cells usually
radially elongated but rarely unmodified;
&Large (many 50 p or more diam.) ; rims conspicuous, adjacent cells very small
and numerous and usually not radially elongated.

(x) Type of domatiurn (almost always primary-axillury in psition).

A-Absent ;
B-Marsupiform, shallow and V-shaped with long pointed ‘arms’;
C-Marsupiform, V-shaped with very short or no ‘arms’;
D-hbetiform, opening over half the &am. of the domatium;
E-Lebetiform, opening under half the diam. of the domatium.
The results are shown in Table 1.

Among the 29 species examined was Termidiopsis tetrandru Danguy (1923), which
Exell (1931) included in Terminulia. Whilst recognizable as M e r e n t from any of the
other species examined, T . tetrundrus is not separable from Terminalia as a whole on
epidermal characters. The same, however, is also true of other genera closely related
to Terminalia, e.g. Ramatuella, Bucida and Buchenuvia, and thus this similarity should
not be used as evidence for or against the inclusion of Terminaliopsis in Terminalia.
Considerable difficulty is sometimes encountered in distinguishing sterile material of
Terminalia and Combretum (cf. Exell, 1931); the absence or presence respectively of
glandular trichomes, however, will always indicate the correct genus, although
macroscopic examination alone is inadequate.
 The sign$cunce of the leaf epidermis in the taxonomy of the Combretaceae 243

Table 1. Summary of the major epidermal chnrncfers

of 29 species of Terminalia

(See text for explanation)

- .r c t
5

c,

archboldinnu Esell , . .. C A c A A B C d A B
brownii Fresen. .. .. A. B C A B B C C D x
bursarina F. Nuell. .. .. E d C A C-D C D D D C
catuppa L. .. .. .. E h C h B B C B-C A A
chebula Retz. .. .. Al -1-B B h A B B-C D D B
chicharronia Wright ., .. h -1 A A A B B C D C
citrina (Gaertn.) Roxb. e s Flem. -4 d B A d B-C B-C A-B B B-C
glabrescens Mart. .. .. E A C A A C C A A C
grandi$ora Benth. .. . I D A Al A D C D C C C
hypargyrea K. Schum. Br Laut. D *A C A B B C C C B
intricata Hand.-hIazz. .. -1 c c A x B B C C A
latipes Benth. .. .. B B C A C B B-C D D A
laxijora Engl. 8r Diels .. d A B .
1 A
. B D D D D
~tnelnnocarpaF . Nuell. .. D A A A A B B-C D B D
microcarpa Decne .. .. E A C A B C C B A-B
mollis Laws. .. .. B A C x A A C D D 1)

moluccana Lam. , . .. c A c -A A B-C C D D B

witens Presl .. .. E A A B C D D X B D
oreadum Diels .. .. c -4 c -1, C B C C D c
pellucida Presl , . .. c A A B -1 B-C C C C A
phanerophlebin Engl. & Diels B B C A C B C B-C B-C B
plngata Men-. .. .. D A B-C A A B B-C B A B-C
pterocarpn F. Muell. .. .. E X B A D B-C C D D C
sepicana Diels .. .. c A C x A B C c c B
sogerensis Bak. f . .. .. E B C A B B B-C B B B-C
suberosa R. E. Fries , . .. B d C A A h C D D D
torulosa F. Hoffm. , , .. B A c A B A c D C-D C
triptern Stapf .. .. A A-B A 9 €3 B-C A-B B B
Terminaliopsis tetrandrus , . Al A B B A-B c c B B C
244 -
E A. STAGE

9. Bucida (About 7 spp., i n tropical Central and northern South America)

Three species were examined.
Midrib, veins and venule reticulum conspicuous on lower epidermis, very much less
so on upper epidermis. Epidermal cells strongly undulate-walled, sometimes with well-
developed cuticular striations. Domatia absent. Stomata mostly confined to lower
epidermis, without thickenings, anomocytic. Compartmented hairs usually sparse, no
other types of trichomes present. Apparent water-stomata sometimes present.
The 3 species examined are alike in general leaf morphology, and do not represent the
full range of the genus in this respect. B. bueeras L. differs from B. angustifolia DC. and
B. sp'msa (Northrop) Jennings in that the cuticular membrane is conspicuously striated
and some stomata are present on the upper epidermis. In the first 2 species the stomata
are oblong, c. 25 x 15 p, but in B. s p h s a they are often almost circular, e. 20 x 15-20 p.
Bucida i s not distinguishable from Terminalia on epidermal characters and the 2
genera are obviously closely related.

