Botanical Journal of the Linnean Sociery ( 1993), 113: 227-262. With 15 figures
Contribution of vegetative anatomy to the
systematics of the Zygophyllaceae R.Br.
M. C. SHEAHAN AND D. F. CUTLER F.L.S.
Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS
Received February /993, accepted for publication July /993
SHEAHAN, M. C. & CUTLER, D. F., 1993. Contribution of vegetative anaton1y to the
syste01atics of the ZygophyUaceae R.Br. The Zygophyllaceae sensu lata are a heterogeneous
family of trees, shrubs and herbs growing in arid and semi-arid areas of the world. There has been
disagreement about the systematic status of some groups within the family, and the position of
Balanites has also been disputed. The vegetative anatomy of the family was examined to see if it
could throw light on current systems of classification. The anatomy of 37 species in 19 genera is
described, and the results of tests of C, activity in 27 species are given. There is anatomical evidence
to support the exclusion of Balanites into a separate family, and some groups (Engler's Peganoideae
and Nitrarioideae) have characteristics which set them apart from the rest of the family. This is in
accordance with other analyses of the family based on morphological, palynological and
biochemical studies. There is also evidence that the tribuloid genera Tribulus, Kallstroemia and
Kelleronia should be separated from the zygophylloid genera, at least at subfamily level; however,
.Neoluederit;;.ia and Sisyndite should remain in the Zygophylloideae. Brief reference is made to
relationships with other families in the Geraniales.
ADDITIONAL KEY WORDS:- Balanites- C, plants- Kranz anatomy- stomata- tracheoidsvenation - vestured pits
CONTENTS
Introduction .
Previous anatomical investigations.
Taxonomic problems .
Material and methods.
Results
Characters of taxonomic value
Anatomical descriptions .
Results of carbon dioxide compensation point tests.
Discussion
Anatomical features .
Taxonomic implications
Concluding remarks
Acknowledgements
References
227
229
229
231
233
233
236
252
253
253
255
259
260
260
INTRODUCTION
The Zygophyllaceae are a family of some 24 genera of plants adapted to semidesert and Mediterranean climates, which grow in arid, semi-arid and saline
areas throughout the tropics and subtropics.
0024-4074/93/011227 + 36 $08.00/0
227
© 1993 The Linnean Society of London
228
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
The systematic relationships within the family have been the subject of
disagreement for many years. Engler's ( l896a, 1931) full accounts have
dominated subsequent treatments of the family; but more recently, investigations
of the morphology, palynology, cytology and biochemistry have shown it to be
very heterogeneous. Hutchinson ( 1967) was atypical in finding it homogeneous.
Engler ( 1931) divided the family into seven subfamilies, each composed of
tribes and subtribes. He regarded the genera in his subfamily Zygophylloideae
(which included <:Jgophyllum) as the central, typical group; the Peganoideae,
Chitonioideae (now generally known as Viscainoideae), and Tetradiclidoideae
were placed at the beginning of his treatment of the family, differing from the
Zygophylloideae mainly in having alternate rather than opposite leaves.
Nitrarioideae and Balanitoideae were put at the end. These also have alternate
leaves, and are further distinguished by their drupaceous rather than capsular or
schizocarpic fruits. This arrangement was followed by Scholz ( 1964) and
Hegnauer (1973), among others. However many (e.g. Hutchinson, 1967, 1973;
Van Tieghem, 1906) considered that Balanites constitutes a different family, and
some (e.g. Dahlgren, 1980; El Hadidi, 1975; Takhtajan, 1980, 1983) have also
considered some of the other outlying groups to be sufficiently different to be
given family status (Table I). The position of the Zygophyllaceae in relation to
other plant families has also been subject to disagreement. Table l shows that
the family has been placed at different times in no fewer than five different
TABLE I. Taxonomic treatments of the Zygophyllaceae
Name
Order
Engler, 1931
Willis, 1931
Lawrence, 1960
Scholz, 1964 (Engler's Syllabus)
Cronquist, 1968
Geraniales
Geraniales
Geraniales
Geraniales
Takhtajan, 1969
Geraniales
(but connected to Rutales)
Hutchinson, 1973
Malpighiales
(derived from Tiliales)
El Hadidi, 1975
Heywood, 1978
Dahlgren, 1980
Cronquist, 1981
Takhtajan, 1980, 1983
Sapindales
Geraniales
Polygalales
Geraniales
Family
Zygophyllaceae (incl. Balanites)
Zygophyllaceae (incl. Balanites)
Zygophyllaceae (incl. Balanites)
Zygophyllaceae (incl. Balanites)
Zygophyllaceae
Balanites in Simaroubaceae
Zygophyllaceae
Peganaceae
Nitrariaceae
Balanitaceae
Zygophyllaceae
Balanitaceae
Zygophyllaceae
Nitrariaceae
Tribulaceae
Balanitaceae
(Tetradic/is & Peganum to be excluded)
Zygophyllaceae (incl. Balanitaceae)
complex
Zygophyllaceae
Nitrariaceae
Peganaceae
Balanitaceae
Sapindales
Zygophyllaceae
(possibly with Balanitaceae/NitrariaceaefPeganaceae as satellite families)
Rutales
Zygophyllaceae (incl. Peganaceae)
Nitrariaceae
Balanitaceae
(Tetradic/is to go in Rutaceae)
M. C. SHEAHAN AND D. F. CUTLER
229
orders, though the consensus is that it is most closely related to families in the
Geraniales.
Previous anatomical investigations
The anatomy of some species of the family was discussed in the classic works
on anatomical aspects of adaptation to xeric habitats Oonsson, 1902; Sabnis,
1920; Volkens, 1884, 1887; Zemke, 1939). Pantanelli (1900) examined the
physiological anatomy of many members of the family, and some genera were
included in Chermezon (1910), Haberlandt (1914) and Solereder (1908).
Gamaley (1984) studied some of the Zygophyllaceae (species of ,Qgophyllum,
Nitraria, and Peganum) in his work on the morphology and anatomy of plants in
the Gobi desert. The anatomy of some individual genera and species has also
been studied; for example Balanites (Parameswaran & Conrad, 1982; Van
Tieghem, 1906); .<,. fabago (Cunningham, 1927); Larrea (Barbour et al., 1977;
Runyon, 1934); Peganum harmala (Elgin, 1950); .<,. album (Montasir & Foda,
1955); Tetraena mongolica (Vasilevskaya & Petrov, 1964); Fagonia (El Hadidi,
1966); Plectrocarpa (Castro, 1981); Bulnesia (Glaser de Banus, 1981).
Taxonomic problems
Here the taxonomic problems arising from Engler's ( 1931) subfamilies will be
considered in turn. The characters uniting and separating the groups within the
family are summarized in Tables 2 and 4.
The Peganoideae comprise two genera, Peganum and Malacocarpus. Takhtajan
( 1969) put these genera in their own family Peganaceae, but in 1980 he returned
them to the Zygophyllaceae. Dahlgren ( 1980) assigned them to a separate family
Peganaceae, and El Hadidi (1975) also thought that they should be kept apart.
It has been suggested that they show more affinity with the Rutaceae; for
example, the pollen grains have some characters in common with those in
Rutaceae (Erdtman, 1952). However, Peganum does not have a close relationship
to any of the Rutaceae (Engler, 1896b), and in particular it lacks the lysigenous
TABLE
2. Engler's diagnostic characters for subdivision of the Zygophyllaceae
Leaf
Fruit
Peganoideae
alternate, much divided
Chitonoiodeae
(Morkillioideae)
Augeoideae
alternate, simple or
imparipinnate
opposite, simple, clavate
Zygophylloideae
opposite, simple or
pinnate
opposite, pinnate
alternate, simple
undivided
alternate, bipinnate
berry-like, or loculicidal
capsule
septicidal capsule, one
or many seeded
septicidal capsule, 1-2
seeded
loculicidal, septicidal, or
schizocarpic
schizocarpic
drupe with hard-seeded
kernel
drupe with hard-seeded
kernel
Tribuloideae
Nitrarioideae
Balanitoideae
Endosperm
+
+!+!-
230
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
oil glands characteristic of that family. Furthermore, other studies have drawn
attention to similarities between the pollen of zYgophyllum and Peganum (Xi &
Zhou, 1989, 1992).
The Morkillioideae Rose & Painter (Engler's Chitonioideae) include the three
genera Morkillia, Viscainoa and Sericodes, which are similar to the Zygophylloideae
in features of flower and fruit; however Engler separated them from the
Zygophylloideae on account of their alternate branching and imparipinnate
leaves.
The Tetradiclidoideae are represented by a single low-growing species with
small succulent lobed leaves, Tetradiclis tenella, which has caused some
puzzlement to taxonomists. El Hadidi (1975) thought that this species, with
Peganum and Malacocarpus, should be excluded from the Zygophyllaceae because
of morphological and biochemical differences. Takhtajan (1980) included it in
the Rutaceae. Unfortunately, desiccated herbarium material was too delicate to
allow anatomical examination.
Engler (1896a, Appendix) listed Augeoideae as a separate subfamily, with
Augea capensis as the sole member. Convinced of the greater similarity of its seed
and fruit characters to those of zYgophyllum, he included it in the subtribe
Zygophyllinae within the Zygophylloideae (1896b). However, in Engler (1931),
which was published posthumously, Augea was left as it appeared in Engler
(1896a), in its own subfamily Augeoideae. El Hadidi (1975) recommended that
it should be placed within the Zygophylloideae.
The Zygophylloideae form the largest subfamily. zYgophyllum is the type genus
of the family, and also the largest, with about 80 to 100 species. Close to it are
(among other, smaller genera) Fagonia in the Old World, and Bulnesia, Porlieria,
Larrea, and Guaiacum in the New.
Engler ( 1931) put Trihulus and Kallstroemia, with Kelleronia, Neoluederitzia and
Sisyndite, into the tribe Tribuleae within the Zygophylloideae. Porter ( 1974)
thought that Tribulus, Kallstroemia, Kelleronia and Tribulopis (the Australian genus
which is considered by many to be congeneric with Trihulus) should be moved
into their own subfamily Tribuloideae, but that Neoluederitzia and Sisyndite
appeared to belong with Larrea in the Zygophylloideae. El Hadidi (1975, 1977)
proposed a new family Tribu1aceae, based on Engler's tribe Tribulae. He
divided this family into two subfamilies, Tribuloideae (containing Tribulus,
Kallstroemia, Kelleronia and Tribulopis) and Neoluederitzioidae (containing
Neoluederitzia and Sisyndite). He considered that this group showed many
differences from the Zygophylloideae; these were chiefly that the zygophylloid
type is woody, with opposite, stipulate leaves, dehiscent capsules and
endospermic seeds, while the tribuloid type is mainly herbaceous, with alternate
exstipulate leaves, indehiscent mericarps and non-endospermic seeds. There is
also palynological evidence for the separation (Descole et al., 1940; Praglowski,
1987), and there are biochemical differences (Saleh et at., 1982).
The single genus Nitraria, placed by Engler ( 1931) in its own subfamily
Nitrarioideae, is considered by many to be sufficiently different from the rest of
the Zygophyllaceae to warrant inclusion in its own family Nitrariaceae (for
example Dahlgren, 1980; Takhtajan, 1969, 1980). Nitraria differs
morphologically in having simple, alternate, fasciculate leaves, distinctive pollen
(Agababyan, 1964; Xi & Zhou, 1989), and drupaceous rather than capsular or
schizocarpic fruits. There are also biochemical differences (Hegnauer, 1973;
M. C. SHEAHAN AND D. F. CUTLER
231
Saleh eta!., 1982), and differences in flower structure (Ronse Decraene & Smets,
1991 ).
Engler ( 1931) put Balanites in a subfamily Balanitoideae, but the position of
this species in relation to the Zygophyllaceae has long been a source of
disagreement. Originally regarded as a distinct family, Balanitaceae, Delile
(1813) and de Candolle (1824) put it in the Zygophyllaceae, chiefly because of
the bipinnate leaves which resemble those of many zYgophyllum. Bentham &
Hooker (1862) thought it was closer to the Simaroubaceae and included it in
that family, but Engler (1896a Appendix; 1931) returned it to the
Zygophyllaceae, as a separate subfamily. Later it was assigned to its own family:
Van Tieghem (1906) considered that there were three genera constituting a
separate family Agialidaceae, but most have considered it a monogeneric family
Balanitaceae (Hutchinson, 1973; Parameswaran & Conrad, 1982; Takhtajan,
1983). Cronquist ( 1968) put Balanites in the Simaroubaceae, but according to
Hegnauer (1973), Balanites is not chemically similar to the Simaroubaceae
because it lacks the quassia-like alkaloids typical of that family. Scholz (1964)
and Hegnauer ( 1973) both included Balanites in the Zygophyllaceae, as did
Cronquist ( 1981). There are biochemical similarities beween Balanites and
Zygophyllaceae; Maksoud & El Hadidi ( 1988) did not think that these disagreed
with the treatment of Balanites as a distinct family, but in the opinion of
Narayana et al. ( 1990) they indicate that Balanites should remain within the
Zygophyllaceae.
