Pak. J. Bot., 55(6): 2351-2367, 2023. DOI: http://dx.doi.org/10.

30848/PJB2023-6(34)

SEEDLING STRUCTURE AND SURFACE MICROMORPHOLOGY

OF STERCULIA FOETIDA L. (MALVACEAE)
D. KHAN AND RUBINA ABID

Department of Botany, University of Karachi, Karachi-75270, Pakistan

Email: [email protected]

Abstract

The seedling structure and surface micromorphology of Sterculia foetida L. (Malvaceae) is described. Seedling of S.
foetida may be Phanerocotylar-epigeal - Reserve type or Cryptocotylar – hypogeal - Reserve type. When aboveground,
cotyledons unfolded, expanded and turned green on exposure to sun, developing dense crop of trichomes. The whole seedling
surface was trichomatous. Cotyledonary trichomes were conical and multicellular. Some four kinds of trichomes were observed
on leaflets. 1) Long, apically pointed non-glandular unicellular (acicular) trichomes – predominantly abundant. 2) Long,
apically curved or hooked, unicellular or uniseriate multicellular trichomes. 3) Long apically club- shaped, Bicellular, uniseriate
glandular trichomes. 4) Dark globular (ball-like, peltate) glandular trichomes on the midrib. Epidermal cells in cotyledons were
polygonal and straight in anticlinal contour. The adaxial epidermis of leaf was with straight to curvy anticlinal walls and
abaxially the epidermal cells were sinuous and irregular in shape. A diversity of stomatal complexes was recorded on
cotyledons and leaflets. Stomatal density was lesser on cotyledonary sun-exposed surface than that of leaflets. Leaflets were
hypostomatous. Foliar stomatal density varied with the size of leaflets. Stomatal density in the smallest leaflet of 184 mm2 was
249.14 ± 5.54 (varying from 157.26 to 324.36 stomata per mm2, CV: 14.05%) and 125.22 ± 3.449 stomata per mm2 in the
largest leaflet (4709 mm2). Stomatal size inclusive of normal and giant stomata averaged to 21.15 ± 14.86 µm x 14.86 ± 0.176
µm (L x W) in 265 observations. It may be concluded that S. foetida is quite rich in trichomal and stomatal diversity.

Key words: Sterculia foetida L., Seedling structure, Surface micromorphology, Trichomes and Stomatal complexes.

Introduction accumulates K in leaves (Lustosa et al., 2017). The

environment of 50% shading was found to be most suitable
Sterculia foetida L. (Vern. Names: Homrong or to produce S. foetida seedling even under salinity of 5.1
Hamrong, Marong, Chammahong, Samrong, Java Olive, dS.m-1 (Lima et al., 2018). In India, a leaf rolling insect
Jangli Badam Pinari, Bastard Poon nut, Hazel Sterculia, wild (Sylepta balteata) is a serious pest (http://www.
Indian almond, Skunk tree, Banksho Badam, Kalumpang nparks.gov.sg/florafaunaweb).
etc.), a multipurpose tropical deciduous tree of ornamental The structure and surface micromorphology of seedlings
and medicinal value, belongs to family Malvaceae (former or mature plants are very useful taxonomic tools to
Sterculiaceae). The genus Sterculia was named after the characterize plants. Recently, structure and distribution of
Latin god Sterculius = god of fertilizer and manure and heteromorphic stomata in a malvaceous species, Pterygota
species name comes from the foul-smelling flowers and alata (Roxb.) R. Br have been studied by Mitra et al., (2015).
leaves of some species of genus Sterculia. The genus To our knowledge, no such studies have been undertaken in
comprises some 300 species (Thabet et al., 2018). It is S. foetida. The present paper, therefore, describes the
distributed in India, Taiwan, Indo-China, Philippines, seedling structure and surface micromorphology of this
Hawaii, Indonesia, Australia, and some African countries – species when raised in pots under irrigation.
now cultivated on small scale in Pakistan (Fig. 1). During
flowering phase, it is prominent and presents a brilliant sight Materials and Methods
due to orange red flowers against leafless state of the plant.
The fruits are capsules - red and lobed (Fig. 1B, C). A fruit Seeds: The seeds of Sterculia foetida were provided by
contains 10-15 seeds (Sudrajat et al., 2018). There are two Dr. M. Azeem, department of Botany, University of
shells of seed. The outer shell is brown and the inner shell
Karachi. The weight of air-dried seeds selected to sow (N
black. The kernel is pale brown. Seed morphology and its
= 30) for germination averaged to 2.785 ± 0.08123g
taxonomic significance in Family Malvaceae have been
described by Abid et al. (2016). The Seeds of S. foetida are varying from 1.373 to 3.696g per seed (CV= 15.98%).
edible but purgative. Sterculia seed oil is a high-quality oil of Some 63.4% of seeds belonged to the size class of 2.51 -
oxidative stability and potentially edible and used in the food 3.0g and 23.3% to the size class of 3.1-4g.
industry (Chanyawiwatkul et al., 2018). Seed oil, according
to Verma et al. (1957) contains 71.8% Sterculic acid and Seedling procurement: To procure seedlings, the seeds
minor proportion of oleic and linoleic acids. Empty fruits and were sown in plastic pots (five seeds per pot) under shade
seeds are rated as excellent sources of thermal energy in, in the first week of April, 2022 at Karachi. Pots
(Vaishnavi and Pugazhvadivu, 2017). Seeds extract is contained sandy loam soil with compost manure. Prior to
reported to be anti-termite (Amuthavalli et al., 2020). It is a sowing, the seeds were sterilized with 1% sodium
species of potential therapeutic value (Thabet et al., 2018). hypochlorite solution, rinsed and submerged in water for
Its leaves can be used as fodder. 2 h. The pots were arranged in completely randomized
It may be planted in areas with low rainfall and air design under the green shade at 30 ± 2 oC.
temperature up to 40-45oC (Nhan et al., 2019). Its wood is
easy to cut but not durable. Gum karaya exudates from the Seedling emergence: Seedlings began emerging within a
stem of the tree. It has some tolerance to salinity and week quite synchronously.
2352 D. KHAN & RUBINA ABID