10. Buchenavia (24 spp.,* tropical and subtropical Central and South America)
Fifteen species were examined.
This is the third largest genus in the Combretaceae, and considerable variation in
epidermal characters is to be found, so that a useful generic description cannot be
compiled. Hydathodes, etc., and trichomes other than typical compartmented hairs
(text-figs.3,4) are absent. The stomata are anomocytic. Twenty-three species were exam-
ined with regard to their domatia: these are marsupiform in 13 species (Pl. 1, fig. 1);
lebetiform in 1; and absent in 9. In many cases routine identification of species can be
facilitated by an examination of the domatium structure, as is the case in Terminalia.
All species examined could be distinguished on epidermal characters alone, and a key
is given which indicates the most important characters in this respect. I n many cases,
however, very few specimens were examined (frequently very few exist), and the key
should therefore be used with caution. It is evident, however, that 4 main groups of
species may be recognized: with marsupiform domatia and slightly raised venation
system (species 2-10); as the last but with labetiform domatia (species 1); without
domatia and with the venous system not a t all raised (species 11-12); and without
domatia and with the lateral veins very strongly raised, the venule reticulum not too
very strongly raised (species 13-15). The last group was under-represented in the
sample.
1 Conspicuous primary -axillary domatia present . . 2
Domatia absent . . 11
2 Domatia very conspicuous and deep, some or a l l with openings narrower than the
widest part of the domatium (lebetiform); venule reticulum very indistinct on both
epid. . 1. B. famkawei Exell & Mapire
Domatia mamupiform; venule reticulum nearly always conspicuous a t leaat on 1. epid . 3
3 U. epid. cells straight- or inconspicuously undulate-walled, small (c. 20 p across);
domatie rather small and shallow . . 4
U. epid. cells strongly undulate-walled, or if not then 30-40 p across; domatia large and
oftenvery deep . . . 5
4 Venules on u. epid. narrow but distinct, on 1. epid. broad and conspicuous 2. B. huberi Ducke
Venules on u. epid. & indiscernible, on 1. epid. narrow . . 3. B. crericocarpa Ducke
5 U. epid. midrib very namow, almost glabrous; cells of u. epid. not very conspicuously
undulate-walled . . 4. B. ochroprumna Eichl.
U. epid. midrib usually broader, with 4 or more hairs per 500 p length; u. epid. cells
various . . 6