The vegetative anatomy of several members of the family was examined in the
hope of clarifying the taxonomic relationships within the family. Brief
anatomical descriptions are given, and the diagnostically important anatomical
characters are discussed to see what light they cast on the taxonomic problems
outlined above, and also, briefly, on the position of the Zygophyllaceae in
relation to allied families.
The type of photosynthesis was also investigated, as the Zygophyllaceae are
among the relatively few families ( 18 according to A pel, 1988) containing both
C 3 and C 4 members, and Crookston & Moss ( 1972) thought that an indication of
relationships might be provided by finding out which were C 4 plants. All living
species available were screened for evidence of the C 4 assimilation pathway, by
measuring their C0 2 compensation point (Das & Raghavendra, 1973; Downton
& Tregunna, 1968; Tregunna et al., 1970); in addition, leaves were examined for
the presence or absence of Kranz anatomy (W elkie & Caldwell, 1970).
MATERIAL AND METHODS
Living plants were necessary for tests of C 4 activity; most of these were grown
from seed, but in a few cases (species of Guaiacum, Porlieria and Bulnesia) live plant
material was used from the Royal Botanic Gardens, Kew. In all, 19 genera and
37 species were examined. When there was no other source oflive or freshly-fixed
material for anatomical investigation, dried Herbarium specimens from R.B.G.
Kew were used. However, the leaves of the many succulent and semi-succulent
members of the family had become so shrunken and distorted on desiccation that
anatomical investigation was not possible. A list of the species examined,
together with the sources of material obtained, is given in Table 3.
232
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
TABLE 3. Sources of materials
Species
Peganoideae
Peganum karma/a L.
Malacocarpus crithmifolius (Retz.) Fischer
& C. Meyer
Morkillioideae
Morkillia mexicana (Mo~ifto & Sesse) Rose
& Painter
Viscainoa geniculata (Kellogg) E. Greene
Augeoideae
Augea capensis Thunb.
Zygophylloideae
Fagonia moll/is Del.
,Qgophyllum album L.
coccineum L.
darvasicum Boriss.
dumosum Boiss.
eremaeum (Diels) Ostenf.
eurypterum Boiss. & Buhse
fabago L.
fontanesii Webb & Berth.
kaschgaricum Boriss.
oxianum Boriss.
simplex L.
stapffii Schinz
xantho;rylum Engl.
Bulnesia arborea Oacq.) Engl.
Guaiacum guatema/ense Planchon Rydb. &
Vail
qjficinale L.
sanctum L.
Porlieria chi/ensis I. M. Johnston
hygrometra Ruiz Lopez & Pavon
Larrea tridentata (Sesse & Mo~ifto ex DC.)
Cov.
Pintoa chilensis C. Gray
Plectrocarpa rougesii Descole, O'Don. &
Lourt.
.!Veo/uederit;:,ia sericeocarpa Schinz
Siryndite spartea E. Meyer ex Souder &
Harvey
Tribuloideae
Kallstroemia grandij/ora Torrey ex A. Gray
T ribulus terrestris L.
;:,eyheri Souder
Source
Reference no.
I. Tblisi BG
2. RBG Kew
3. RBG Kew
Tashkent BG, Uzbekistan, USSR
R 85 19(321)
417-70-04037
65 7-68-00459
R 87 12
s
s
RBG Kew (coli. McKee, Puebla,
Mexico)
I. Mildred E. Mathias BG, USA; w.coll.
Baja California
2. RBG, Kew (coli. Carter & Kellogg,
Chile)
11037
D
2945
National BG, Kirstenbosch, SA
SA 87 II
Tel Aviv, Israel; w.coll.
Kew, Wakehurst Place
Orman BG, Giza, Cairo
Pamir BG, USSR, w.coll.
Jerusalem Univ., Israel, w.coll. Tzin
heights
Perth BG, Australia
Leningrad BG, USSR
I. Tenerife BG, Canaries
2. RBG Kew
Tenerife BG, Canaries
Leningrad BG, USSR
Lesnaia, Kishinev, USSR
I. El Hadidi, Cairo, w.coll. Helwan
desert
2. Jerusalem University, Israel
Dept. Agr., Pretoria, SA
RBG Kew (from Gansu Agricultural
University, China)
RBG, Edinburgh
Honolulu BG, Hawaii
I 87 08
9687 7610027
E 86 07
R 85 23(355)
s
s
s
s
I 87 SL454
A 85 18(303)
R 86 3077
Ca 85 17(242)
083-33-0830 I
Ca 85 22(242)
R 86 3387(85)
R 86 06
s
s
s
s
s
s
s
s
E 86 05
I 87 13
SA 86 03
s
s
s
396-84-04134
696299
H 87 FL-70
s
I. Honolulu BG, Hawaii
2. RBG, Kew
3. RBG, Kew (Puerto Rico)
National BG, Cuba
RBG, Kew (Chile University)
RBG, Kew
California, w.coll.
us 83
#5442
H 87 16
361-61-36103
20372 LOC WI
c 87 15
102-71-01063
000-73-12398
Ca 85 17 (208)
RBG, Kew (coli. Reed, Atacama, Chile)
leaf only
RBG, Kew (coli. Palacios eta!.,
Tucuman, Argentina) leaf only
I. SWA Herbarium, Windhoek, SWA
w.coll. Fish River
2. RBG, Kew (coli. Engler, Namaland,
SWA) stem only
Dept. Agriculture, Pretoria, SA
Phoenix, Arizona, w.coll. Pima County
I. Arizona, US, via HDRA
2. Tel Aviv, Israel
Dept. Agriculture, Pretoria, SA
F
s
s
D
S,F
F
s
s
F
D
s
F
F
s
D
1682
D
SWA 88 16
s
6620
SA 86 02
D
us 87 10
us 85 00
s
s
s
s
I 87 09
SA 86 OJ
s
233
M. C. SHEAHAN AND D. F. CUTLER
TABLE
Species
Ni trarioideae
Nitraria retusa (Forsskal) Asch.
3. --continued
Source
Reference no.
I. Beer Sheva, Israel, w.coll. Eilat
I 86 7654
s
only
I. Perth, Australia
2. Pamir BG, USSR, w.coll.
20374 LOC WI
R 85 20(303)
R 85 21(355)
D
Beer Sheva, Israel, coli. Eilat
Dept. Agriculture, Pretoria, SA
I 85-200
SA 86 04
s
s
2. RBG Kew (coli. Jordan Plain) stem
schoberi L.
Balani toideae (Balani taceae)
Balanites aegyptiaca (L.) Del.
maughamii Sprague
s
s
S = seeds; F = fresh plant material; D = dried plant material; BG = Botanic Garden; RBG = Royal
Botanic Gardens; HDRA =Henry Doubleday Research Association; SA= South Africa; SWA =South West
Africa; w.coll. = wild collected.
For light microscopy, leaf and stem material was fixed for 24 hours in FAA,
and sectioned with a Reichert sliding microtome. Herbarium material was
swelled and softened by boiling before sectioning.
Sections were routinely stained with safranin and Alcian blue, and mounted in
'Euparal'. Scarlet R was used to test for lipids and cutin; and iodine in potassium
iodide for starch. Fragile and succulent material was embedded in paraffin wax
Qohansen, 1940) or acrylic resin (Feder & O'Brien, 1968) and cut either on a
Reichert 4020 rotary microtome or on a Cambridge Huxley Mark 2 ultramicrotome. Leaf clearing was normally according to Foster (1953); but very
succulent or delicate leaves were treated by the method of Kurth ( 1978).
Epidermal peels were also made when possible.
Slides were viewed with a Wild M20 binocular light microscope with camera
Iucida attachment.
Carbon dioxide compensation points (r) were measured at Imperial College,
London, on an Analytical Developments Type 225-Mark II infra-red gas
analyser, using a form of the rapid screening method of Goldsworthy & Day
(1970).
RESULTS
Characters of taxonomic value
Some anatomical characters are common to all the species studied. In the leaf,
stomatal guard cells have an outer ledge and thickened upper and lower walls
(Fig. IE). In the stem, the cells of the phellem have thin suberized walls (Fig.
14), and the phloem sieve elements are narrow (diameter 5-8!J.m). The xylem
forms a complete cylinder early; vessel elements are narrow and short with
simple perforations and minute alternate bordered pits, ends transverse to
oblique. Axial parenchyma is fusiform, sometimes with cross walls.
Other characters are found in most of the species studied, and only departures
from the usual state are mentioned in the descriptions:
( 1) Leaf venation is mainly of two types. In leaves and leaflets with
reticulate,
pinnate,
is
venation
lamina,
flattened
dorsiventrally
brochidodromous; leaflets of pinnate leaves often asymmetric (Fig. 3). Areole
development is incomplete or imperfect, irregular in shape and size (Fig. 2D, E;
terminology from Hickey, 1973). This is called type A in the descriptions.
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
234
0
100 fLm
E
l25
,J
(
IJ.m
[sao 11m
r-.,....--,---1
parenchyma
chlorenchyma
collenchyma
phloem
xylem
sclerenchyma
Figure I. A-D. Trichomes on leaf (all to same scale): A, <)gophyllum eurypterum: lobed trichomes in
adaxial surface view. B, Kallstroemia grandiflora: raised trichome base (adaxial). C, Peganum harmala:
multicellular trichome at base of young leaf. D, Viscainoa genicula/a: unbranched unicellular trichome
(abaxial). E-F, TS leaflets. E, Guaiacum r!fficinale: abaxial epidermis. F, Z· album: arrangement of
tissues.
235
M. C. SHEAHAN AND D. F. CUTLER
100 J.Lm
E
Figure 2. A-C. Adaxial leaf epidermis (all to same scale). A, Peganum harmala showing elongated
epidermal cells. B, ,Qgophyllum coccineum. C, Viscainoa genicula/a. D-F. Venation (all to same scale). D,
Nitraria retusa showing tracheoids at veinlet terminations; the mid vein is at the bottom, with a lateral
branching from it. E, Bulnesia arborea: leaflet margin. F, Plectrocarpa rougesii: very dense tracheoids at
leaflet apex.
236
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
(2) In centric leaves and leaflets there is a central primary vein which divides
towards the apex. One or two secondary lateral veins run parallel to it, which
branch off to form a peripheral network of higher order veins, with xylem
external to phloem. This is called type B (Fig. IF).
(3) Dilated tracheids (tracheoids) associated with higher order veins and veinlet
endings; especially thick at the margin and apex (Figs 2D, F; 8).
(4) Anomocytic stomata (Figs 2B, C).
(5) Straight unbranched unicellular trichomes, with tapering apex; narrowing
towards the base, and widening again slightly at the foot (Fig. ID). Sometimes
such trichomes emerge from a basal plinth or rosette of raised epidermal cells
(Fig. IB).
( 6) Thin leaf cuticle ( ~ I Jlm) .
(7) Absence of Kranz anatomy.
(8) Circular stem in transverse section.
Some anatomical features in the family are liable to phenotypic modification,
and may have evolved in response to environmental pressures, especially water
stress. These include, for example, the size and form of the leaf, and the relative
amounts of palisade, spongy mesophyll and water storage tissue within it; in the
stem, the thickness of vessel and fibre walls, lignification of rays and
parenchyma, tertiary helical thickening of vessel walls, clustering of vessels,
narrow vessel diameter, and the presence of vasicentric tracheids (Carlquist,
1988).
The following characters were found to be most useful for distinguishing taxa.
(I) Leaf vasculature, trichome type, stomatal type, epidermal cell shape, the
presence or absence of Kranz anatomy, mucilage cells and type of crystal.
(2) Stem: the orientation of stomata, and arrangement and type of
sclerenchyma in the cortex.
(3) Xylem: vessel arrangement, presence or absence of vestured intervascular
pits, type of imperforate element, arrangement of axial parenchyma, and ray
width.
A summary of the chief distinguishing features for each group is given in
Table 4.
Anatomical descriptions
Peganum ( Peganum harmala)
Leaf venation. 2° veins branching off towards the end of each linear segment,
parallel to I o vein; marginal ultimate venation looped; areoles elongated. Sparse
veinlet termination tracheoids, single or in clusters, inside areoles.
Leaf surface. Bands l-2 cells wide of large epidermal cells considerably
elongated in direction of axis (length: width=8: I), alternating with wider
bands of only slightly elongated (3 : 2), more irregular cells (Fig. 2A). Stomata
large, found only in bands of shorter, irregular epidermal cells. Trichomes at
base of young leaves (Fig. I C), c.I50 Jlm long; multicellular, caducous, capitate.
Lamina in TS. Outline (Fig. 5): leaf segments narrow, some nearly centric;
slightly flattened with shallow adaxial depression; lamina thick (c.400 Jlm).