Seedling micromorphology: The seedling type was Table 1. Leaf morphometry of Primary, secondary and tertiary
described according to Garwood (1996). Hickey (1973) and leaves of 20-day old seedlings of S. foetida.
Leaflet area Total leaf
Ash et al. (1999) for description of leaf. The impressions of Leaflets LL LW
(mm2)
AA (o) BA (o)
area (mm2)
surface of leaflets were made with clear nail polish Wang et Primary leaf (Petiole length: 4.1 cm)
al. (2006). The nail polish imprints were studied under Leaflet 1 6.9 2.4 960 46 57
compound optical microscope for ornamentation and micro- Leaflet 2 7.3 2.2 964 47 48
morphological structures. Stomatal nomenclature suggested Leaflet 3 7.5 3.1 894 44 40 4709
by Metcalfe and Chalk (1950), Van Cotthem (1970), Dilcher Leaflet 4 8.0 2.3 1102 55 58
Leaflet 5 6.9 2.0 729 44 52
(1974), Wilkinson (1979), Carpenter (2005) and that Mean leaflet area = 929.8 ± 25.12 mm2
presented by Mitra et al. (2015) for stomatal description in Secondary leaf (Petiole length = 3.7 cm)
Pterygota alata (Roxb.) R. Br. (Family Malvaceae, formerly Leaflet 1 5.0 1.4 450 50 55
Sterculiaceae), Sabo et al. (2007) for genus Arum, Surat un Leaflet 2 7.4 2.0 857 45 55
Nisa et al. (2019) for Vincetoxicum arnottianum (Fam. Leaflet 3 7.6 2.2 1138 51 48 4359
Apocynaceae), and Den Hartog née Vanter Tholan and Baas Leaflet 4 7..4 1.9 693 36 40
Leaflet 5 8.0 2.0 1147 52 44
(1978) for Celastraceae were followed to ascertain stomatal Mean leaflet area = 857 .0 ± 133.35 mm2
types. Stomatal size was measured microscopically at 45 x Tertiary leaf (Petiole length = 1.2 cm)
10 X magnification. The data on stomata and trichomes was Leaflet 1 10 - - - -
analyzed statistically. Leaflet 2 24 - - - -
Leaflet 3 20 - - - - 101
Results and Discussion Leaflet 4 21 - - - -
Leaflet 5 12 - - - -
Seedling: The seedlings were obtained from seeds Mean leaf area per seedling = 9169 mm2
varying from 1.373 to 3.696g per seed which were more Acronyms: LL, Leaflet length (cm), LW, leaflet width in cm (widest point),
AA, apex angle, BA, base angle,
or less comparable to the size of single seed reported from Leaf area was determined as sum of the areas of the leaflets of a leaf
Indonesia (2.89 ± 0.64 to 4.05 ± 0.52g (Sudrajat et al., estimated by drawing their accurate outlines on graph paper.
2018). The maximum emergence was recorded to be c
60%. Germination in soil was also reported to start in a Leaves: Leaf base was swollen with two spinous conical
week reaching to 70% by Rai (2014) in the climate of stipules (c 2mm wide in base and 3 mm in length). The
Meerut District, India. Santos et al. (2004) has reported leaflets are arranged in umbrella like manner on top of the
that mechanical scarification and soaking in water for
green petiole (palmate leaf). The leaflets were free but the
around 24h overcome dormancy. According to the
basal portion was connate. This agreed with Berger
scheme of Garwood (1996), the seedling of S. foetida
appeared to be Phanerocotylar-epigeal-Reserve type or (1972). Leaflets were lanceolate in shape in mature plants
Cryptocotylar-hypogeal-Reserve type depending upon the - acute at base and apex (Table 1) and widest in the mid
seed-sowing-depth. When seeds were sown in superficial (Fig. 5). They were revolutely marginate. The leaves were
soil, cotyledons were sent aboveground by vigorous palmate with five leaflets at seedling stage. The mean
hypocotylar growth (Fig. 4A, B and C). If sown in deeper number of leaflets per leaf averaged 5.47 ± 0.29, N = 15).
layer of soil only epicotyl emerged out lodging cotyledons Berger (1972) reported 5-8 leaflets per leaf which was
underground (Fig. 4D). At 20 days of age, the hypocotyl higher in upper leaves. Palmate leaves are reported to
was meaured 4.5cm and epicotyl c 5 cm. The seedling at characterize S. foetida. Other species of Sterculia have
this age had three leaves (two large and one small) and been reported to have simple leaves (Hussin & Sani
leaf area per seedling: 9169 mm2 (Table 1). (1998). Leaflets dorsiventral, marginally entire, variable
in size and entire (Table 1) covered all over with
Cotyledons: Cotyledons of an imbibed seed were thick trichomes. All parts of leaf were trichomatous – quite
(both cotyledons combinedly around 1 cm in thickness), denser on midrib and the upper foliar surface (Fig. 6).
fleshy, heavy, pale green in colour and oval in shape.
They were c 2.7 cm in length and 1.5 cm broad in
Epidermal micromorphology
imbibed seeds. Cotyledons were unequal in size. Inner
surface was concave and outer surface surface convex.
Trichomes: All aerial parts of a seedling were
The ridge on the inner surface of smaller cotyledon fitted
trichomatous (Figs. 3-6). Trichomes heteromorphic of
with the groove of the larger cotyledon (Fig. 2). If sown
several types (Figs. 7-11). On sun exposed surface of
near soil surface, hypocotyl grows rapidly and brought
cotyledons trichomes were conical and multicellular.
cotyledons aboveground. They unfolded, expanded and
They were long and bluntly narrow at the apex, and
turned green on exposure to sun, developing dense crops
densely covering the surface (Figs. 7, 8). The basal part of
of trichomes. After some time, they twisted and got rolled
the trichome was light in colour or colourless. Trichomal
releasing nutrients to developing epicotyl (Fig. 3, 4A, B,
density on two cotyledons studied varied (Table 2)
C). In seedling bearing one leaf, the two cotyledons, the
significantly (t = 2.65, p<0.001). Such a difference in
cotyledons measured 4.3 and 3.3 cm in length.
trichomal density may be thought to arise as a result of
Hypocotyl: Hypocotyl was c 0.5 cm in diameter and 1cm in size difference or differential removal of trichomes with
length, green and trichomatous in young seedling. In deep- time due to random events. Trichomal scars on cotyledons
sown seeds, no cotyledons or hypocotyl came aboveground. appeared to be circular and their diameters at right angle
It was only epicotyl which came above soil (Fig. 4D). averaged to 28.32 ± 0.7198 and 26.86 ± 0.6788 µm. The
ratio of their magnitudes, 1.081 ± 0.0306, indicated their
Epicotyl: It grew rapidly into epicotylar stem and palmate near- perfect circular shape (Table 3). The scar of broken
shiny leaves. All parts of epicotyl were trichomatous. trichome was also circular on hypocotyl (Fig. 14).
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A B C