* This number may now be reduced to 22: B. huberi is the same as B. grandis Ducke, and B. di8cOhJr
Diels (the only species not examined microscopically)is the same aa B. ochroprumna.
 The signi$cance of the leaf epidermis in the taxonomy of the Combretaceae 245
6 U. epid. midrib rather sparsely pubescent, with up to c. 20 hairs per 500 p length . 7
U. epid. midrib densely pubescent, with usually over 30 hairs per 500 p length . . I0
7 Hair-bases mostly over 15 p diam., thin-rimmed; u. epid. midrib very narrow .
5. B. punctata Eichl.
Hair-bases almost all under 15 p diam., often thick-rimmed; u. epid. midrib not very
narrow . . 8
8 Domatia very deep . . 9
Domatia shallow . . 6. B. acunzinata Exell & Stace
9 Cells of u. epid. slightly undulate-walled; venule reticulum inconspicuous; cuticular
membrane thick; cell outlines very distinct 7. B. parvifolia Ducke
Cells of u. epid. very conspicuously undulate-walled; venule reticulum conspicuous;
cuticular membrane rather thin; cell outlines not very distinct 8. B. oxycarpa (Mart.) Eichl.
10 Domatia several per leaf, all large and deep . 9. B. capitata (Vahl) Eichl.
Domatia few per leaf, mostly rather shallow . . 10. B. kkinii Exell
11 L. epid. lateral veins and venules narrow and not raised; lvs. very slightly pubescent
apart from midribs; 1. epid. cells nearly all straight-walled . 11. B. suaweokns Eichl.
& 12. B. pterocarpa Exell & Stace
L. epid. lateral veins broad and raised; lvs. slightly to densely pubescent apart from
midribs; 1. epid. cells conspicuouslyundulate-walled, or if not then venule reticulum on
1. epid. also wide and raised . . 12
12 L. epid. venule reticulum not or scarcely raised: 1. epid. cells mostly over 35 p across,
strongly undulate-walled; hairs rather sparse on 1. epid. apart from midrib and lateral
veins . . 13. B. nzacrophylla Eichl.
L. epid. venule reticulum broad and raised; 1. epid. cells mostly under 30 p across,
straight- to strongly undulate-walled; hairs frequent to abundant on 1. epid. apart from
midrib and lateral veins . . 13
13 L. epid. cells conspicuously undulate-walled; hairs frequent; hair-base often over 30 p
across . . 14. B. callistachya Ducke
L. epid. cells straight- or slightly undulate-walled; hairs abundant; heir-bases rarely
over 15 p across . 15. B. reticulata Eichl.

Buchenavia is not separable from Terminalia on epidermal characters, and shows the
same type of variation. Indeed, specimens without flowers cannot be placed in their
correct genus on any characters.

11. Ramatuella (6 spp., in tropical South America)

All 6 species were examined.

Midrib and lateral veins conspicuous but venule reticulum never represented on
epidermis. Epidermal cells characteristically with walls undulate in the outer part only.
Domatia absent. Stomata very abundant on lower epidermis, frequent near midrib on
upper epidermis, large, comparatively broad, with T-pieces and conspicuous outer
stornatal ledges, retuse a t the poles, anomocytic. Typical compartmented hairs with
asymmetric bases the only trichomes present. Cuticular membrane and flanges strongly
developed.
With regard to epidermal characters the 6 species fall into 3 groups:
1 Lower epidermis very densely pubescent, with silvery hairs . . R. argentea Kunth
Lower epidermis in general sparsely pubescent. . . 2
2 Lower epidermis rather densely pubescent on and near the midrib in basal parts of
thelamina . . R. crispialata Ducke C R. obtwa (Maguire) Exell & Stace
Lower epidermis sparsely pubescent throughout . R. Zrirem Spruce ex Eichl.,
R. maguirei Exell & Stace t R. latifololia Maguire

These 3 groups coincide with those recognizable on macroscopic characters, except

that on the latter basis R. maguirei forms a 4th group.
Ramtuella is a small group of closely related species which are not distinguishable
macroscopically or microscopially from Terminalia on a single character, but which in
both instances are recognizable by a combination of such characters.
246 CLIVEA. STACE
12. Conocarpus (2 or 3 spp., in tropical and subtropical America and Africa,
and in Arabia)
All 3 taxa were examined.
Midrib and lateral veins well developed but venules not discernible on epidermides.
Epidermal cells stright-walled. Hydathodes, etc., usually absent, but sometimes a few
apparent water-stomata present. Domatia lebetiformia present, very large and con-
spicuous (Pl. 1, fig. 2). Stomata almost equally abundant on 2 epidermides, not sunken,
anomocytic; outer stornatal ledge conspicuous; T-pieces absent. Typical compartmented
hairs (Text-fig. 1) very scarce to very abundant. Small stalked glands (Text-figs. 36, 37)
present sparsely on both epidermides, borne on trichome-bases with small, thick-walled
adjacent cells. Cuticular membrane and flanges strongly developed.
C. erectus L. var. erectus and var. sericeus Forsstr. ex DC. ( = C. sericeus (Forsstr. ex
DC.) G. Don) are very easily distinguishable since the leaves of the former are very
sparsely and of the latter very densely pubescent. Apart from this feature the 2 taxa
differ by other very minor epidermal characters. Little material of C. lancifoliw Engl.
& Diels was available for study, but the epidermis is extremely similar to that of C.
erectus var. erectus. C. erectus is a well-known mangrove of tropical West Africa and
tropical America, whereas C. lancifolius is a shrub of wet sandy soils in north-east
Africa and Arabia. Thus it is of some taxonomic importance that the 2 species are
extremely similar or perhaps identical in epidermal anatomy (Stace, 1963).
C o n ~ ~ a r p uiss easily distinguished from all other genera on epidermal characters.
The presence of stalked glands is of considerable importance since these are not found
in other genera of the Terminalieae. They are slightly different in structure from those
of genera of the Combreteae, and thus may not be homologous with them. Nevertheless
the possession of glandular trichomes by Conocarpus is a complete anomaly. Few
epidermal characters appear to connect C0nocarpu.s with the Terminalieae rather than
with the Combreteae, presumably due to the extreme leaf modifications in this man-
grove genus. The conspicuous lebetiform domatia, however, are not found in any
Combreteae but are common in Terminulia.