Epidermis irregular; elongated cells larger than ordinary cells. Mesophyll radial;
central part oflamina occupied by large colourless thin-walled cells surrounding
veins. Vascular bundles forming an arc; midrib in proximal part of leaf with a
Venation
Trichomes
Stomata
Epidermal
cell shape
unicellular;
straight or
clavate,
warty
unicellular,
straight
type A
type A
zygophyllaceous
I double, I
single arc
Balanitoideae
petiole absent areoles
elongated
Nitrarioideae
Peganoideae
anomocytic, polygonal
a few
paracytic/
weakly
actinocytic
anomocytic, polygonal
actinocytic,
paracytic
absent
absent
present
simplex)
z.
absent
(except
in
absent
solitary or
in radial/
tangential/
dendritic
chains
fibre strands,
solitary or
in short
scanty
brachysclereids radial
chains
solitary or
fibre strands,
in radial
lignified
clusters or
parenchyma
chains; 2
size classes
solitary or
fibre strands,
in short
outer ring of
brachysclereids radial lines
or clusters
thick-walled
fibres, often
with
brachysclereids
lib. fibres,
fibretracheids,
vasicentric
tracheids
lib. fibres,
vasicentric
tracheids
absent
abundant,
paratrachealf
aliformconfluent
abundant,
mainly
apotracheal
to subreticulate
fibre
tracheids,
present
tracheids
low, 1-3
cells wide
high,
broad
.,;; 20 cells
wide
height
variable,
1-3 cells
wide
1-2 cells
scanty,
paratracheal, wide
lignified
scanty to
abundant,
diffuse, often
lignified
lib. fibres
vasicentric
low, 2-3
cells wide
sparse, diffuse low, 1-2
cells wide
absent
absent
lib. fibres
absent
lib. fibres & abundant,
diffuse
fibre
tracheids
absent
v. thick-walled solitary or
in short
fibres +
brachysclereids radial
chains
radial
thick-walled
fibres
absent
absent
absent
libriform
fibres
absent
rays
Axial
parenchyma
solitary or
in short
radial
chains
Imperforate
Pit
vesturing elements
angular cells,
not thickwalled; no
brachysclereids
Vessels
absent
Sclerenchyma
Kranz
anatomy type
4. Anatomical characters
multicellular, anomocytic, elongated,
in two
mainly
capitate
lengths
among
shorter epid.
cells
anomocytic irreg. with
unicellular
type A
Morkillioideae zygophylundulating
laceous
anticlinal
walls
anomocytic, large
absent
petiole absent type B
Augeoideae
straighta few
sided,
paracytic
hexagonal
anomocytic, polygonal or
type A, type unicellular;
Zygophylloideae zygophylsinuous
unbranched, a few
B&
laceous,
paracyticf
intermediates 2-armed,
centric or
weakly
lobed, or
absent
actinocytic
capitate
discrete vase. type A
unicellular, 2 anomocytic, irregular
Tribuloideae
narrow
bundles
sizes
Petiole
vasculature
TABLE
238
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
M. C. SHEAHAN AND D. F. CUTLER
239
few scattered sclerenchymatous cells abaxial to vascular bundle; wide phloem
with large empty cells elongated parallel to leaf axis.
Stem. Hypodermis present, with thick collenchymatous periclinal walls.
Cortex: 2-4 layers outer chlorenchymatous cells, axially elongated; inner layers
of larger colourless cells. Fibres with angular, medium-thick walls; often forming
complete cylinder 4-10 cells thick separating cortex from phloem; phloem ducts
as in leaf. Periderm originating in inner cortex. Xylem poorly developed; vessels
solitary or in short radial chains; libriform fibres with few pits, and shorter
narrow fibre-tracheids with bordered pits. Rays and axial parenchyma absent.
Pith of large unlignified irregular brick-shaped cells with elongated simple pits;
pith breaking up. Crystals: raphides and short acicular crystals in cortex.
Malacocarpus ( Malacocarpus crithmifolius)
Leaf venation. Secondary veins running parallel to pnmary vem; areoles
elongated. Tracheoids sparse (Fig. 4).
Leaf surface. Wide band of long narrow epidermal cells ( 11 : 1), alternating
with bands of shorter but still elongated cells with undulating anticlinal walls
(7 : 2). Stomata± circular, mainly among shorter epidermal cells. Trichomes
c. 70 Jlm long; multicellular, capitate, glandular, on young leaf only.
Lamina in TS. Outline narrow, flattened, with adaxial groove; depth c.400 Jlm.
Mesophyll thick, more or less dorsiventral; not more than 5-6 vascular bundles.
Midvein arc-shaped; lateral veins very small. Crystals: many raphide sacs in
mesophyll.
Stem. Cortex: groups of fibre strands in cortex, with medium thick walls,
becoming sloughed off. Periderm differentiation early in inner cortex. Xylem:
vessels solitary, some with tertiary spiral thickening; numerous dense fibres with
simple, slit-shaped pits, some with living contents; also narrow fibre-tracheids
with bordered pits; axial parenchyma absent. Pith narrow, of large thin-walled
cells becoming lignified.
Viscainoa J M orkillia ( Viscainoa geniculata, M orkillia mexicana)
Leaf venation. Type A; tracheoids sparse, slender.
Leaf surface. Epidermal cells larger adaxially than abaxially, irregular, slightly
elongated, some with undulating anticlinal walls (Fig. 2C). Trichomes c.400 Jlm
long; on young leaf only (Fig. lD).
Lamina in TS. Outline shallow (c.l30 Jlm) with prominent midrib. Mesophyll
dorsiventral; 1-2 layers short wide palisade cells, and loosely packed
chlorenchymatous spongy mesophyll. Central vascular bundle arc-shaped,
phloem wider than xylem; collenchyma adaxial and abaxial to larger veins.
Petiole. Outline± circular with two broad lateral wings; vascular system in
form of interrupted arc, with abaxial groups of collenchymatous cells and two
or more small lateral bundles (Fig. 9F).
Figures 3-8. Fig. 3. Guaiacum guatemalense: two distal pairs of leaflets cleared to show venation. Fig. 4.
Malacocarpus critkmifolius: part of cleared leaf. Fig. 5. Peganum karmala: TS narrow leaf segment with
radial mesophyll and water storage cells in the centre. Fig. 6. zYgophyllumfabago: epidermal cells and
stomata. Fig. 7. Guaiacum officinale: part of cleared leaflet showing narrow vein endings. Fig. 8.
:{,.fabago: part of cleared leaflet showing enlarged terminal tracheoids. (Scale bars= 150 J.lm, except
in Fig. 3 where= 4 mm, and Fig. 6 where= 25 j.lm.)
240
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
Stem. Epidermis persistent; trichomes with living contents on young stem.
Cortex 5-7 cells wide, chlorenchymatous; clusters of very thick-walled fibre
strands in inner cortex, associated with medium thick-walled brachysclereids.
Periderm differentiation late, in outer cortex. Xylem: vessels solitary or in short
radial chains, fibre-tracheids with bordered pits, thick-walled fibres with one row
of simple pits on tangential walls only; axial parenchyma abundant, diffuse; rays
heterocellular, 2-3 square and upright cells wide at widest point, tapering to
upright cells. Pith of large thin-walled cells.
Augea ( Augea capensis)
Leaf venation. Type B; tracheoids in large clusters at veinlet terminations.
Leaf surface. Epidermal cells large, straight-sided, angular, frequently
hexagonal in surface view; stomata large, scanty, a few paracytic. Trichomes
absent.
Lamina in TS. Outline: thick (c.6 mm), almost circular, with no distinct
boundary between adaxial and abaxial surfaces. Epidermal cells with thick
mucilaginous outer and inner periclinal walls. Mesophyll centric, with outer
layer of 3-5 palisade cells, and very wide area oflarge thin-walled water storage
cells surrounding central vascular bundle. Vascular tissue: central bundle
forming a flattened cylinder or double arc, with narrow outer band of phloem
and radial rows of 4-8 xylem tracheids with scalariform pitting. Peripheral
vascular bundles small, mainly at junction between palisade and water-storage
tissue.
Stem. Outline a slightly flattened circle; cortex with extremely wide band of
large colourless water storage cells. Fibres in cortex, in incomplete irregular
band, with very thick walls, much reduced lumen and simple unbranched pits.
Periderm originating in outer cortex. Vascular system a flattened cylinder;
phloem with numerous rays. Xylem well developed; vessels in radial rows;
libriform fibres with thick walls and sparse pits; densely pitted vasicentric
tracheids; axial parenchyma sparse, diffuse. Rays 1-2 cells wide, becoming
lignified. Pith of thin-walled cells, smaller at periphery. Crystals: occasional large
crystal masses in cortex.
Fagonia ( Fagonia mollis)
Leaf venation. Type A; primary vein ending in cluster of libriform, unpitted
fibres extending beyond apex to form mucronate point; veinlets terminating in
dense tracheoids, becoming very abundant just below leaflet apex.
Leaf surface. Epidermal cells polygonal, sometimes slightly elongated, with
straight or slightly sinuous anticlinal walls. Trichomes c. 70 j.lm long; unbranched, capitate, on young leaf only.
Lamina in TS. Outline: leaflets narrow, thick (c.500 ~m), with narrow adaxial
groove; midrib not protruding. Epidermis thin. Mesophyll weakly isolateral,
with biseriate palisade; chloroplasts less dense in centre of leaf. Vascular bundles:
veins small, dense; sclerenchyma absent.
Petiole. Outline oval, flattened adaxially. Central vascular bundle a wide arc,
with two lateral bundles; ground tissue of large thin-walled chlorenchyma cells.
Stem. Outline (Fig. lOD): ±pentagonal. Trichomes: capitate, some on basal
plinth of epidermal cells. Cortex of large loosely-packed thin-walled cells;
bundles of fibres in two irregular, concentric rings; outer ring of five large groups
M. C. SHEAHAN AND D. F. CUTLER
241
of fibres forming five ridges or angles in stem, alternating with inner ring of
smaller groups of fibres, augmented by irregularly shaped sclereids with large
simple pits. Origin of periderm differentiation in mid-cortex; outer ring of fibres
becoming sloughed off. Xylem: vessels mostly solitary, circular to oval; richly
pitted fibre-tracheids; libriform fibres with scanty slightly bordered pits;
vasicentric tracheids present. Axial parenchyma sometimes lignified. Rays
mostly uniseriate; cells square to upright. Pith of lignified, densely pitted cells.
Stipule spiny, with chlorenchymatous cortex and large central mass of tightlypacked lignified fibres; vascular bundles in ring round sclerenchyma, xylem
external.
zYgophyllum ( zYgophyllum fabago, ,Z. oxianum, ,Z. xanthoxylum, ,Z. kaschgaricum, ,Z.
darvasicum, Z· eurypterum, ,Z. simplex,
dumosum, ,Z. album, Z· fontanesii, ,Z.
coccineum, ,Z. stap.ffii, ,Z. eremaeum)
Leaf venation. Type A (e.g. ,Z. fabago, ,Z. darvasicum) and B (e.g. ,Z. album, ,Z.
fontanesii, ,Z. simplex) both present; also intermediate form in some fleshy leaves,
with line of bundles curving down towards margin (e.g. ,Z. xanthoxylum). Veins
slender. Terminal tracheoids sparse to moderately dense (Fig. 8).
Leaf suiface. Trichomes usually unicellular; unbranched, 2-armed (Fig. 2B), or
lobed (Fig. lA); thinly cutinized, often caducous; some on basal plinth of
epidermal cells. Stomata: some paracytic or weakly actinocytic (Fig. 6).
Lamina in TS. Outline: leaves and leaflets may be oval (e.g. Fig. IF), flattened,
or recurved abaxially at margins; midrib not prominent. Mesophyll dorsiventral,
isolateral, or centric; more or less fleshy, often with water storage cells in centre
of leaf. Vascular bundles: midvein compound, or an interrupted cylinder,
sometimes with collenchyma strands abaxial to phloem. Minor veins small,
closely spaced; sclerenchyma scanty. Semi-circular bundle sheath adjacent to
outer part of veins present in ,Z. simplex only (Fig. lOB).
Petiole (where present) zygophyllaceous, with central vascular bundle and two
or more smaller bundles (Fig. 9E), or similar to type A venation, with central
arc-shaped vascular bundle and peripheral network of smaller bundles.
Stem. Outline: mainly circular, flattened below nodes. Trichomes, where
present, caducous, appressed to stem. Cortex in young stem of large thin-walled
chlorenchymatous cells, becoming replaced by wide layer of thin-walled cork
cells. Groups of lignified thick-walled fibre strands in cortex, often associated
with thick-walled brachysclereids. Periderm differentiation usually in middle to
inner cortex. Xylem dense. Vessels usually solitary, sometimes in short radial or
tangential chains; rather angular, occasionally with tertiary spiral thickening
(e.g. ,Z.fabago). Vasicentric tracheids present in some species. Axial parenchyma
diffuse, often lignified. Rays short, mostly uniseriate, often lignified; some
storying; cells square to erect in immature stem, procumbent in older wood.
z.
Bulnesia ( Bulnesia arborea)
Leaf venation. Type A; tracheoids sparse (Fig. 2E).
Leaf suiface. Epidermal cells small, randomly orientated, with undulating
anticlinal walls. Trichomes 140-280 ~m long; only on petiole, rachis and leaflet
margin.