Fig. 1. A) Sterculia foetida Habit – image from Karachi, Pakistan. B) Five-lobed dehiscing fruit. C) A fruit lobe split to show black
seeds attached on the ventral suture.

A B C D

Fig. 2. Emergence of seedling from S. foetida seeds. A, Seed germinating from superficial soil. B, Cotyledon from imbibed seed (inner
surface view showing an area in the middle depressed in form of a groove in one cotyledon and mid area raised as a ridge in the other
cotyledon); C, Cotyledon (outer surface view – prominent in convexity) and D, Cotyledon of recently emerged seedling showing inner
yellow-green and outer brownish cotyledonary surface. Hypocotyl green.

A B C

Fig. 3. A) Enlarged view of epicotyl represented by a leaf in very early seedling stage, the hypocotyl is hairy. B) Aboveground
cotyledons undergone rolling and twisting as they are consumed. C) The inner surface of cotyledons facing sun on emergence. It
becomes green and highly trichomatous on exposure to sun. The epicotyl with a single primary leaf emerging in between the
cotyledons. Hypocotyl is green, stout and trichomatous.

A B C D

Fig. 4. Seedlings of S. foetida. A) Abovground cotyledons rolling and twistimg tightly. B) Growth of a primary palmate leaf with
several leaflets. C) Early seedling with two primary leaves. Aboveground cotyledons and epicotyl are all over trichomatous. D) Only
epicotyl arising from the soil in case of deep-sown seeds, no cotyledons or hypocotyl aboveground.
2354 D. KHAN & RUBINA ABID

A B

Fig. 5. (A) Ten-day old seedlings

arising from superficial soil. Smaller
seedling arising from smaller seed and
larger seedling from the larger
Epicotyl (heavier) seed. Note the twisted
trichomatous cotyledons and palmate
shining leaves with leaflets hanging
like an umbrella. The venation is
brachidodromous (B).

Hypocotyl Cotyledons

A B C
Palmate Leaf

Cotyledon

Fig. 6. Trichomes on leaves (A) – trichomes are present all over the leaf dorsally and ventrally, but they are denser on dorsal surface
i.e., on midrib, and on the top where the leaflets unit (connate). They are present on the margins of leaves also. Trichomes are present
on stem and petiole (B and C). The leaves are stipule-bearing when young (C).

A B

Fig. 7. Cotyledonary surface with multicellular trichomes and stomata interspersed amongst the trichomes (A). A single Cotyledonary
multicellular conical trichome (B). Epidermal cells straight in anticlinal contour. Magnification – A) 10 x 10X; B) 45 x 10 X.
PLEASE INSERT RUNNING TITLE HERE 2355

A B

Fig. 8. Multicellular trichomes and a stoma on surface of cotyledon exposed to sun - the anticlinal walls of the epidermal cells are
straight (A). Trichomes on hypocotyl (B) were frequently long, unicellular and apex-pointed. Multicellular trichomes were less-
frequent than unicellular trichomes (B). Magnification – A) 45 x 10X; B) 10 x 10X.

Fig. 9. Dense trichomes on stipules. 10 x 10X. Fig. 10. Surface of young leaf showing trichomes. 10 x 10 X.