13. Anogeissus (About 12 s p p . , in tropicul Africa and Asia)

Six species were examined.
Midribs, lateral veins and venule reticulum represented on both epidermides. Upper
epidermal cells straight- or undulate-walled; lower straight-walled. Domatia marsupiform
or, more usually, absent. Stomata on upper epidermis very sparse to as abundant as on
lower epidermis, without thickenings, anomocytic. Typical compartmented hairs the
only trichomes present; hair-bases often very large and with many adjacent cells. Cuti-
cular membrane usually thin, with ill-developed cuticular flanges.
The 6 species examined can be separated by means of the following key with regard
to the material which was available, but once again the possibility must be noted that
this sample might not represent the true ranges of the species.
1 Most u. epid. cells markedly (though not strongly) undulate-wdled . . 2
Nearly aJl u. epid. cells straight-walled, but sometimes undulate-walled in small
patches . . 4
2 Stomata frequent alongside u. epid. midrib, and not uncommon elswhere on u. epid .
A . acuminata (Roxb. ex DC.) Wall. ex Bedd.
Stomata absent or rare on whole of u. epid . . 3
3 Cuticular membrane extremely thin and fragile; venule reticulum rather ill-defined,
especially on u. epid. ; 2 epid. subequally pubescent, margin slightly more so; domatia
absent . . A . peidula Edgew
Cuticular membrane fairly thin; venule reticulum well defined on both epid. ; u. epid.
conspicuously more pubescent than 1. epid., margin more so than either; domatia
present . . A . schimperi Hochst. ex Hutch. & Dalz.
 The signi’cance of the leaf epidermis in the taxonomy of the Combretaceae 247
4 U.epid. sparsely pubescent t o almost glabrous; 1. epid. also rather sparsely pubescent
A . latifoZia (Roxb. ex DC.) Wall. ex Bedd.
Both epid. densely pubescent . . 5
5 Two epid. conspicuously different; stom. rare on u. epid., usually confined to region
of midrib d. c w o m t u Stapf
TTO epid. rather similar; stom. very common on u. epid, almost as frequent as on
1. epid. . A . bentii Bak.

A nogeissus possesses no notable epidermal features, and on such is not distinguishable

from Terminalia by any finite combination of characters. Its morphology strongly
suggests a close relationship t o Conocarpus, in which it was once included, but the
epidermal characters scarcely indicate this. It differs markedly in its poorly developed
cuticular membrane, lack of lebetiform domatia, and lack of glandular trichomes. The
tendency t o possess numerous stomata on the upper epidermis, however, may show a
connexion with Conocarpus, and the fact that the 2 genera occupy totally different
habitats might explain the absence of other similarities.