Lamina in TS. Outline shallow (c.lOO ~m), with slightly protruding midrib.
Cuticle 2-3 ~m, thicker at leaflet margin. Epidermal cells small, with slightly
242
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
500
~m
F
Figure 9. TS petioles (all to same scale). A, Guaiacum officinale: central cylindrical vascular bundle
with two smaller bundles in the latera-adaxial position. B, }ieoluederit?.ia sericeocarpa: vascular bundle
in the form of an interrupted cylinder, with two adaxial bundles. C, Kallstroemia grandiflora: Kranz
tissue is marked with arrows. D, Balanites aegyptiaca: the vascular system is formed of an abaxial arc of
discrete collateral bundles, and a double adaxial arc of bundles, with external phloem. E,
:Q>gophyllum kaschgaricum: the line of smaller bundles is recurved abaxially, as it is in the leaflet. F,
Viscainoa geniculata: vascular bundle in the form of an interrupted arc.
thickened outer walls. Mesophyll dorsiventral, with unH occasionally hi- )seriate
adaxial palisade. Vascular bundles: main vascular bundle forming an arc;
phloem more extensive than xylem. Sclerenchyma surrounding principal
vascular bundles, and adaxial to many minor bundles.
Petiole. Outline a flattened circle with two lateral wings; central vascular tissue
cylindrical, with two smaller latera-adaxial bundles.
Stem. Cortex persistent; periderm originating in outer cortex. Pericyclic
cylinder of sclereids with large simple pits in association with strands of thickwalled sparsely pitted fibres, separated from phloem by layer of 8-10 cortical
cells. Phloem well-developed, storied. Xylem: vessels circular, but angular when
in radial chains; sometimes irregularly storied; solitary or in radial or dendritic
M. C. SHEAHAN AND D. F. CUTLER
243
chains of up to 10 cells; abundant narrow thick-walled libriform fibres with
sparse pits in radial walls only; some fibre-tracheids; vasicentric tracheids few,
narrow, with numerous bordered pits. Axial parenchyma scanty, some in
isolated strands, some associated with vessels. Rays storied, homocellular, low, 13-seriate (Fig. 13).
Guaiacum (Guaiacum rdficinale, G. sanctum, G. guatemalense)
Leaf venation. Type A; veinlet terminations narrow, lacking dilated tracheids
(Figs 3, 7).
Leaf surface. Cuticle with beaded anticlinal flanges. Epidermal cells small,
±straight-sided; usually longer axially than wide, randomly oriented. Stomata:
some paracytic, some weakly actinocytic. G. oifi.cinale hypostomatous, G. sanctum
and G. guatemalense amphistomatous. Trichomes on petiole, rachis and margin
only; thin-walled c.l20 Jlm long.
Lamina in TS. Outline: wide, c.220 Jlm thick, with moderately prominent
midrib. Cuticle thick, especially at margin, with cuticular flanges. Stomata:
outer wall of guard cells thickly cutinized, with prominent outer stomatal ledge
(Fig. IE). Mesophyll: bi-(tri-)seriate adaxial palisade; slightly smaller, more
closely packed abaxial cells. Vascular bundles: main vein arc-shaped with
extensive xylem and numerous adaxial fibres; strands of thick-walled fibres and
some collenchyma abaxial to phloem. Larger lateral veins often with cylindrical
xylem and abaxial fibres; smaller veins with abaxial collenchyma. Crystals:
numerous large druse idioblasts in mesophyll, especially round main vein;
occasional small styloids in mesophyll; solitary crystals in epidermal cells.
Petiole. Outline circular, with two prominent latera-superior wings curving
forward adaxially (Fig. 9A). Cortex of closely packed chlorenchymatous cells.
Central vascular bundle a cylinder with well-developed xylem and phloem; two
lateral bundles in latero-adaxial position with xylem in shape of a cylinder,
phloem surrounding it on three sides, and fibres external to phloem. Scanty
trichomes as on leaf surface. Crystals: many druses in cortex.
Pulvinus at leaflet base with grooves perpendicular to leaflet axis: cortex of
closely packed, rather thick-walled isodiametric cells, with much thick-walled
collenchyma round central cylindrical vascular bundle.
Stem. Short unicellular caducous trichomes with thin walls. Cortex well
developed. Groups of thick-walled fibre strands outside phloem, replaced by
collenchyma at node. Solitary brachysclereids frequent in cortex, especially at
node. Periderm differentiation immediately below epidermis. Xylem: vessels
solitary, oval, with very small pits. Fibre-tracheids, closely packed, with small
diameter, thick walls and small bordered pits. Parenchyma scanty paratracheal
or diffuse in aggregates or in narrow bands. Rays storied, almost entirely
uniseriate, low (4--7 cells high); cells procumbent, many containing resin. Pith of
isodiametric cells, becoming lignified in centre. Crystals: druses in cortex and
pith, solitary crystals in phloem; many epidermal cells containing a single small
acicular crystal.
Porlieria ( Porlieria hygrometra, P. chilensis)
Leaf venation. Type A: higher order veins forming dense network bounding
irregular areoles. Numerous tracheoids associated with veins and vein endings in
P. hygrometra; vein endings thin and tapering in P. chilensis.
244
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
Leaf suiface. Epidermal cells small, irregular in size and shape. Stomata sparse,
with wide stomatal ridge; some weakly actinocytic. Trichomes on petiole, rachis
and leaflet margin: c.600 Jlm long, slender, appressed towards leaflet apex; thickwalled, with narrow lumen and striate surface.
Lamina in TS. Outline: c.230 Jlm thick, with shallow midrib and slight adaxial
groove. Some epidermal cells tanniniferous in P. hygrometra. Stomata superficial;
leaflet amphistomatous. Mesophyll dorsiventral in P. chilensis; isolateral in P.
hygrometra, with biseriate palisade adaxially, uniseriate abaxially. Broad layer of
large empty cells in centre of leaflet surrounding vascular bundles; absent at
margin. Vascular bundles: main vein and 2° veins with unusually large area of
phloem, and narrow abaxial cap of collenchyma in P. hygrometra; thick-walled
fibres in P. chilensis. Sclerenchyma absent. Crystals: many druses and a few
styloids in mesophyll.
Petiole. Outline: elliptic, flattened adaxially and abaxially, with slight adaxial
groove. Central vascular bundle a flattened cylinder with narrow band of xylem
circled by abundant collenchyma; two much smaller cylindrical lateral bundles.
Abundant thick-walled trichomes, as leaf. Central parenchyma lignified.
Pulvinus. Grooves in epidermis perpendicular to axis. Epidermal cells with
thickened walls, elongated. Stomata absent. Cortex: cell walls thicker in adaxial
part of cortex than in abaxial; collenchyma surrounding vascular bundles and in
pith.
Stem. Epidermal cells elongated axially; soon becoming sloughed off. Cortex:
cortical cells somewhat elongated radially; small clusters of thick-walled fibre
strands in inner cortex. Periderm differentiation very early, immediately below
epidermis; phellem cells large, irregular. Elongated tanniniferous cells in cortex
and outer phloem. Xylem (Fig. 11): vessels small, solitary, circular to oval; some
elements very short (shorter than wide). Fibre-tracheids thick-walled.
Parenchyma abundant, diffuse and in irregular tangential uniseriate bands.
Rays uniseriate, homogeneous, narrow, low (mostly 2-4 cells high), storied; cells
procumbent to square. Pith of large lignified cells, with pitfields. Crystals: very
numerous solitary crystals (styloids and rhomboids) in phloem; a few druses in
cortex.
Larrea (Larrea tridentata)
Leaf venation. Type A; leaflets fused at base, venation extremely asymmetric.
Leaf suiface. Epidermal cells small, polygonal, rather irregular in size. Leaf
amphistomatous. Trichomes very dense especially at margins: 200-300 Jlm long,
thick-walled with thin cuticle, inner wall surface uneven; appressed towards leaf
apex; cutinized round base on mature leaf.
Lamina in TS. Outline narrow, c.250 Jlm thick, with shallow midrib. Epidermal
cells thick-walled; many with brownish contents. Stomata slightly raised above
level of epidermis, with strongly projecting cutinized outer ledge; guard cells
partly overlying adjacent cells. Mesophyll weakly isolateral: 2-3 rows tightly
packed adaxial palisade cells, length-width ratio c.5: 1; two rows shorter abaxial
cells; narrow zone of chlorenchymatous spongy mesophyll in centre of leaf.
Midvein with thick-walled collenchymatous fibres abaxial to phloem. Modified
incomplete bundle sheath of cells containing chloroplasts round some veins.
Crystals: numerous druses in mesophyll.
M. C. SHEAHAN AND D. F. CUTLER
245
Petiole. Outline oval, truncated adaxially. Epidermis uneven, ridged, with few
stomata and trichomes. Vascular system: central cylindrical bundle and two
small latera-adaxial bundles; all surrounded by collenchymatous tissue
containing small clusters of lignified cells.
Stem. Outline oval with four lobes. Cuticle thick (c.6 J..lm). Epidermal cells with
thick outer and inner walls, frequently with brownish contents. Stomata raised,
scanty. Cortex: cells thin-walled and chlorenchymatous in young stem; periderm
differentiation in outer cortex; occasional tanniniferous cells in cortex. Up to 12
clusters of thick-walled fibres round vascular cylinder. Occasional thick-walled
brachysclereids with branched pits associated with fibre clusters, some
isodiametric, some 2-4 times longer than wide, axially elongated; in older stem
brachysclereids forming complete cylinder round phloem. Vascular system in
young stem a continuous lobed cylinder; in older stem ± oval in TS. Xylem:
vessels oval, thick-walled, solitary, rarely in twos; many fibre-tracheids with
frequent bordered pits; some thick-walled fibres with pits mainly in radial walls;
vasicentric tracheids present. Rays 1-2-seriate, heterocellular, with square
marginal cells; weakly storied. Parenchyma diffuse, apotracheal. Pith of
isodiametric cells with large pitfields, becoming lignified in older stem but
remaining unlignified at node. Crystals: druses and solitary crystals in cortex;
many large solitary crystals in phloem, sometimes in crystalliferous parenchyma
strands.
Pintoa ( Pintoa chilensis)
Leaf venation. Type A; numerous large, dense tracheoid clusters, especially at
apex. Long, very thick-walled fibres with square ends running abaxially to some
vems.
Leaf surface. Epidermal cells polygonal, with straight anticlinal walls adaxially,
slightly undulating abaxially. Occasional large abaxial idioblasts, in groups of
1-5. Stomata nearly circular; leaf amphistomatous. Trichomes c.300 J..lm long,
appressed to surface; dense adaxially, sparse abaxially.
Lamina in TS. Outline: lamina thick (c.450 J..lm); midrib not protruding.
Epidermal cells with thick outer wall. On abaxial surface occasional small
groups of much enlarged epidermal idioblasts, with thin outer walls and thin
pitted anticlinal walls; extending well below level of surrounding epidermal cells,
and partly overlaid by them. Trichomes cutinized all round region of
attachment in older leaves. Mesophyll dorsiventral, with 2-3 layered irregular
palisade and spongy mesophyll with extensive air-spaces. Vascular bundles
frequent, in mid plane of leaf. Crystals: numerous druses in centre of leaf.
Plectrocarpa ( Plectrocarpa rougesii)
Leaf venation. Type A; frequent large clusters of tracheoids associated with
veins and at vein endings (Fig. 2F).
Leaf surface. Epidermal cells irregular in size. Stomata: leaflet amphistomatous,
more stomata abaxially. Trichomes dense, appressed towards apex, c.200 J..lm
long, thick-walled; basal part with surrounding rosette of epidermal cells.
Lamina in TS. Outline: lamina of even thickness, c.320 J..lm; midrib not
prominent. Epidermal cells low, with thickened outer walls. Stomata level with
centre of surrounding epidermal cells, with very narrow lumen. Mesophyll
weakly isolateral; palisade cells narrow, longer adaxially than abaxially.
246
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
Vascular bundles: veins frequent; midvein and principal lateral veins with
extensive phloem and abaxial sclerenchymatous cap. Crystals: abundant druses
associated with veins.
Petiole. Outline ± semi-circular. Ground tissue chlorenchymatous. Central
vascular system a flattened cylinder with narrow collenchymatous pith. 4-5
large clusters of fibres outside phloem, surrounded by collenchyma. Two smaller
latera-adaxial bundles, each with large fibre cap. Many thick-walled trichomes,
especially adaxially .
.Neoluederit;:,ia ( .Neoluederitzia sericeocarpa)
Leaf venation. Type A; higher order veins slender, often only of 1 or 2 spirally
thickened tracheids. Tracheoids small, sparse.
Leaf surface. Epidermal cells straight-sided, polygonal. Stomata small,
moderately dense. Trichomes appressed to surface; sparse except on margins,
rachis and petiole; 600-800 J.lm long, with surrounding rosette of epidermal cells.
Lamina in TS. Outline c.200 J.lm deep, with shallow midrib. Epidermis shallow.