A B C Conical pointed,
Unicellular
Trichome

Glandular
Trichome

Fig. 11. Ventral surface of leaflet showing;

*, Long conical, apically pointed trichomes arising from the midrib region cells. They are relatively shorter on lamina surface (Fig. 11 A).
Magnification: 45 x 10X, zoom 1.6X.
*, Round-ended curved (hooked) or bent type multicellular trichomes arising from lamina and midrib or secondary vein cells (Fig.11 A).
*, A few long apically club-shaped glandular spherical gland (shown by arrow) – Fig. 11A and B. Magnification B: 45 x 10 X; zoom 2.8X.
*, Dark-coloured globular (peltate), glandular trichomes on the midrib amongst the long apically-pointed trichomes (Fig. 11 C).
Magnification: 45 x10 X; zoom 2.6X).
2356 D. KHAN & RUBINA ABID

The trichomes on hypocotyl were long, frequently 8A). The adaxial epidermis of leaf was with straight to
unicellular and less frequently multicellular (Fig. 8B). curvy anticlinal walls and abaxially the epidermis wall
Abscised trichome left circular scar on hypocotyl (Fig. was sinuous and irregular in shape (Fig. 13). Hussin &
14). On stipule and young leaf, trichomes were dense, Sani (1998) have also reported abaxially wavy anticlinal
generally long and unicellular (Figs. 9, 10). Trichomes walls in S. foetida leaf. The lamina exhibited a well-
of leaflet are presented in Fig. 11. They generally arose developed vascular network studded with trichomes (Fig.
from midrib or veinlets (Fig. 18). They were variable in 18). The costal cells were elongated. Two trichomal scars
length, generally shorter on finer vessels or intercostal on vein were also seen with common elongated basal cells
islands. They may be classified as given below: having straight anticlinal walls (Fig. 13). Cuticular
striation was present on laminar as well as costal cells of
1. Long, apically pointed non-glandular unicellular the leaflets (Fig. 19).
(acicular) trichomes – predominantly abundant.
2. Long, apically curved or hooked, unicellular or Table 2. Cotyledonary trichome density per mm2.
uniseriate multicellular trichomes. Cotyledon I Cotyledon II
3. Long apically club- shaped, Bicellular, uniseriate Parameters
Trichomal density Trichomal density
glandular trichomes.
4. Dark globular (ball-like) glandular trichomes on the N 30 30
midrib. Mean 45.8686 34.074
SE 3.2078 3.08068
There were a number of trichomal scars on the leaflets
Median 49.1449 29.4869
which were circular in outline as on cotyledon and
hypocotyl. Their size in terms of diameters measured at right CV (%) 38.29 49.52
angle (Table 4) in statistically good number of observations G1 0.037 0.740
(N = 30-50) indicated that they were fairly constant in Sg1 0.427 0.427
average size (24.84 ± 1.014 to 29.96 ± 1.357 µm) in four G2 -1.121 0.032
leaflets studied. As regards to the previous publications,
trichomes (non-glandular and glandular) were reported along Sg2 0.833 0.833
or on veins of the leaf surface in Buttneria admanensis of Minimum 19.66 9.63
Family Sterculiaceae by Maity (2011). Non-glandular Maximum 78.63 78.63
trichomes were acicular, simple or multicellular in this KS-T* 0.158 (p<0.055) 0.207 (p<0.002)
species (Maity, 2011). Hussin & Sani (1998) described a Shapiro-Wilk 0.930 (p<0.050) 0.911 (p<0.016)
variety of trichomes in the genus Sterculia and two types of
trichomes in Sterculia foetida, 1) Simple cylindrical non- Symmetry AS AS
glandular multicellular trichomes and 2) Glandular Acronyms: SE, Standard error of mean; CV, coefficient of
trichomes. Our observations indicate that S. foetida is variation; G1, Skewness; Sg1, St, error of skewness; G2, kurtosis;
comparatively richer in trichomal diversity than that reported Sg2, St. error of kurtosis; KS-T*, Kolmogorov-Smirnoff Test with
in earlier studies. Table 5 presents the length of various types Lilliefors significance correction; AS, Asymmetrical
of trichomes. Amongst various trichomes, the longest were
the acicular unicellular trichomes present on the midrib Table 3. Size of trichomal scars in terms of scar diameters
(613.28 ± 22.07, 225.0 – 1025.0 µm, CV: 33.12%). on the sun-exposed (upper) surface of cotyledon.
Distribution of acicular trichome lengths (µm) on a young Statistical Trichome Scar size *
leaflet of S. foetida revealed that some 77.5% of the parameters Diameter I Diameter II Ratio
trichomes belonged to the size class, 251 -750 µm. Shorter
than this class were merely 1.3% and larger than this class N 60 60 60
were 21.20% (Fig. 12). These trichomes appeared to come Mean 28.32 26.86 1.0811
from a population which tended to be normally-distributed. SE 0.71977 0.67877 0.03061
The smallest trichomes were the dark, glandular globular CV (%) 19.64 19.58 21.93
(39.29 ± 3.26, 25-50 µm, CV: 21.95%.) and the others were
Minimum 18.72 15.60 0.58
of intermediate sizes.
Maximum 40.56 39.00 1.86
Ground epidermis: Epidermal cells in cotyledons were *, Diameters I and II measured at right angle
polygonal and straight in anticlinal contour (Fig. 7B and

Table 4. Diameters of trichomal scars at right angles (D1 and D2) on ventral surface of variously sized leaflets.
Statistical Leaflet A* Leaflet B* Leaflet C* Leaflet D*
Parameters D1 D2 D1 D2 D1 D2 D1 D2
N 40 40 50 50 30 30 40 40
Mean 29.96 29.52 29.58 26.15 27.72 24.91 24.84 25.82
SE 1.357 1.186 0.649 0.615 1.372 1.404 1.094 1.149
CV (%) 28.65 25.42 15.51 16.64 27.13 30.88 27.84 28.14
Minimum 15.60 18.72 15.60 15.60 17.72 9.36 15.60 15.60
Maximum 53.04 53.04 37.44 37.44 49.92 46.80 49.92 49.92
Leaflet sizes: *, Leaflet A = 358 mm2, Leaflet B = 842 mm2; Leaflet C = 1138 mm2; Leaflet D = 1786 mm2
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Table 5. Comparison of Length (µm) of various types of Trichomes on leaflet.