14. Finetia (1 sp., F. rivularis Gagnep., in Indo-CJtina)

Midrib, veins and renule reticulum well represented on both epidermides. Epidermal
cells on both epidermides undulate-w-alled, those on lower less so. Domatia absent.
Apparent hydathode-like areas present on lower epidermis. Stomata very sparse on
upper epidermis, small, with no thickenings, anomocytic. Typical compartmented hairs
the only trichomes present.
Einetia is undoubtedly very closely related t o Anageissus, and its epidermal characters
could be said to corroborate this view. There are, however, no major features of its
epidermis that can be used t o separate Finetia from other genera such as Terminalia
and Buchenavia, although F . riwluris can be separated from all species of those 3
genera by its particular combination of characters.

15. Calycopteris (Getonia) (1 sp., C. floribunda (Rozb.)

Lam. (G. floribunda Roxb.), f
romIndia to Indo-China)
Midrib, veins and venule reticulum well developed on both epidermides. Epidermal
cells of both epidermides straight-walled, except under the scales on lower epidermis
undulate-walled. Domatia very slightly developed, marsupiform. Stomata small, with
no thickenings, anomocytic, confined t o undulate-walled-celled areas. Typical compart-
mented hairs present. Conspicuous scales (Text-figs. 13-16) present, c . 35-110 p across,
circular but slightly scalloped a t margin, divided into c. 8-24 elongated cells by radial
walls alone, or less often by a few tangential walls also; cuticular membrane raised and
with yellowish secretion between it and cell-plate; stalks very short, 1 cell long, up to
4 cells wide; scalebase ill-defined, the stalk not inserted into epidermis.
The relationships of Calycopteris have never been fully understood, and Engler &
Diels (1899) placed the genus in a separate tribe. I n the possession of scales it resembles
the genera Guiera, T h i l m and Combreturn, although the latter three differ in that their
scale-stalks are inserted into epidermal pores, whereas in Calycopteris the stalks are
situated on the top of the epidermis (Text-fig. 16). The scales themselves, however, and
indeed the whole epidermis (particularly the epidermal cell shape) are very similar to
those of Guiera, and the evidence from epidermal studies is that the Calycopterideae are
not distinct from the Combreteae.
Near the midrib on the upper epidermis are usually to be found a very few glandular
trichomes which either represent small modified scales or are stalked glands. Due to their
scarcity and state of preservation, however, their anatomy could not be elucidated.
248 CLIVE A. STACE
16. Lumnitzera (2 spp., in the Old World tropics from
East Africa to Australia)
Both species were examined.
Only midrib represented on both epidermides. Epidermal cells all with straight walls,
not secondarily subdivided. Water-stomata and hydathodes not infrequent on both
epidermides. Shallow pits on leaf-margin are said to be domatia. Margin, as in all pre-
ceding genera, composed of several regular rows of rectangular, elongated cells with
angular lumina. Stomata, slightly more abundant on upper than on lower epidermis, not
or slightly sunken, more or less randomly orientated, without T-pieces but with well-
developed outer stornatal ledges, cyclocytic with (3-) 4 (-5) regular subsidiary cells
(Pl. 1, fig. 4).Trichomes absent or extremely sparse, only compartmented hairs present.
Cuticular membrane thick, with stongly developed 5anges.
The 2 species, L. racemosa Willd. and L. littoreu (Jack) Voigt, can be separated with
certainty by the appearance of the stomata as seen in vertical transverse section (Stace,
1963), and less accurately by a number of other epidermal features. Otherwise the
2 species are indistinguishable on any vegetative characters, so that epidermal studies
are here of some importance.
The 2 species are well-known mangroves and share a number of features in common
with Cmocarptu and Laguncularia, the other 2 genera of Combretaceous mangroves.
Lumnitzera is, however, easily distinguished from all other genera of the family by
means of epidermal characters alone. It differs from Conocarptu in particular in the
absence of the lateral venous system on the epidermides; the presence of cyclocytic
subsidiary cells; the absence of stalked glands; the absence of the typical domatia;
and in the presence of hydathodes. Thus there appears to be good evidence from epidermal
studies for placing Lumnitzera and Conocarpm in separate tribes.