Stomata slightly sunken. Trichomes sometimes with slightly raised bases.
Mesophyll weakly isolateral; palisade biseriate adaxially, uniseriate abaxially,
with spongy mesophyll in centre of leaflet; chlorenchymatous throughout. Some
chlorenchyma cells forming rudimentary sheath round vascular bundles.
Vascular bundles: midvein arc-shaped; some thin-walled collenchyma abaxial to
phloem. Crystals: druses present in mesophyll, sometimes in large clusters; also
abundant small rhomboidal crystals.
Petiole. Outline oval with adaxial groove (Fig. 9B). Epidermal cells small with
thick walls. Hypodermis with thickened cellulosic walls. Stomata and trichomes
as leaflet. Vascular system with 6-8 discrete bundles, each with external and
internal cap of collenchymatous cells. Central adaxial bundle larger than rest,
with U-shaped xylem. Two smaller bundles in latera-adaxial position,
cylindrical, with lateral collenchyma cap.
Stem. Cortex of large cells slightly elongated axially, smaller immediately
below epidermis. Moderately thick-walled fibres, in clusters of 10-30 cells.
Periderm differentiation in outer cortex. Xylem: vessels variable in size, thickwalled, in a radial pattern separated by broad radial bands of very thick-walled
fibres with unpitted tangential walls; occasional vasicentric tracheids. Rays 1-3
cells wide, cells square to procumbent, walls becoming lignified. Axial
parenchyma abundant, diffuse, apotracheal; becoming lignified. Pith of large ±
isodiametric cells with thin walls; breaking up. Crystals: large rhomboidal
crystals in cortex and pith, sometimes > 1 per cell; druses in cortex and pith.
Si~ndite
( Si~ndite spartea)
Leaf venation. Type A. Abundant rather small irregular tracheoids associated
with small 3° veins and vein endings in loosely connected clusters of 1-8 cells;
especially dense at margin; tracheoids mostly narrow, with scalariform pitting.
Leaf surface. Epidermal cells straight-sided, regular, smaller adaxially than
abaxially. Stomata nearly circular. Trichomes c.l50 J.lm long; on adaxial surface
only; extremely sparse ( ~ 10 per leaflet).
Lamina in TS. Outline: leaflet thick (c.250 J.lm); midrib shallow. Stomata ±
level with centre of epidermal cells. Mesophyll isolateral, with 2-3 layers long
palisade cells (4: 1) ad axially, and shorter palisade (3: 1) abaxially; central
M. C. SHEAHAN AND D. F. CUTLER
247
A
D
500 1-lm
Figure 10. A & B. TS leaf(lets) (both to same scale). A, Tribulus terrestris showing one small bundle
with sheath. B, <:,ygophyllum simplex showing sheath partly surrounding one vascular bundle. C,
T. terrestris: bundle sheath in paradermal view. D, Fagonia mol/is: TS stem.
region of spongy mesophyll cells with scanty chloroplasts. Vascular tissue:
midvein arc-shaped; abaxial to it a cluster of cells with slightly thickened
cellulosic walls. Crystals: large druse-containing idioblasts among cortex cells of
rachis and petiole; druses in petiolule; minute acicular crystals in many
epidermal cells of leaflet.
Petiole. Outline circular. Cuticle c.1.5 J.lm thick, with shallow cuticular flanges.
Epidermal cells isodiametric, regular, with thickened peri- and anticlinal walls.
Stomata sunken. Shallow hypodermis of small clear cells with slightly thickened
walls, elongated axially. Mesophyll: outer three layers palisade cells; inner part
of larger, empty, mostly isodiametric cells. Vascular tissue of discrete collateral
bundles; some with phloem cap offibres with very thick cellulosic walls, only the
outermost wall layer lignified; interspersed with smaller bundles without caps.
Stem. Wax on surface. Cuticle 4-5 J.lm thick. Epidermis persistent, low, with
occasional stomata. Hypodermis present. Cortex: outer layers of isodiametric
chlorenchymatous cells; inner layers of larger empty cells. Cork development
late, immediately below epidermis; inner periderm cells thin-walled, empty;
outer cells becoming lignified. Fibre strands in loose clusters outside phloem,
248
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
medium thick-walled, only partly lignified. Vascular system: phloem extensive,
with wide ray parenchyma cells in TS. Xylem: vessels circular, variable in
diameter, in loose radial clusters; fibre-tracheids. Axial parenchyma cells
lignified. Rays: variable in height (2-50 cells), 1-3 cells wide; cells square to
procumbent, becoming lignified. Pith of isodiametric cells with thick lignified
walls and many pitfields; breaking up except at node. Crystals: druses and
rhomboidal crystals in cortex.
Tribulus ( Tribulus terrestris, T. zeyheri)
Leaf venation. Type A; veinlet termination tracheids sparse, not swollen.
Leaf surface. Cuticle striate, especially at base of trichomes. Epidermal cells
small, irregular in size and shape. Stomata moderately dense, rather narrow;
leaflet amphistomatous. Trichomes of two types: one short and pointed,
appressed to surface, length 40-50 J.lm; especially on adaxial surface; the other
type longer (length 240-400 J.lm), with wider basal part surrounded by
prominent rosette of epidermal cells. Both types found on abaxial surface,
margin, midrib, petiole and rachis; trichomes denser in T. zeyheri.
Leaflet in TS. Outline thin (120-200 J.lm), with shallow midrib. Stomata
superficial to slightly sunken. Trichomes of both types with thinly cutinized wall
near base; in close contact with underlying palisade cells; neighbouring
epidermal cells raised; larger trichomes cutinized round zone of attachment.
Mesophyll: one row long (3 or 4: 1) palisade cells adaxially, shorter cells
abaxially; narrow zone of spongy mesophyll with few chloroplasts inside abaxial
epidermis. Vascular tissue: midvein weak, with small associated area of
collenchyma; veins small, closely spaced. Bundle sheath (Figs 1OA, C; 15)
prominent, round all veins, of large cells, slightly elongated radially
(c.23 x 18 J.lm), also elongated perpendicular to vein axes; completely
surrounding veins; walls pitted and rather thicker than cells of ordinary
mesophyll. Chloroplasts small in mesophyll cells (c.3 x 2 J.lm), lining cell walls;
larger chloroplasts (c.5 X 3 J.lm) in centripetal position in bundle sheath cells.
Crystals: a few large druse-containing idioblasts in mesophyll.
Petiole. Outline slightly elliptical, flattened laterally. Epidermal cells low, with
convex outer wall. Trichomes and stomata as leaflet. Mesophyll of very large
thin-walled parenchyma cells, smaller towards periphery; short row of palisade
cells adaxial to two latero-adaxial veins; otherwise chlorenchyma lacking.
Vascular tissue: four discrete vascular bundles in centre, each with cap of fibres
with thickened cellulosic walls; two smaller bundles in latera-adaxial position,
partly inverted so that xylem poles face each other, with poorly developed
xylem, each with incomplete bundle sheath, and cap of collenchymatous fibres.
Stem. Epidermis shallow. Trichomes present, some long with raised bases, some
short emerging directly from epidermis, as leaflet. Cortex: irregular row of small
cells, slightly elongated axially, immediately below epidermis; inner layers of
large thin-walled parenchyma; periderm differentiation in outer cortex. Xylem a
continuous cylinder; vessels mainly solitary or in short radial chains; alternating
with zones of thick-walled fibre-tracheids; vasicentric tracheids present. Axial
parenchyma mostly paratracheal, scanty, lignified. Rays mostly uni-, a few
biseriate; cells square to upright. Crystals: a few acicular crystals in epidermis,
cortex and pith; druses in cortex.
M. C. SHEAHAN AND D. F. CUTLER
249
Kallstroemia ( K allstroemia grandiflora)
Leaf venation. Type A; veinlets terminating in 1-2 narrow tracheids.
Leaf surface. Epidermal cells with undulating anticlinal walls especially
abaxially. Stomata small, some paracytic. Trichomes caducous, abundant on
abaxial surface of petiole and rachis, especially on midrib and margin; less
frequent adaxially; two main size classes: smaller length c.200 Jlm, longer
c.1300 Jlm; trichomes cu tinized around region of attachment; surrounded by
rosette of raised enlarged epidermal cells.
Lamina in TS. Outline 200-250 Jlm thick, with shallow midrib. Epidermis low.
Stomata superficial to slightly sunken. Trichomes: smaller ones with narrow
bases; larger with bases inside plinth of elongated and elevated epidermal cells
(Fig. lB); plinths remaining when trichomes fall. Mesophyll: one row palisade
cells each side, adaxial longer than abaxial; a layer of large, loosely organized
spongy mesophyll cells immediately inside abaxial epidermis, containing few
chloroplasts. Vascular tissue: bundles small, closely spaced; some collenchyma
abaxial to midvein. Bundle sheath round all veins, prominent, with large cells
elongated radially (c.40 x 30 Jlm); chloroplasts: in mesophyll cells c.2 x 4J.!m; in
bundle sheath cells centripetal, diameter c.5 Jlm.
Petiole (Fig. 9C). Outline a flattened pear shape, with broad raised adaxial
ridge. Mesophyll: ground tissue of large empty cells, larger towards the centre;
chlorenchymatous tissue forming band inside adaxial half of epidermis: 1-2
seriate palisade under central adaxial ridge; spongy mesophyll on either side.
Vascular tissue: four well-spaced central vascular bundles, each with broad
xylem and cap of collenchyma; one much smaller bundle in central adaxial
position, with xylem orientated outwards and internal collenchyma extending
laterally on both sides. Kranz tissue: a single, occasionally double, row inside
palisade; one row round outside of phloem collenchyma cap of both lateral
bundles.
Stem. Epidermal cells shallow, thin-walled. Cortex narrow in TS, of boxshaped cells elongated axially. Large clusters of moderately thick-walled fibre
strands. Xylem: vessels mostly solitary, sometimes in pairs; elements ± storied.
Fibre-tracheids angular in outline, with sparse pits. Axial parenchyma
paratracheal. Rays low, uniseriate, cells square to upright.
Nitraria ( Nitraria schoberi, N. retusa)
Leaf venation. Type A; veinlets branched, ending in very large clusters of
tracheoids.
Leaf surface. In N. retusa covered in wax platelets. Epidermal cells polygonal,
irregular in shape and size. Stomata: a very few paracytic or weakly
stephanocytic in N. retusa; with raised thickly cutinized areas at each end of
guard cells inN. schoberi. Trichomes 120-220 Jlm long, sparse, linear-elliptical in
surface view, sometimes clavate in N. schoberi; warty, appressed towards leaf
apex; with thinly cutinized walls.
Lamina in TS. Outline 450-850 Jlm thick in N. retusa; 320-480 Jlm in N.
schoberi; shallower at margins; midrib not protruding. Epidermal cells somewhat
convex; sometimes showing anti- and periclinal divisions. Stomata small, slightly
sunken; with inner ridge forming small inner chamber in N. schoberi. Mesophyll
± dorsiventral: 3 layers of short adaxial palisade cells and 3-4 abaxial layers of
smaller chlorenchymatous cells with many air spaces; in N. retusa a central area
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
250
15
M. C. SHEAHAN AND D. F. CUTLER
251
of 4-5 layers large, more closely packed thin-walled parenchyma cells with few
chloroplasts. Vascular tissue: central vascular bundle slender, arc-shaped, with
poorly developed xylem; scanty associated sclerenchyma in .N. retusa. Crystals:
few minute acicular crystals and small druses in epidermal cells, rarely also in
mesophyll. Tannin cells abundant in .N. retusa, in palisade and outer layers of
central parenchyma, also in petiole parenchyma. Mucilage: occasional mucilage
cells in mesophyll; also abundant in petiole of N. retusa.
Stem. Outline round to oval. Trichomes in .N. schoberi clavate, dense on young
stem. Cortex: one or two outer layers of small cells with thick paradermal walls;
main part of cortex of large thin-walled cells. Fibres very thick-walled, forming
crescent-shaped caps round bundles; lignified parenchyma cells intercalated
between caps. Periderm originating in innermost part of cortex. Phloem well
developed, with abundant parenchyma. Xylem (Fig. 12): vessels circular to oval;
solitary or in short radial clusters or chains; grouped in radial bands separated
by fibres; storied, some spiral thickening. In .N. retusa vessels of two different size
classes: smaller 15-35 J.lm diameter, larger 45-100 J.lm; many with gummy
contents. Libriform fibres abundant, some with living contents. Axial
parenchyma abundant, paratracheal; aliform-confluent in .N. retusa. Rays 1-3seriate, of variable height ( 1-25 cells). Mucilage: large mucilage cells and
cavities in cortex, also canals in older stem; mucilage also frequent in phloem
parenchyma and rays, in pith and at nodes.
Balanites (Balanites aegyptiaca, B. maughamii)
Leaf venation. Type A; veinlets ending in large compact clusters of tracheoids.
Leaf surface. Cuticle with thickened beaded flanges. Epidermal cells small,
polygonal. Stomata rather narrow; many anomocytic, some weakly
stephanocytic, a few paracytic; leaflet amphistomatous. Trichomes 170-470 J.lm
long, shorter on leaflet margin.