Trichome type Length statistics
Long acicular unicellular trichomes N = 80, Mean: 613.28 ± 22.07, 225.0 – 1025.0, CV: 33.12%.
Long multicellular (on midrib) N = 20, Mean: 260.63 ± 10.19, 200 – 350, CV: 17.49%
Long multicellular on veinlets in Lamina N = 25, Mean: 167.0 ± 10.7, 62.5-250, CV: 32.19%
Long apically curved / bent N = 12, Mean: 290.58 ± 10.70, 250-350, CV: 10.91%
Long Apically gland-dotted N = 10, Mean: 261.36 ± 15.12, 200-362.5, CV: 19.18%
Peltate spherical glandular trichome on midrib N = 7, Mean: 39.29 ± 3.26, 25-50, CV: 21.95 %.

Stomatal complexes: The leaf of S. foetida was found to cyclocytic, complex cyclocytic or bi- or tricyclic stomata
be hypostomatous as also reported by Pereira et al. at least in Celastraceae. They opined that if laterocytic
(2018). The stomata were round to wide elliptical in stomata deserve full recognition as a distinctive stomatal
shape. There was a variety of stomata oriented in various type depends on whether they will be found more often
directions in this species. They may briefly be described outside the Family Celastraceae. Surat un Nisa et al.
as under: (2019) have described it from Vincetoxicum arnottianum
(Apocynaceae) and the present study describes it from
1. Anomocytic: Stomata surrounded with few indistinct Sterculia foetida (Fam. Malvaceae) – Fig. 28A.
neighbouring cells (NCs) (Van Cotthem, 1970; Dilcher,
1974). Such stomata were found on hypocotyl [Fig. 14A 9. Laterocytic II: simple laterocytic – see Wilkinson
and 14 (B1), six NCs] and sun-exposed surface of (1979) – Fig. 29 B.
cotyledon (Fig. 14 B2). On cotyledon they were with 3 to
5 NCs (Fig. 16). Also present on leaflets (Figs. 21, 22 A 10. Laterocytic III. Laterocytic LI type of Surat un Nisa
& B, 27 A & B and 31) et al. (2019) i.e., two lateral subsidiary on one side and
one on the other side of guard cells. (Fig. 26A).
2. Amphiparacytic variate stoma (Mitra et al., 2015)
was found on hypocotyl (Fig. 14 B5) and Fig. 15). 11. Brachyparacytic subtype I: Stomata are with two
lateral SCs one on each side of the guard cells enclosing
3. Paracytic: Two lateral subsidiary cells (SCs) the completely only at one pole, other pole is with an
completely flanking stoma (Figs. 20, 21, 24, 28B) on additional SC (Mitra et al., 2015) - Fig. 25.
leaflet – Metcalfe and Chalk (1950); Von Cotthem
(1970); Dilcher (1974) and Wilkinson (1979). Carpenter 12. Staurocytic: Four SCs more or less equal in size, with
(2005) referred to it as holoparacytic. the anticlinal walls of the SCs extending at right angles
from the poles and the middle of the guards cells (Dilcher,
4. Actinocytic: Stomata with five or more radiating 1974) - Fig. 29A.
subsidiary cells (Van Cotthem, 1970; Wilkinson, 1979
(Fig. 20). 13. Anisocytic: Stomata with three SCs unequal in size -
two larger and one smaller surrounding the guard cells
5. Tetracytic: Four cells surrounding guard cells in an (Metcalf and Chalk, 1950; Dilcher, 1974) – Figs. 27B,
irregular and variable manner (Dilcher, 1974) – Fig. 21, 28B, 30).
28B.
14. Hemiparacytic: One lateral SC flanking the guard
6. Stephanocytic: In typical form SCs are arranged cells on one side and on the other side there may be
radially around the guard cells. The cells are of different unspecialized cell (Dilcher, 1974; Surat un Nisa et al.,
shapes and sizes - such stomata are with five subsidiary 2019; Tomlinson, 1969; Fryns-Claessens & Van Cotthem,
cells, with two small placed on one side, and one on the 1973) (Figs. 26B, 27A & 30).
other side of the guard cells. One subsidiary cell is present
at each pole (Surat un Nisa et al. (2019) - (Fig. 21, 28B, 15. Brachyparahexacytic monopolar variant: Stomata
29 D). with five SCs almost resembling Brachyparahexacytic
monopolar subtype I of Mitra et al. (2015) (Fig. 26A).
7. Bicyclic Stephanocytic: Stomata surrounded by two
cycles of cells with inner specialized and outer weakly 16. Contiguous stomata: Such stomata were present on
specialized SCs forming more or less defined rosette cotyledons (Fig. 17A & B) and leaflets (Fig. 32). They
(Carpenter, 2005) (Fig. 24B). were of two types – oriented at right angle and juxtaposed
type. A unique pair of contiguous stomata was observed
8. Laterocytic I: Two lateral subsidiary cells are on one on a leaflet situated on top of a flat-topped chimney-like
side and three on the other side of guard cells (sub type structure formed of single tiers of epidermal cells (Fig.
L3 of Surat un Nisa et al. [2019]). It was originally 32). Contiguity of three stomata was evident in Fig. 20.
described by Den Hartog née Vanter Tholan & Baas
(1978) for Celastraceae. They suggested it to arise from 17. Giant stomata: Giant stomata were frequently-
anisocytic type and to be developmentally related to such occurring in S. foetida. These stomata were generally
complex stomatal types as complex laterocytic, stephanocytic, mono-or polycyclic nature. These stomata
2358 D. KHAN & RUBINA ABID