17. Laguncularia (2 spp., in tropical and subtropical

America and West Africa)
Both species were examined.
Only midrib represented on both epidermides. Epidermal cells all with straight walls,
often secondarily divided by very thin walls. Water stomata and hydathodes present
but very sparse on both epidermides. Domatia absent. Margin composed of small
unaligned cells with round lumina. Stomata often slightly more abundant on upper
than on lower epidermis, very slightly sunken, those on the upper epidermis orientated
a t right angles to the midrib, without T-pieces but with well-developed outer stornatal
ledges, cyclocytic with (3-) 4 (-5) regular subsidiary cells. Compartmented hairs present.
Dome-shaped apparently sessile glands (Text-fig. 45) deeply sunken in very narrow-
apertured pits present on both epidermides. Cuticular membrane and 5anges strongly
developed.
The 2 species, L. racemosa Gaertn. f. and L. glabri$ora Presl., are indistinguishable on
epidermal characters, and in fact may be conspecific.
This genus resembles Lumnitzera most closely on the basis of both epidermal and
macroscopic characters. It differs, however, in the secondarily divided epidermal cells ;
the type of marginal cells; the shape and orientation of the stomata; the presence of
more or less seseile sunken glands; and in the absence of marginal domatia. All these
characters, however, apart from the presence of glands, are of relatively minor sig-
nificance, and do not argue against the inclusion of the 2 genera in 1 tribe. The glands
are of great taxonomic importance, being unique in the family. Since their homology
is obscure they cannot be taken as indicating any particular intergeneric relationships.
The ‘numerous submarginal pits (domatia?)’ referred to by Graham (1964) are in fact
the glandular pits, any connexion between these and true domatia being entirely con-
jectural.
 The significance of the leaf epidermis in the tuxonomy of the Corabretacae 249
18. Macropteranthes (4 s p p , endemic to North and North-East Australia)
All 4 species were examined.
Only midrib differentiated on upper epidermis, only midrib or major lateral veins
as well on lower. Epidermal cells all straight-walled, or those on lower and some on
upper epidermis undulate-walled. Domatia absent. Hydathodes, etc., absent or very
rare. Margin composed of several rows of slightly elongated, rectangular cells with
angular lumina. Stomata present only on lower epidermis to equally distributed on
both epidermides, with no thickenings, anomocytic. Typical compartmented hairs
present, very sparse t o abundant. I n M . leichhardtii alone very large, thin-walled,
non-compartmented hairs also present (Text-fig. 10). Glandular trichomes absent.
Cuticular membrane often strongly striated parallel with midribs and margin, and
radially to stomata and trichome-bases.
The 4 species are separable into 3 groups on the basis of epidermal characters, as in
the following k e -
1 Stomata equal15 abundant on the 2 epidermides; cuticle extremely conspicuously
striated . . X.kekwtckzz F. Muell. & M. montanu ( F Muell.) F. Muell.
Stomata absent or very sparse on the upper epidermis; cuticle not or onlv sllghtly
striated . . 2
2 Hairs abundant on 1 epid., frequent on u. epid.; nearly all cell-walls straight; a few
large, thin-walled, non-compartmented h a m present . M leichhardttz F. Muell.
H a m very sparse on both epid.; some cell-walls, a t least on 1 epid., conspicuously
undulate; all hairs compartmented . -If jtuzlnnzi F. JIuell
M. nwntanu and X.kekwickii appear to be indistinguishable on leaf characters. The
leaves of M . Jitzalunii are much larger and less pubescent, have stomata only on the
lower epidermis, hare the lateral veins often discernible on the lower epidermis, have
conspicuously undulate-walled lower epidermal cells, and have no cuticular striations.
M . leichhurdtii is intermediate between these 2 groups possessing some characters of
each. I n addition it possesses very long, thin-walled non-compartmented hairs 1%hich
are unique in the Combretaceae.
Unlike the other 2 genera in the Laguncularieae Macropteranthes species are not
mangroves, but shrubs of dry scrub or creek-sides. It is not surprising, therefore, that
the leaves show considerable differences from those of h m n i t z e r a and Laguncularia.
I n all 3 genera, however, axillary domatia are absent, stomata are present on both
epidermides to roughly equal extents (not so in 2 species of Macropteranthes), stalked
glands and scales are absent, the epidermal cells are straight-walled (except in 111.
jititzalanii), and the midribs are the only part of the venous system discernible on the
epidermides (though the lateral veins also are distinguishable on the lower epidermis
in 2 species of Macropteranthes). From its reproductive organs Nacropteranthes would
seem to be very closely related to Lwmnitzeru, and the epidermal characters certainly
support rather than refute this. The main points of difference are the anomocytic
stomata of iMacropteranthes, and the absence of stomata on the upper epidermis of 2
species and the presence of undulate cell-walls in 1 species of that genus. AS with the
ConocarpslAnogeissus situation, the totally different habitats occupied by the genera
probably accounts for the lack of more epidermal similarities.