Lamina in TS. Outline: depth in B. aegyptiaca c.300 J.lm; in B. maughamii
c.200 J.lm, with more protruding midrib. Stomata slightly or very sunken, with
large substomatal cavity and tall, narrow adjacent cells; overlying cuticle
forming raised rim round stomata. Mesophyll: 1-2 rows adaxial palisade; one
row of large cells lengthened in same axis as palisade in centre of leaf; 3-4 rows
slightly elongated abaxial cells. Vascular system: midvein with well developed
phloem; cap of collenchyma associated with mid vein and some 2° veins. Crystals:
many druses and large solitary crystals in petiole mesophyll; also druses in
mesophyll.
Petiole (Fig. 9D). Outline ± circular; cuticle thick with cuticular flanges.
Trichomes short, curved. Mesophyll: wide outer area of parenchyma,
chlorenchymatous at periphery. Vascular system forming an abaxial arc of
Figures 11-15. Figs II, 12. TS stem. Fig. II. Porlieria hygrometra: solitary vessels, thick-walled fibretracheids and diffuse parenchyma (scale bar=25j.!m). Fig. 12 . .Nitraria retusa: TS wood, showing
vessels in two size classes, abundant aliform-confluent parenchyma, and narrow rays (scale
bar=200j.!m). Fig. 13. Bulnesia arborea: TLS stem showing storied arrangement of rays (scale
bar= 100 j.!m). Fig. 14 . .N. schoberi: TS stem showing mucilage cells; the narrow rays and thickwalled fibres can also be seen, and the clear phellem cells (scale bar= 100 j.!m). Fig. l5. Tribulus
zryheri: TS leaflet with prominent bundle sheath (scale bar= 50 j.!m).
252
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
discrete collateral bundles; adaxially forming a double arc of bundles, all with
external phloem; collenchyma adjacent to phloem of all bundles.
Stem. Cuticle very thick, with broad cuticular flanges extending in places
nearly the depth of anticlinal wall. Epidermal cells persistent, still present on 2year-old stem. Stomata deeply sunken; guard cells almost all perpendicular to
axis. Cortex: 3-6 layers densely packed palisade; inner cortex of larger colourless
cells, some elongated tangentially; periderm differentiating very late, just below
epidermis. Clusters of fibres in cortex; outside them 1-3 layers brachysclereids
forming complete cylinder. Xylem: vessels circular to oval, solitary or in short
radial lines or clusters; elements storied; intervascular pits vestured.
Fibre-tracheids with thick walls and intrusive ends. Vasicentric tracheids
present, slightly longer than vessel elements. Axial parenchyma abundant,
mainly apotracheal, sub-reticulate or in radial to diagonal lines one cell wide;
storied. Rays broad, multiseriate ( ~20 cells wide); cells mainly procumbent
with larger sheath cells, lignified. Crystals: druse crystals in cortex, some very
large ( ~90 Jlm diameter), often associated with brachysclereids; solitary
rhomboidal crystals in rays.
Results of carbon dioxide compensation point tests
Full results are given in Table 5. The readings fall into two clearly separated
groups: most of the species had carbon dioxide compensation points (r) of 45
volumes per million (vpm) or more, while zYgophyllum simplex, Tribulus terrestris,
TABLE
5. C0 2 compensation points m the
Zygophyllaceae
r
Species
Peganum harmala
M alacocarpus crithmifolius
Viscainoa genicula/a
Bulnesia arborea
Fagonia mollis
:(ygophyllum fahago
~· xanthoxylum
~. darvasicum
~·simplex
~·album
~· coccineum
~· stapffii
~· eremaeum
Guaiacum rifficinale
G. guatemalense
Porlieria hygrometra
P. chilensis
Larrea tridentata
Neo/uederitda sericeocarpa
Sisyndite spartea
Tribulus terrestris
T. zryheri
Ka//stroemia grandiflora
Nitraria schoberi
N. retusa
Balanites aegyptiaca
B. maughamii
in J.!IJ-I
I
II
60
55
52
60
60
60
55
62
51
60
52
5!
68
2
60
45
65
65
63
50
63
52
65
75
62
90
88
55
60
60
2
4
5
59
68
60
60
61
I
58
85
58
78
80
55
63
57
1
3
58
45
69
M. C. SHEAHAN AND D. F. CUTLER
253
T. ;::eyheri and Kallstroemia grandiflora had readings of 5 vpm or less. Together with
the presence in these species of a bundle sheath, this indicates that they are c4
plants. This is in accord with the findings of earlier investigations. The other
species tested, which do not possess a bundle sheath and have r of 45 vpm or
more, are assumed to be C 3 plants.
DISCUSSION
Anatomical features
Leaf
Vasculature. Venation type is recognized as important in leaf systematic studies
(Fisher & Evert, 1982; Hickey, 1973). In the leaves and leaflets the venation is of
the two types described. In the petiole, the commonest form of vasculature is a
central cylinder, or interrupted cylinder, with two or more much smaller veins,
either collateral or cylindrical, in the latera-adaxial position (Fig. 9A). In
general, departures from this pattern probably reflect ecological adaptation. In
Sisyndite spartea, for example, the anatomy of the petiole resembles that of the
photosynthetic stem; and in species with centric leaves the petiole anatomy is
similar to that of the leaflets. In both cases the petiole assumes the function of the
leaflets for a period if they are shed. Petioles of C 4 species may have some form of
Kranz tissue (Fig. 9C). In Balanites the adaxial part of the central vascular
system of the petiole is formed of two arcs-the phloem in one orientated
adaxially and in the other abaxially-and a separate abaxial arc; an
arrangement precisely described by Van Tieghem (1906); and there are no small
bundles in the latera-adaxial position (Fig. 9D).
Trichomes. These are present in many members of the family; they are mostly
unicellular and predominantly unbranched, with a straight body appressed to
the surface of leaf or stem. In Tetraena and a few species of zYgophyllum they are
two-armed, and in some species of zYgophyllum they have a flat lobed-stellate
upper part parallel to the leaf surface (Fig. 1A). However multicellular
trichomes were observed in P. harmala, M. crithmifolius and Fagonia mollis, and
have been reported in some species of zYgophyllum. Tribulus, Kallstroemia and
Kelleronia are unusual in having trichomes of two markedly different sizes: short
and pointed, or much longer and wider and growing from a basal 'plinth' of
epidermal cells (Fig. 1B).
Stomata. There are differences between the species in the disposition of the
surrounding epidermal cells as seen in surface view. The usual arrangement in
the family is anomocytic, that is without subsidiary cells (Hutchinson, 1967;
Montasir & Foda, 1955). Inamdar (1969) and Inamdar & Patel (1970)
recorded other forms in the family. Some are apparently paracytic or weakly
cyclocytic; these are particularly numerous in Balanites. In Peganum and
Malacocarpus stomata are found mainly among the smaller, less elongated
epidermal cells, which are separated by areas occupied only by elongated
epidermal cells (Fig. 2A). Wilkinson (1979) pointed out that, without a
knowledge of the ontogenetic pathway by which a particular arrangement was
reached, it is difficult to use these patterns to deduce systematic relationships.
However the stomatal arrangement in these two genera is so different from that
in other sections that it may well have some bearing on their systematic position
within the family.
254
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
Epidermal cell shape. The epidermal cells seen in surface view are most often
polygonal, sometimes with undulating anticlinal walls. However Peganum and
Ma{acocarpus are unusual in the family on account of their large elongated
epidermal cells (Fig. 2A).
Kranz anatomy. Leaves were examined for Kranz anatomy (used here to
indicate a concentric arrangement of the bundle sheath and the surrounding
mesophyll cells; see Laetsch, 1974), and the size, position and distribution of
chloroplasts in mesophyll and bundle sheath cells.
True Kranz anatomy, as defined above, was observed only in Tribulus terrestris,
T. zeyheri and Kallstroemia grandijlora. In these species there is a bundle sheath
encircling the veins, and the mesophyll cells are closely arranged round the cells
of this sheath (Figs 1OA, C; 15). In ,Z. simplex, as in some other species of
zYgophyllum (e.g. ,Z. album), the leaf is more or less cylindrical, the inner part of
the leaf taking the form of water storage tissue; the veins form a peripheral
network between the palisade and water storage cells. In ,Z. simplex there is a
single layer of palisade cells, and a sheath of closely packed cells seen in TS as
forming an arc, but not a complete cylinder, round the veins (Fig. lOB). The
C0 2 compensation tests indicated that ,Z. simplex, Kallstroemia grandijiora and the
two Tribulus species tested were all C 4 species.
Stem
Stomata. In the stem epidermis, before periderm differentiation, the guard cells
are usually oriented with the long axis parallel to the axis of the stem. However
in Balanites aegyptiaca and B. maughamii the guard cells are orientated
perpendicular to the axis, I.e. when the stem is vertical the long axis IS
horizontal.
Sclerenchyma. Stone cells or brachysclereids are a common feature of
zygophyllaceous stems. They are often intercalated between fibre bundle caps
(e.g. Bulnesia and Larrea), or in association with them. These cells probably
develop by lignification of parenchyma cells of the secondary phloem. In
Balanites, where they form a complete cylinder outside the fibres, they are less
clearly associated with phloem, and might have developed by lignification of
cortical cells. Peganum and Malacocarpus differ from other members of the family:
their pericyclic fibres have thinner, more angular walls with larger pits, and
sometimes form a complete cylinder.
Vessels. The commonest arrangement of vessels in secondary xylem is solitary
or in short radial chains; however, there is a tendency towards a dendritic
arrangement in some South American genera (Porlieria, Bulnesia). In Nitraria and
Balanites vessels are sometimes found in clusters as well as in short radial chains.
Nitraria is the only genus in which vessels in two distinct size classes were seen
(Fig. 12).
Balanites is alone among the genera studied in having vestured intervascular
pits, which is a valuable diagnostic and taxonomic character (Carlq uist, 1988).
Imperforate elements. The cells associated with vessels in most species consist
mainly offibre-tracheids, and in some species (e.g. Bulnesia, Nitraria) oflibriform
fibres (definitions according to Wheeler et al., 1989). In practice there is an
intergradation between the two types; the fibre-tracheids of Fagonia represent
one extreme, having numerous large distinctly bordered pits, while those of
Kallstroemia and Tribulus tend towards libriform fibres.
M. C. SHEAHAN AND D. F. CUTLER
255
Axial parenchyma. This is predominantly diffuse apotracheal, and scanty
paratracheal. However, in Nitraria it is paratracheal aliform-confluent, forming
concentric bands.
Rays. These are mostly 1-2-seriate (rarely 3-4, as in N. retusa). In Balanites the
rays are broad, up to 20 cells wide, and also higher than in the rest of the
Zygophyllaceae.
Storying is common, though not universal, throughout the family in vessel
members and axial parenchyma. In some genera the rays are also storied (Fig.
13).
In both leaf and stem
Mucilage cells. Mucilages were found in the leaf epidermis of Augea, and have
been reported in the leaf epidermis of Peganum and Plectrocarpa (Castro, 1981;
Volkens, 1887). Mucilage cells were apparent in the leafmesophyll of N. schoberi
and N. retusa; there were also abundant large mucilage cells and cavities in the
cortex and phloem of these species (Fig. 14). Mucilage cells were not found in
these positions in any other genera; and this may provide some additional
evidence of the isolation of this genus within the family (see Gregory & Baas,
1989).
Crystals. Types of crystal can be of diagnostic importance, although the
frequency of occurrence is of more ecological than taxonomic interest. Crystals
are found abundantly in the Zygophyllaceae; only three species examined had
no crystals in either leaf or stem. Almost all the types described in the literature
are present. The commonest form is druse crystals, some in idioblastic cells; there
are also small acicular crystals, and rhomboidal and styloid crystals; the last two
are sometimes solitary, and sometimes more than one to a cell. However
raphides were seen only in Peganum and Malacocarpus.
Taxonomic implications
Peganoideae (Peganum, Malacocarpus)
Several features distinguish these two genera from the rest of the family: large
stomata, the presence of raphides, and elongated leaf epidermal cells alternating
with shorter cells (Fig. 2A); in the stem, the presence of a hypodermis, angular,
thin-walled pericyclic fibres, and the absence of brachysclereids. There are also
morphological differences, especially the pinnatisect leaf. Pantanelli ( 1900) drew
attention to the poorly developed stem xylem in comparison with other members
of the family. He also considered that the absence of stipules in Peganum was
another distinguishing feature; there are, in fact, minute setaceous stipules on
some leaves, although they are usually absent in Malacocarpus. The presence of
stipules provides a further reason for excluding Peganum from the Rutaceae,
which lack stipules altogether.
It may be that these two species should constitute a separate family as
proposed by Takhtajan (1969) and Dahlgren (1980).