averaged to 26.42 ± 0.416 µm in length (N=45, 23.40 - two varieties of Pterygota alata reported that giant stomata
40.56 µm, CV: 10.56%) and 18.11 ± 0.479 um (N = 45, were exclusively of amphicyclocytic nature. In S. foetida,
9.56 -28.06 µm, CV: 17.79%) in width. These stomata however, the giant stomata were of stephanocytic or
showed characteristic ornamentation and cuticular striation actinocytic or anomocytic types. Rarely, a giant
on subsidiaries. The presence of giant stomata is not anomocytic stoma was found to have neighbouring cells
uncommon in angiosperms and has been reported from (NCs) arranged in staurocytic order (two conjoint walls of
several unrelated families. Boldt & Rank (2010) reported NCs joining at the poles and two with meeting the poral
giant stomata (those of > 25 µm in length) in thirty families epidermal wall on lateral sides (Fig. 31).
of dicotyledonous outdoor plants of varied life forms of
Germany including Family Malvaceae (Hibiscus rosa- 18. Persistent Stomatal initials: They were frequently seen in
sinensis). Aesculus hippcastanum (Family Sapindaceae) groups on leaflets of S. foetida seedlings (Figs. 20, 21, 23 and
had largest giant stomata (> 40 µm in length). All giant 30). Mitra et al. (2015) have also reported persistent stomatal
stomata in their study also invariably showed striation on initials in leaves of two varieties of Pterygota alata, a member
of Family Malvaceae from India.
subsidiary cells (SCs). Mitra et al. (2015) in their studies of

Acicular trichomes
N = 80
Mean = 613.28 µm
SE = 22.700
Median = 612.50
CV % = 33.12
G1 = -0.099
Sg1 = 0.269
G2 = -0.712
Sg2 = 0.532
Minimum = 225.0
Maximum = 1025.0
KST = 0.087
p<0.200
Shapiro-Wilk = 0.975
p<0.116

Fig. 12. Distribution of acicular trichome lengths (µm) on a young leaflet Fig. 13. Scars of two trichomes surrounded with
of S. foetida. Some 77.5% of the trichomes belonged to the size class, 251 - radially elongated basal cells with straight anticlinal
750 µm. Shorter than this class were merely 1.3% and larger than this class walls. Note the common basal cells between them.
were 21.20%. Magnification: 45 x 10 X.

A B

Trichome
Scar

Fig. 14. A) Surface of hypocotyl showing two stomata surrounded with 5-6 NCs (enclosed in a circle) and a circular scar of the broken
trichome. Note the straightness of the epidermal anticlinal cell walls and trichome base surrounded by six unequal cells Magnification:
45 x 10 X, zoom 1.2 X. B) Stoma on hypocotyl - anomocytic (B1), Stoma on cotyledon with 3 NCs (B2), a multicellular conical
trichome, common on hypocotyl and cotyledon (B3), A scar of a trichome (B4) and an Amphiparacytic variate stoma (see Mitra et al.
(2015) on hypocotyl. (Fig. 14 (B5). Stomata not drawn to scale.
PLEASE INSERT RUNNING TITLE HERE 2359

Table 6. Cotyledonary stomatal density per mm2 on sun-

exposed cotyledonary surface.
Cotyledon I Cotyledon II
Parameters
Stomatal density Stomatal density
N 30 30
Mean 28.504 15.39898
SE 3.2428 2.2934
Median 29.4869 14.7435
CV (%) 62.32 81.58
G1 0.234 0.691
Sg1 0.427 0.427
G2 -0.440 0.387
Sg2 0.833 0.833
Minimum zero Zero
Maximum 68.80 49.14
KS-T* 0.124 (p<0.2000) 0.171, p<0.025
Shapiro-Wilk 0.961 (p<0.329) 0.903, p<0.010
Symmetry AS AS
Acronyms: SE, Standard error of mean; CV, Coefficient of
variation; G1, Skewness; Sg1, St, Error of skewness; G2, Kurtosis;
Fig. 15. Amphiparacytic variate stoma (see Mitra et al., 2015) Sg2, St. Error of kurtosis; KS-T*, Kolmogorov-Smirnoff Test with
on hypocotyl. Magnification: 45 x 10 X, zoom 1.4 X. Lilliefors significance correction; AS, Asymmetrical

A B C

Fig. 16. Stomata on sun-exposed surface of cotyledon – Stoma surrounded with 3 NCs (A) and anomocytic stomata with 4- and 5-
neighbouring cells (B and C, respectively). Epidermal cells are straight in anticlinal contour. Magnification: 45 x 10 X, zoom 1.4 X).

A B

Fig. 18. Surface view of dorsal side of leaflet showing trichomes

of different sizes distributed on the veins and the laminar islands.
Fig. 17. Cotyledonary surface showing Contiguous stomata (at- Note the well-developed vascular network. Several trichome have
right-angle type (A) and near juxtaposed type (B)’ Cotyledonary broken leaving behind the scar on the surface. There are no
stomata. Magnification 45 x 10 X, zoom 1. 6 X. stomata on dorsal surface. Magnification: 10 x 10 X.
2360 D. KHAN & RUBINA ABID

A B

Fig. 19. Dorsal Epidermis cuticular striation of leaflet - Striae are in form of bands running parallel to each other on the periclinal surface
of cells and frequently continuing on adjacent cell (s). In the middle of each image is scar of a trichome surrounded with several basement
cells. There are no stomata on dorsal side. Magnification: 45 x 10 X, zoom 1.2 X. A) Lamina surface; B) veinlet surface