K E Y TO THE EPIDERMIDES O F THE GENERA O F COMBRETACEAE

The following key brings out the differences between the epidermides of the Com-
bretaceous genera, but also shows that not all the genera can be separated by these
means. It does, however, serre as a summary to Section 3.
1 Stomata basically paracytic, the 2 subsidiary cella sometimes subdivided; hairs, if
present, either one-armed or two-armed and either compartmented or non-compart-
mented; domatia revoluta usually present . . Strephonetna
Stomata basically anomocytic, with ( 3 ) 4 or more adjacent cells; two-armed hairs
absent; domatia revoluta absent . 2
250 CLIVE A. STACE
Upper epidermis showing at the most only the midrib of the venous system; frequently
only this present on lower epidermis also . . 3
At least some veins as well as midrib evident on upper epidermis . . 5
Stomata anomocytic; hairs abundant on both epidermides or if sparse then stomata
present only or almost only on lower epidermis . Macropteranths
Stomata cyclocytic; hairs very sparse to absent on both epidermides; stomata
abundant on both epidermides . . 4
Secondary division of epidermal cells evident ; conspicuous deeply-sunken glands
present on both epidennides; margin composed of small, unaligned cells with rounded
lumina . . Laguncularia
Secondary division of epidermal cells absent; glands absent; margin composed of rec-
tangular, usually slightly elongated cells arranged in longitudinal files . Lurnnitzera
Compartmented hairs the only types of trichomes present .
Terminalia, Anogeissus, Pteleopsis, Buchnavia, Bwida, Finetia & R a m a t u e l b
Glandular trichomes present, sometimes very sparsely . . 6
Scales present, sometimes with stalked glands also . . 7
Scales absent ; stalked glands present . . 9
Scale stalks not inserted into epidermal pore ; scale-bases very inconspicuous Calycopteris
Scale stalks inserted into epidermal pore; scale-bases very conspicuous , . 8
Scales GUed with blackish secretion between cell-plate and cuticular membrane, con-
f h e d to shallow depressions in lower epidermal areolae . . Guiera
Scales iilled with secretion between cell-plate and cuticular membrane or not, but
secretion never very dark; scales rarely sunken in lower epidermal depressions only .
T h i b a & Combreturn p.p.
Conspicuous primary-axillary lebetiform domatia present . . Conoca.rpus
Domatia, if present, marsupiform . Combreturn p.p., Cabpyxis & Quisqwlis

DISCUSSION

The Combretaceae pose a number of interesting phylogenetic and taxonomic problems,