Morkillioideae (Morkillia, Viscainoa)
There is little to distinguish Viscainoa and Morkillia anatomically from the
central group of the Zygophylloideae. The supposedly distinguishing feature of
imparipinnate leaves (Engler, 1896b; El Hadidi, 1975) is also found in Fagonia,
256
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
Seet;:enia and Neoluederit;:ia within the Zygophylloideae; in any case this difference
may not be significant, since many paripinnate species of the family have a
vestigial terminal leaflet at the end of the rachis (e.g. Guaiacum, ,Qgophyllum).
According to Poggio ( 1978), Viscainoa and Morkillia have the same chromosome
base number (x = 13) as Larrea, Porlieria and Plectrocarpa in the Zygophylloideae.
The main anatomical differences are that these genera have more collenchyma
round the leafvein, and few, rather slender, terminal tracheoids. On anatomical
grounds there seems no reason to exclude them from the Zygophylloideae.
Tetradiclidoideae (Tetradiclis)
The absence of detailed anatomical results for this group was disappointing.
The brief description of the anatomy of the leaf by Chermezon ( 1910) does not
contain features which would set it apart from the rest of the family, and they do
not seem to indicate a particular affinity with the peganoid genera; indeed the
mesophyll arrangement he described appears to resemble the centric leaves of
Augea and some ,Qgophyllum species rather than those of Peganum and
Malacocarpus, in which the vein network is in the central plane of the lea(
Augeoideae (Augea)
In its leaf anatomy Augea shares several features with the species of ,Qgophyllum
which have centric leaves; e.g. a single slender vascular bundle in the centre of
the leaf, surrounded by water storage tissue and connected to a network of
slender peripheral veins, and abundant brachysclereids. One difference is the
extreme degree of succulence of this genus, which has a considerable volume of
water storage tissue in leaf and stem.
The anatomical similarities between Augea and ,Qgophyllum support the
inclusion of Augea in the Zygophylloideae, as suggested by Engler ( 1896b) and El
Hadidi (1975).
,Qgophylloideae (Zygophyllum, Fagonia, Bulnesia, Guaiacum, Porlieria, Larrea,
Pintoa, Plectrocarpa, Tribulus, Kallstroemia, Neoluederitzia, Sisyndite)
On the whole, the anatomy of this central group is fairly homogeneous.
,Qgophyllum is the type genus. It is characterized by thick leaves, often with some
water storage tissue, thin cuticle and epidermis, amphistomaty, slender veins,
thin-walled mesophyll cells, and little or no leaf sclerenchyma, apart from the
tracheoids associated with the vein endings. In the stem, periderm differentiates
towards the inner cortex, and there are frequently brachysclereids associated
with the fibres in the cortex. Xylem elements tend to be heavily lignified; vessels
are mostly solitary.
,Z. simplex is the most outstanding species, on account of both its leaf anatomy
and its different photosynthetic pathway. In her scheme of relationships within
the genus, Van Huyssteen (1937) agreed with Engler (1896b) that ,Z. simplex
belonged in subgenus Agrophyllum (whose members are found mainly in
Africa), which she considered to be the oldest group within the family. She
regarded ,Z. simplex as being of ancient origin, because it is both polymorphic and
widespread, providing a link between the northern and southern African species
of ,Qgophyllum. The development of the C 4 syndrome is considered to be a
relatively recent evolutionary event (Peisker, 1986). The Kranz anatomy of the
leaflet appears to be at an early stage of evolution (Brown, 1975), and it seems
M. C. SHEAHAN AND D. F. CUTLER
257
probable that -(;'. simplex in its present form is of recent evolutionary origin. A
similar inference was made by Carolin et al. ( 197 5), concerning members of
Chenopodiaceae.
In many features, the anatomy of-(;'. simplex resembles that of other species of
zYgophyllum, and it should probably be left in the genus. Possession of the C4
pathway may not in itself be grounds for separating a species from other taxa
with which it otherwise shares many similarities. However the different leaf
anatomy associated with C 4 photosynthesis might justify Engler's (1896a)
original separation of this species into a separate section.
Other genera in this subfamily show similar anatomical features to
zYgophyllum. Fagonia is the second largest genus in the family, with 30 to 40
species. Anatomically it resembles zYgophyllum in many respects, especially in
wood anatomy. The main difference is the distinctive arrangement of bundles of
fibre strands in the stem cortex, which El Hadidi ( 1975, 1977) said were useful in
the delimitation of species within the genus. Overall, however, the differences are
slight, and do not warrant a change in the existing position of this genus.
Bulnesia, Guaiacum, Porlieria and Larrea are the New World genera of Engler's
Zygophylloideae, placed by him in l896b in their own subtribe Guajacinae, but
in Engler ( 1931) they were put with zYgophyllum in the subtribe Zygophyllinae.
They are close in the flower, fruit and seed features which Engler used as the
basis for his classification, and they are also similar in many anatomical features.
The main differences relate to their different growth form. They are tall shrubs
and trees, with thinner leaves and thicker cuticle than in zYgophyllum; but have
similar petiole vasculature and frequently similar veinlet termination tracheoids.
The secondary xylem is more developed, and some genera (Bulnesia, Guaiacum)
have a high proportion of libriform fibres; but in other respects the wood shows
similarities with that of zYgophyllum, with mainly solitary vessels, low narrow
rays, and scanty, mostly apotracheal axial parenchyma. On anatomical grounds
there seems no reason to exclude them from the Zygophylloideae.
Reference was made in the introduction to El Hadidi's view (1975, 1977) that
his tribuloid genera ( Tribulus, Kallstroemia, Kelleronia, Tribulopis) and
neoluederitzioid genera (Neoluederit;:.ia, Sisyndite) should be separated from the
zygophylloid genera on the grounds that the two former groups are mainly
herbaceous, with alternate leaves and no stipules. Neoluederit;:.ia and Sisyndite
have alternate leaves, but they are in fact both stipulate and woody. The species
of Tribulus and Kallstroemia studied here had stipules and opposite though
unequal-sized leaves. If, as often happens, the smaller leaf falls before the larger,
the habit may appear alternate; but this is true of several other species in the
Zygophylloideae which have opposite leaves.
Anatomically Tribulus and Kallstroemia show some differences from the other
Zygophylloideae: they were the only genera studied to have two distinct sizes of
trichome; their petiole vasculature is distinctive; and in the stem there is an
unusual arrangement of broad radial bands of vessels and fibres; in this they
resemble Neoluederit;:.ia but not other Zygophylloideae. The chief difference
however is in the Kranz arrangement of the mesophyll: the distinct bundle
sheath and abaxial layer of water storage cells have no counterpart in the rest of
the family. These differences, and the fact that Tribulus and Kallstroemia are C 4
plants (only one species of Kallstroemia has been reported as being C 3 : see
Robbins, 1974), lend support to the suggestion ofEl Hadidi (1977) and Saleh et
258
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
al. ( 1982) that they should be separated from the Zygophylloideae, at least at
subfamily level.
Neoluederitzia and Sisyndite are among the most interesting and the most
difficult to place. They are isolated geographically, both endemic to the Namib
desert in south-western Africa. There are resemblances between the two in flower
and fruit characters (although Neoluederitzia is unusual in the family in being
dioecious). They both have alternate branching and similar pollen types
(Praglowski, 1987). However, Sisyndite is unlike Neoluederitzia in its reduced leaves
and absence of trichomes, and in its specialized leaf axis anatomy; it also lacks
the axillary thorns of Neoluederitzia.
These two genera have some features in common with the tribuloid genera in
flower and fruit characters. Neoluederitzia also has a similar distinctive radial
arrangement of vessels and fibres in the stem wood. They are unlike in habit
(Neoluederitzia and Sisyndite are shrubs, and have alternate branching) and in
pollen (Praglowski, 1987), and some researchers have also found differences in
biochemistry (Saleh et al., 1982). Crookston & Moss ( 1972) suggested that it
might be possible to elucidate the relationships of this group by finding out
which of them were C 4 plants. The C0 2 compensation point tests, and the lack of
true bundle sheath anatomy, show that both species are in fact c3 plants, while
Tribulus and Kallstroemia are C 4 • This supports the separation of Neoluederitzia and
Sisyndite from the tribuloid genera. Pollen studies also suggest that these two
species have more affinity with members of the Zygophylloideae than with the
tribuloid genera (Praglowski, 1987), although one must agree with El Hadidi
(1975) that Engler's Zygophylloideae form a somewhat heterogeneous group.
Nitrarioideae (Nitraria)
Several anatomical observations supplement the morphological differences
already outlined. Mucilage, elsewhere in the family found mainly in leaf
epidermis and seeds, is abundant in cells and cavities in the leaf and stem. In the
stem, there is an unusually extensive development of secondary phloem
parenchyma (Fig. 14). In the wood, there is abundant aliform-confluent axial
parenchyma and, in N. retusa, the vessels are in two different size classes (Fig.
12). These features are not found in any other groups within the family, and
support the separation of this genus from the rest of the family.
Balanitoideae (Ba1ani tes)
There are some morphological similarities between this genus and the other
Zygophyllaceae, apart from the bipinnate leaves already mentioned. Axillary
thorns, for example, appear in other members of the family (Neoluederitzia and
Plectrocarpa). Stipules, present in the Zygophyllaceae, are reported to be absent in
Balanites (e.g. by Zohary, 1972; Hutchinson, 1973), but there are in fact minute
pointed stipules on either side of the petiole in the youngest leaves of the plants
studied here, albeit caducous and extremely small. Engler (l896a) also observed
stipules, as did Sands ( 1989).
However, the fruit of Balanites is a fleshy drupe, with some similarity to that of
Nitraria, but unlike the capsular and schizocarpic fruits of .?,ygophyllaceae. There
are differences in the pollen (Agababyan, 1964). The anatomy of the leaf shows
many dissimilarities to that of other Zygophyllaceae: the cuticle is very thick, the
stomata are sunken with a raised rim, and in surface view the type of the stomata
M. C. SHEAHAN AND D. F. CUTLER
259
is more varied: there are more cyclocytic and paracytic stomata than
anomocytic, which is the commonest form in the Zygophyllaceae. The petiole
vasculature is also distinctive.
In the stem, the stomata are perpendicular to the longitudinal axis; this is an
unusual feature which was not seen in other members of the Zygophyllaceae.
It is in features of the wood that there are considered to be the most significant
differences between Balanites and the Zygophyllaceae. There are several
similarities: small intervessel pits (although they are slightly larger in Balanites
than in Zygophyllaceae); the mainly diffuse apotracheal arrangement of the
fusiform axial parenchyma; abundant thick-walled fibre-tracheids with bordered
pits; the presence of vasicentric tracheids; and storying of some elements.
However the main differences, which are held to be of great taxonomic
importance, are the height and width (up to 20 cells wide) of the xylem rays in
Balanites, and the vestured pits; also the vessels sometimes occur in clusters,
which is not the case with any other members of the family except to a lesser
extent in Nitraria.
Taken together the differences in anatomy indicate that there are considerable
discontinuities between Balanites and other members of the Zygophyllaceae,
which would lend some support to the views of those who think that this genus
should constitute a separate family.
The Zygophyllaceae share some anatomical characters with members of other
typical families within the Geraniales, such as predominantly anomocytic
stomata and small often solitary vessels with small inter-vascular pits. There are
raphide sacs in some families, as there are in Peganum and Malacocarpus.
However there are differences: members of the Geraniales often have a welldefined ring of sclerenchymatous fibres in the stem cortex. In the
Zygophyllaceae only Balanites and Peganum have this feature; other members of
the family have separate fibre strands, sometimes interspersed with groups of
stone cells, and the dilated vein endings which are common among the
Zygophyllaceae are lacking in the Geraniales (except the Oxalidaceae).
Storying, common in the Zygophyllaceae, is absent in most Geraniales.
Petiole anatomy is also different: the typical zygophyllaceous petiole has a
central cylinder or interrupted cylinder, with two or more smaller bundles in the
latero-adaxial position. In members of the Geraniales the petiole usually has a
ring (an arc in the Balsaminaceae) of separate bundles. (Anatomy details from
Metcalfe & Chalk, 1950.) Clearly it is not easy to draw firm conclusions about
the relationship of the Zygophyllaceae to other families within the Geraniales on
anatomical evidence alone.
CONCLUDING REMARKS
In summary, the anatomical evidence of this study suggests that:
(1) Balanites should constitute a separate family Balanitaceae (as is generally
accepted).
(2) Anatomically there is little to separate the Morkillioideae from the
Zygophylloideae.
(3) The monotypic species Augea capensis is close to <)gophyllum, and should be
included in the subfamily Zygophylloideae.
260
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
(4) :(ygophyllum simplex is probably of relatively recent evolutionary ongm,
rather than ancestral to the genus.
(5) Peganum and Malacocarpus show many distinctive features, and should be
assigned to a separate family Peganaceae.
(6) There is evidence that the tribuloid genera Tribulus, Kallstroemia and
Kelleronia should be separated from the zygophylloid genera, at least at subfamily
level; however Neoluederitzia and Sisyndite should remain in the Zygophylloideae.
(7) There seems little doubt that Nitraria does not have very close affinities
with the rest of the family.