Fig. 20. General view ventral surface of larger leaflet showing vascular region with a scar of a broken trichome (white circle), stomata
of two types - brachyparacytic (stoma incompletely surrounded by two subsidiary cells (Red triangle) and actinocytic stoma
surrounded by 7-8 cells (Blue squares), and cuticular striation in form of parallel bands on subsidiaries and the costal cells. Paracytic
stoma is shown within a green circle. The epidermal anticlinal contour is curvy to sinuous. Two persistent stomatal initials in yellow
circle. A cluster of three stomata with no subsidiaries among them (within red circle). Some persistent stomatal initials are also visible
(Blue circle). Magnification: 45 x 10 X, zoom 1.4X, enlarged).
PLEASE INSERT RUNNING TITLE HERE 2361

Fig. 21. Ventral surface of leaflet showing

paracytic (white square), tetracytic (red
circles) and anomocytic stoma (yellow
circle). Magnification: 45 x 10, zoom
1.4X). Stephanocytic stoma (five
subsidiaries of different shape and size) in
blue circle – such stomata are with five
subsidiary cells, with two small placed on
one side, and one on the other side of the
guard cells. One subsidiary cell is present
at each pole. Anisocytic in green circle.
Magnification: 45 x 10 X.

A B

Fig. 22. Anomocytic stoma. (A) Surrounded by five elongated cells on the vein of a more or less mature leaflet. Note that the cuticular striation
in form of parallel bands. Mag. 45 x 10X, zoom 1.5X. (B) Another anomocytic stoma in vascular region where epidermal cells are transversely
elongated with striations. The cells of laminar islands are irregular in shape and typically curvy to sinuous. Magnification: 45 x 10X.

Fig. 23. Persistent stomatal initials in groups. Magnification: 45 x 10 X, zoom 2.0 X).
2362 D. KHAN & RUBINA ABID

A B

Fig. 24. Paracytic stomata (A) - note the persistent stomatal initials in lower most region of the image. Bicyclic stephanocytic stoma
(B). Magnification: 45 x 10 X, zoom 2.0).

Table 7. Length and width (µm) of stomata on sun- Stomata in the family Malvaceae (former Sterculiaceae)
exposed (upper) surface of cotyledon. were reported to be anomocytic Metcalf & Chalk, 1950).
Stomatal size Hussin & Sani (1998) reported anomocytic stomata in S.
Statistical parameters foetida. However, anisocytic, paracytic, cyclocytic
Length Width Brachyparacytic, amphibrachyparacytic were also found by
N 60 60 Maity (2011). Six stomatal types, anisocytic, anomocytic,
Mean 20.57 18.60 diacytic, amphipericytic, paracytic and abnormal types were
SE 0.6467 0.5859 reported in five malvaceous species by Udofia et al. (2020).
Gangadhara et al. (1977) reported anomocytic, paracytic,
CV (%) 24.36 24.40 diacytic, hemidiacytic, single-subsidiary stomatal type and
Minimum 9.36 8.58 some aberrant types in Gossypium herbaceum cotyledon and
Maximum 34.32 31.20 hypocotyl. Essiett & Iwok (2014) reported laterocytic,
brachyparacytic, anisocytic, anomocytic and staurocytic
stomata in Hibiscus species. Mitra et al. (2015) reported
stomatal polymorphism from two varieties of Pterygota
alata viz. Pterygota alata (Roxb.) R.Br. var. alata and P.
alata (Roxb.) R.Br. var. irregularis (W.W. Sm.) Deb and
S.K. Basu (Family Malvaceae) - amphibrachyparacytic (two
subtypes), amphicyclocytic (three subtypes), anisocytic,
anomocytic, anomotetracytic (one subtype), Brachyparacytic
(two subtypes), Brachyparahexacytic (monopolar three
subtypes), dipolar (4 subtypes and three intermediate type),
Brachyparatetracytic, Cyclocytic (with one subtype),
Paracytic, Parahexacytic dipolar, Paratetracytic,
Stephanocytic and Giant stomata. Thus, there appears a great
diversity of stomatal types in Family Malvaceae.
The presence of stomatal polymorphism (10 types of
normal stomata along with 4 subtypes and one intermediate
type between stephanocytic and Hemiparacytic and some
abnormal stomatal structures both in the vegetative and floral
Fig. 25. A stoma - Brachyparacytic subtype I of Mitra et al. organs of Canella winterena (L.) Geartn. (Family
(2015). Enlarged from an image photographed at 45 x 10X. Canellaceae) have been reported by Mandal et al. (2014).
The epidermal cells were polygonal, isodiametric in surface
Stomatal clustering: Stomata were observed to cluster in view with straight anticlinal walls. The stomatal complexes
the form of an arch on one side of a giant stoma (Fig. included amphibrachyparacytic, anomocytic, anisocytic,
28C) or clustered in groups, separated by a narrow strip of brachyparacytic, brachyparatetracytic, cyclocytic,
epidermal ground cells (Fig. 30). hemiparacytic, laterocytic, holoparacytic, stephanocytic, one
PLEASE INSERT RUNNING TITLE HERE 2363