and i t is evident from the preceding data that in a considerable proportion of cases
epidermal studies may be of some importance in their elucidation.
Of particular interest is Strephonema, which differs from the rest of the family in its
semi-inferior ovary and which was originally placed in the Lythraceae. The genus has
other unique features in its paracytic subsidiary cells, revolute domatia, and two-armed
hairs. Of greatest importance, however, is the possession of typical Combretaceous one-
armed compartmented hairs by a t least 2 species, indicating the affinity of this genus
with the Combretaceae. Consequently, the treatment of Strephonema as a separate sub-
family of the Combretaceae is strongly supported by epidermal characters.
The 4 tribes of the Combretoideae are much less distinct. The Laguncularieae are
more easily circumscribed on macroscopic characters than are the other 3 tribes but
this scarcely applies to the epidermal features, perhaps because two of the genera are
mangroves and the third not. However the lack of scales or stalked glands and the
absence of a distinguishable lateral venous system on the upper or both epidermides
are constant features of all 8 species, and the latter character is not found ekewhere in
the family, even in Conomrpus which is a mangrove showing many similarities to
Lumnitzera and Lagunculuria. Within the Laguncularieae the 3 genera are easily separa-
ted on epidermal characters, although those of Macropteranthes are very variable from
species to species.
The other 3 tribes are not separable by a single or even a few macroscopic characters,
but (at least in the case of the Combreteae and Terminalieae) represent groups of genera
showing a tendency to possess a certain combination of features. The same is true of the
epidermal characters. The Combreteae in general have multicellular glandular as well
as unicellular non-glandular trichomes, whilst the Terminalieue tend to possess the latter
only. On this basis there are 2 anomalous genera: Pteleopsis, a member of the Com-
breteae without glandular trichomes; and C o n o c a r v , a glandular member of the
Terminalieae. Any other feature used to separate the 2 tribes, e.g., presence of petals
or andromonoecious flowers, has a similar or greater number of exceptions, and the
 The sigiziJicance of file leaf epidermis in the taxonomy of the Combretame 151
position of a genus in one tribe or the other must always be assessed on a combination
of all available characters. Thus the use of epidermal anatomy does not suggest a re-
classification of the tribes Combreteae and Terminalieae, but provides a number of
additional characters 1% hich enables a precise definition of each tribe to be made more
easily.
The position of the Calycopterideae is problematical. Calycopteris is distinguishable
from all the other genera of the Combretaceae by either macroscopic or epidermal
characters, but this is no less true of several other genera and there does not seem to be
sufficient evidence for creating a separate tribe for Calycopteris. It certainly does not
form a group as distinct as the Combreteae and Terminalieae, but obviously falls much
closer to the former as it possesses glandular scales. It appears to be advisable t o unite
the Calycopterideae and Combreteae.
Combretum and Terminulia are 2 large genera exhibiting a very wide range of structure,
and many of the other genera in the same tribes differ only very slightly. Buchenavia
and Terminulia, for instance, differ only on one or two minor floral characters, so i t is
not particularly surprising that no differences exist in their epidermal anatomy. The
ranges of epidermal features of many of the smaller genera are quite narrow and easily
defined, but in several cases are overlapped by those of the larger genera, so that the
genera cannot always be separated on epidermal characters alone. This applies more
to the Terminalieae, since here the glandular trichomes which are diagnostically so
important in the Combreteae are lacking. However, even in the former tribe epidermal
characters are often extremely useful in identification at specific and generic levels, and
in adding to the pool of taxonomic information which can be used in constructing a
classification of maximum usefulness.

ACKXOWLEDGEMENTS

This work was carried out in the Department of Botany, British Xuseum (Natural
History), with the assistance of a Research Studentship from the D S.I.R., to both
Departments of which I wish to express my thanks. I am especially indebted to Dr
A. W. Exell for his interest throughout the xork, and for his valuable help and dis-
cussion a t all stages.

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EXPLANATION OF PLATE 1
All are cuticular preparations.
Fig. 1. Mamupiform domatium of Buchenavia capitata. x 75.
Fig. 2. Lebetiform domatium of Conocarpua erectwr var. sericeus. x 75.
Fig. 3. Anomocytic stomata of Teminaliopsis tetrandrus. x 500.
Fig. 4. Cyclocytic stomata of Lumnitzera r a c e m a . x 500.
Fig. 5. Paracytic stomata of Strephonema sericeum. x 500.
Fig. 6. Internal compartments of compartmented hairs of Macropteranthes kekwickii. x 500.
Fig. 7. Scale of Thiloa glawocarpa. x 500.
Fig. 8. Stalked gland of Quisqualis henaii. x 500.