ACKNOWLEDGEMENTS
This work was funded in part by the Science & Engineering Research Council
(award no. 85313771). We are glad to acknowledge help and advice from Dr K.
Alvin and Dr A. Goldsworthy at the Imperial College of Science and
Technology, University of London.
REFERENCES
Agababyan VS. 1964. Morphological types of pollen and systematic classification of the Zygophyllaceae.
hvestiya Akademii .Nauk Armyanskoi, SSR, Biologicheskikh .Nauk 17: 39-45.
Apel P. 1988. Some aspects of the evolution of C, photosynthesis. Kulturpflan::.e 36: 225-236.
Barbour MG, CWlllingham G, Oechel WC, Bamberg SA. 1977. Growth and development, form and
function. In: Mabry TJ, Hunziker JH, DiFeo DR Jr, eds. Creosote bush: biology and chemistry of Larrea in .New
World deserts. Stroudsberg, Pennsylvania: Dowden, Hutchinson and Ross.
Bentham G, Hooker JD. 1862. Genera Plantarum, I. London: Pamplin.
Brown WV. 1975. Variations in anatomy, associations and origins of Kranz tissue. American Journal rif Botany
62: 395--402.
Car1quist S. 1988. Comparative wood anatOI'!Y· Berlin, N.Y. & London: Springer Verlag.
Carolin RC, Jacobs SWL, Vesk M. 1975. Leaf structure in Chenopodiaceae. Botanische Jahrbucher fiir
Systematik, Pflan::.engeschichte und Pflan;;engeographie 95: 226-255.
Castro MA. 1981. Anatomia foliar del genera Plectrocarpa. Lilloa 35: 137-147.
Chermezon H. 1910. Recherches anatomiques sur les plantes littorales. Annales des Sciences Naturelles Botaniques
12: 117-313.
Cronquist A. 1968. Evolution and classification rifflowering plants. London & Edinburgh: Thomas Nelson.
Cronquist A. 1981. An integrated system of classification offlowering plants. New York: Columbia University Press.
Crookston RK, Moss DN. 1972. C, and C, carboxylation characteristics in the genus .Qgophyllum. Annals of
the Missouri Botanic Garden 59: 465--4 70.
CWlllingham LM. 1927. Observations on the structure of .Qgophyllum fabago L. Transactions of the Botanical
Sociery rif Edinburgh 29: 353-361.
Dahlgren R. 1980. A revised system of classification of the angiosperms. Botanical Journal of the Linnean Sociery
80:91-124.
Das VSR, Raghavendra AS. 1973. A screening of the dicot weed flora for the occurrence of the C,
dicarboxylic acid pathway of photosynthesis. Proceedings rif the Indian Academy rif Science 77: 93-100.
De Candolle AP. 1824. Prodromus, I. Paris: Treuttel and Wiirtz.
Delile, AR. 1813. Description de l'Egypte, 2.
Desco1e HR, O'Donell CA, Lourteig A. 1940. Revision de las Zigofilaceas Argentinas. Lilloa 5: 257-352.
Downton WJS, Treguaaa EB. 1968. CO, compensation--its relation to photosynthetic carboxylation
reactions, systematics of the Graminae, and leaf anatomy. Canadian Journal rif Botany 46: 207-215.
Elgin N. 1950. Les caracteres morphologiques et anatomiques du Peganum harmala L. (Zygophyllaceae). Revue
de Ia Faculte de Science de l' Universitt d' Istanbul, sir. B 15: 333-361.
El Hadidi MN. 1966. Anatomical features of the stem in Egyptian species of Fagonia L. Cando/lea 21: 35 7-364.
El Hadidi MN. 1975. Zygophyllaceae in Africa. Boissieria 24: 317-323.
El Hadidi MN. 1977. Tribulaceae as a distinct family. Publications from the Cairo Universiry Herbarium 7-8:
103-108.
Engler A. 1896a. Zygophyllaceae. In: Engler A, Prantl K, eds. Die natiirliche Pflan;;erifamilien, 1st edition, Vol.
3, Section 4. Leipzig: Engelmann.
Engler A. 1896b. tJber die geographische Verbreitung der .Qgophyl/aceen. Berlin: Kiiniglich Akademie der
Wissenschaften.
M. C. SHEAHAN AND D. F. CUTLER
261
Engler A. 1931. Zygophyllaceae. In: Engler A, Prantl K, eds. Die natiirliche Pflanzerifamilien, 2nd edition, Vol.
19a, Section 2. Leipzig: Engelmann.
Erdtman G. 1952. Pollen morphology and plant taxonomy. Waltham, Mass.: Chronica Botanica.
Feder N, O'Brien TP. 1968. Plant microtechnique-some principles and new methods. American Journal rif
Botany 55: 123-142.
Fisher 00, Evert RF. 1982. Studies on the leaf of Amaranthus reflexus. American Journal rif Botany 69: 1133-1147.
Foster A. 1953. Techniques for the stut!J rif venation patterns in the leaves rif angiosperms. Proceedings of the 7th
International Botanical Congress, Stockholm ( 1950).
Gamaley YV. 1984. Leaf morphology and anatomy of Gobi desert plants. Botanical Journal of the USSR 69:
569-584.
Glaser de Banus SD. 1981. Anatomia foliar comparada de las especies del genera Bulnesia (Zygophyllaceae).
BoleHn de Ia Sociedad Argentina de Botdnica 20: 53-69.
Goldsworthy A, Day PR. 1970. A simple technique for the rapid determination of plant CO, compensation
points. Plant Physiology 46: 850-851.
Gregory M, Baas P. 1989. A survey of mucilage cells in vegetative organs of the dicotyledons. Israel Journal rif
Botany 38: 125-174.
Haberlandt G. 1914. Physiological plant anatomy (English translation of 4th German edition). London:
Macmillan.
Hegaauer R. 1973. Chemotaxonomie der Pflanzen, 6. Basel & Stuttgart: Birkhauser.
Heywood VH. 1978. Flowering plants of the world. Oxford, London & Melbourne: Oxford University Press.
Hickey LJ. 1973. A classification of the architecture of dicotyledonous leaves. American Journal rif Botany 60:
17-33.
Hutchinson J. 1967. The genera rif flowering plants, 2: Dicotyledones. Oxford: Clarendon Press.
Hutchinson J. 1973. The families rif flowering plants. Oxford: Clarendon Press.
huundar JA. 1969. Epidermal structure, stomatal ontogeny and relationship of some Zygophyllaceae and
Simaroubaceae. Flora 158: 360-368.
huundar JA, Patel RC. 1970. Epidermal structure and development of stomata in Fagonia cretica. Flora 159:
63-70.
Johansen DA. 1940. Plant microtechnique. New York & London: McGraw Hill.
Jonsson B. 1902. Der anatomischen Baues der Wiistenptlanzen. Lunds Universitets Arsskrift 38: 1-61.
Kurth E. 1978. A modified method for clearing leaves. Stain Technology 53: 291-293.
Laetsch WM. 1974. The C, syndrome: a structural analysis. Annual Review rif Plant Physiology 25: 27-52.
Lawrence GH. 1960. Taxonomy of vascular plants. New York: Macmillan.
Maksoud SA, El Hadidi MN. 1988. The tlavonoids of Balanites aegyptiaca from Egypt. Plant Systematics and
Evolution 160: 153-158.
Metcalfe CR, Chalk L. 1950. Anatomy rif the Dicotyledons. Clarendon Press: Oxford.
_
Montasir A, Foda H. 1955. Structure and reproduction of :(ygophyllum album L. Bulletin de I' lnstitut d' Egypte 37:
137-151.
Narayana L, Satyauarayana P, Radhakrishnaiah H. 1990. Systematic position of Balanitaceae. In:
Bilgrami K, Dogra J, eds. Phytochemistry and plant taxonomy. Delhi: C.B.S. Publications.
Pantanelli E. 1900. Anatomia fisiologica delle Zygophyllaceae. Atti della Societii dei Natura/isla e Matematici di
Modena, ser. 4 2: 92-181.
Parameswaran N, Conrad H. 1982. Wood and bark anatomy of Balanites aegyptiaca in relation to ecology
and taxonomy. lAWA Bulletin, n.s. 3: 75-88.
Peisker M. 1986. Models of carbon metabolism in C,-C, intermediate plants as applied to the evolution of C,
photosynthesis. Plant, Cell, Environment 9: 627-635.
Poggio L. 1978. Estudios cromos6micos en Bulnesia, Pintoa, Porlieria, Plectrocarpay Sericodes (Zygophyllaceae).
Darwiniana 21: 139-151.
Porter DM. 1974. Disjunct distributions in the New World Zygophyllaceae. Taxon 23: 339-346.
PraglowskiJ. 1987. Pollen morphology ofTribulaceae. Grana 26: 193-211.
Robbins MJ. 1974. Origin and number of times the Kranz syndrome and C, photosynthesis evolved in each of
ten families of the angiosperms (unpublished thesis, University of Texas at Austin).
Ronse Decraene LP, Smets EF. 1991. Morphological studies in Zygophyllaceae. I. The floral development
and vascular anatomy of Nitraria retusa. American Journal rif Bota'!)l 18: 1438-1448.
Runyon EH. 1934. The organization of the Creosote bush with respect to drought. Ecology 15: 128-138.
Sabnis TS. 1920. The physiological anatomy of the plants of the Indian Desert. Journal of Indian Botany 1:
183-205.
Saleh N, El Hadidi MN, Ahmed A. 1982. The chemosystematics of Tribulaceae. Biochemical Systematics and
Ecology 10: 313-317.
Sands M. 1989. Balanitaceae. In: Hedberg I, Edwards S, eds. Flora of Ethiopia, 3. Ethiopia: Addis Ababa
University and Sweden: Uppsala University.
Scholz H. 1964. Zygophyllaceae. In: Melchior H, ed. A. Engler's Syllabus der Pflanzenfamilien, 12th edition, Vol.
2. Berlin: Borntrager.
Solereder H. 1908. Systematic anatomy rif the dicotyledons [translation of 1899 German edition]. Oxford:
Clarendon Press.
262
ANATOMY AND SYSTEMATICS OF THE ZYGOPHYLLACEAE
Takhtajan A. 1969. Flowering plants: origin and dispersal. Edinburgh: Oliver & Boyd.
Takhtajan A. 1980. Outline of the classification of flowering plants (Magnoliophyta). Botanical Review 46:
225-359.
Takhtajan A. 1983. The systematic arrangement of dicotyledonous families. In: Metcalfe CR, Chalk L, eds.
Anatm1ry rif the dicoryledons, 2nd edition, Vol. 2. Oxford: Clarendon Press.
Tregwma EB, Smith BN, Berry JA, Downton WJS. 1970. Some methods for studying the photosynthetic
taxonomy of the angiosperms. Canadian Journal rif BotaTI:) 48: 1209-1214.
Van Huyssteen DC. 1937. Morphologisch-systematische Studien tiber die Gattung :Qgophyllum. Dissertation
der Mathematisch-Natiirwissenschaftlichen Fakultiit der Friedrich-Wilhelms Universitii.t zu Berlin.
Van TiegheJD P. 1906. Surles Agialidacees. Annales des Sciences Naturelles, sir. 4 9: 223-260.
Vasilevskaya VK, Petrov MP. 1964. The central Asian endemic Tetraena mongolica Maxim. Botanical Journal
of the U.S.S.R. 49: 150&--1513.
Volkens G. 1884. Zur Kenntniss der Beziehungen zwischen Standort und anatomischen Bau der
Vegetationsorgane. Jahrbuch des Koniglichen botanischen Gartens 3: 1-46.
Volkens G. 1887. Die Flora der Aegyptisch-Arabischen Wiiste. Berlin: Borntrager.
Welkie GW, Caldwell M. 1970. Leaf anatomy of species in some dicotyledon families as related to the C 3 and
C4 pathways of carbon fixation. Canadian Journal rif Botany 48: 2135-2146.
Wheeler EA, Baas P, Gasson P, eds. 1989. IAWA list of microscopic features for hardwood identification.
IAWA Bulletin, n.s. 10: 219-332.
Wilkinson HP. 1979. The plant surface (mainly leaf). In Metcalfe CR, Chalk L, eds. Anatomy of the dicoryledons,
2nd edition, Vol. I. Oxford: Clarendon Press.
Willis JC. 1931. ,4 dictionary of the.flowering plants and ferns, 6th edition. Cambridge: Cambridge University Press.
Xi Y, Zhou S. 1989. Pollen morphology and its exine ultrastructure of the Zygophyllaceae in China. Botanical
Research (China) 4: 75-86.
Xi Y, Zhou S. 1992. A contribution to the pollen morphology of Tetraena and Malpighiaceae, with discussion
of the affinity and taxonomic position of Tetraena. Chinese Journal rif BotaTI:) 4: 6-12.
ZeJDke E. 1939. Anatomische Untersuchungen der Namibwiiste. Flora, n.s. 33: 365-416.
Zohary M. 1972. Flora Palaestina, 2. Jerusalem: Israel Academy of Sciences and Humanities.