intermediate type between stephanocytic and hemiparacytic, is distributed asymmetrically in both cotyledons. The
etc. Abnormalities like contiguous stomata, different types of average size of the stomata tended to be 20.57 ± 0.65 x
twin stomata and cytoplasmic bridge between adjacent 18.60 ± 0.59 µm (L x W) (Table 7).
stomata, stomata with single guard cell, pore juxtaposed with
normal stomata are also found. Recently, Surat un Nisa et al. Foliar stomata – Density and size: Foliar stomatal
(2019) have reported stomatal polymorphism in density (SD) was studied in ten leaflets of different sizes
Vincetoxicum arnottianum (Fam. Apocynaceae) – with 40-50 observations for each leaflet (Table 8). The
demonstrating 10 major stomatal types and 36 stomatal number of stomata per mm2 was found to be the function
subtypes. Comparing our results with earlier reported studies of leaflet size. The density was higher in smaller young
of Mitra et al. (2015) and Surat un Nisa et al. (2019), it is leaflets which tended to decline with little irregularity
obvious that S. foetida is rich in stomatal diversity but not as with increase in leaflet size. Stomatal density in the
rich as Pterygota alata (Fam. Malvaceae) and Vincetoxicum smallest leaflet of 184 mm2 was 249.14 ± 5.54 (varying
arnottianum (Fam. Apocynaceae). Since we dealt with from 157.26 to 324.36 stomata per mm 2, CV: 14.05%)
seedlings, stomatal diversity needs to be revisited in mature and 125.22 ± 3.449 stomata per mm2 in the largest leaflet
plants for better elucidation. Surface immaturity often (4709 mm2). Our estimation of stomatal density in S.
imposes difficulty in stomatal identification. foetida was much higher than that reported by Pereira et
It may be mentioned that since stomatal al. (2018) to be 22.25 ± 0.89 stomata per mm 2 under full-
polymorphism is reported from unrelated families, it is light condition and 20.5 ± 0.82 under half-light condition.
currently believed that the presence of more than one type It is known from Salisbury (1928) that stomatal density is
of stomata in a species is probably a reflection of related to leaf size inversely. Stomatal density on young
precarious balance among the influences of the and small terminal leaflets of C. fistula was reported to be
environment that operate at a level of meristemoids (that quite higher than that on relatively larger leaflets (Khan &
form the stomatal mother cells) on one hand and the Zaki, 2019). Khan & Zaki (2020) also reported leaf-size
influences operating at the organ level in deciding the related inverse association of SD in Helianthus annuus
orientation of the cell division at species level on the other Var. US 666. The decrease in SD in larger leaves, as
hand (Humbert & Guyot, 1969; Mandal et al., 2014) and compared to the smaller ones, may be attributed to the
likely phylogenetic pattern on the basis of polymorphic foliar epidermal cells’ expansion. Young leaves have
stomata cannot be drawn (see Mitra et al., 52015). large number of stomata but as the leaf expands the
density declines (Gay & Hurd, 1975).
Cotyledonary stomata – density and size: Stomatal Foliar stomatal size of normal plus giant stomata in
density on sun-exposed cotyledonary surface varied with four leaflets studied (N = 265 observations} averaged to
the two cotyledons studied (Table 6). It averaged 28.50 ± 21.15 ± 14.86 µm (L x W). The length and width of the
2.24 (varying from zero to 68.8) stomata per mm 2 on one stomata remained more or less unchanged amongst the
cotyledon and averaged to 15.40 ± 2.29 (varying from pooled as well individual leaflets and the coefficient of
zero to 49.14) stomata per mm2 on the other cotyledon. It variability (CV) in any leaflet was < 20% (Table 9).

Table 8. Stomatal density per mm2 on ventral surface of variously-sized leaflets of a 2-month-old sapling of S. foetida.
Leaflet # Area mm2 N Mean SE Median CV (%) Skewness Kurtosis Min. Max.
I 184 50 249.14 5.5390 255.553 14.05 -0.468 0.147 157.26 324.36
II 237 50 249.46 4.8307 255.553 13.69 -0.510 -0.235 167.09 304.70
II 358 50 252.60 5.0334 245.724 14.09 0.779 0.180 196.58 344.01
IV 842 40 200.60 3.7536 195.090 13.23 -0.289 -0.262 130.56 250.52
V 936 50 214.66 4.4612 216.238 14.70 -0.474 -0.662 137.61 275.21
VI 1102 40 125.22 3.4487 117.950 19.48 0.043 -0.797 78.63 176.92
VII 1390 40 215.45 3.6274 216.238 11.90 0.802 1.067 167.09 294.89
VIII 1786 50 112.44 3.1043 108.12 19.52 -0.032 -0.189 68.80 167.09
IX 2017 50 185.28 4.5282 191.665 15.46 0.891 1.062 98.29 235.90
X 4709 50 125.22 3.4487 117.917 19.48 0.043 -0.797 78.63 176.92
N = Number of microscopic fields of vision observed; SE = St. Error of means; CV = Coefficient of variability (%); St. Error of
skewness (0.337 for N = 50, 0.374 for N= 40); St. Error of kurtosis (0.662 for N = 50, 0.733 for N = 40); CV, Coefficient of
variability (%); Min. = Minimum; Max. = Maximum

Table 9. Length and width (µm) of stomata on ventral surface of variously sized leaflets (normal + giant stomata both).
Leaflet A* Leaflet B Leaflet C Leaflet D Pooled
Statistical parameters
Length Width Length Width Length Width Length Width Length Width
N 60 60 70 70 75 75 60 60 265 265
Mean 24.34 14.90 19.88 15.49 21.11 14.37 19.08 14.73 21.15 14.86
SE 0.4933 0.3445 0.4429 0.3596 0.3355 0.3318 0.3621 0.3657 0.2334 0.1766
CV (%) 15.70 17.85 18.65 19.42 13.76 19.99 10.90 19.23 17.97 19.35
Minimum 15.60 9.36 9.66 9.36 15.60 9.36 15.60 11.70 9.36 9.36
Maximum 40.56 23.40 28.08 28.08 28.08 24.96 24.96 23.40 40.56 28.08
*, Leaflet size: A = 358 mm2, Leaflet B = 842 mm2; Leaflet C = 1138 mm2 and Leaflet D = 1786 mm2
2364 D. KHAN & RUBINA ABID

A B

Fig. 26. A) Vascular nerve bearing scars of the trichomes and striations parallel to the costal cell’s periclinal surface and a laterocytic type stoma
(yellow circle) – see Laterocytic LI of Surat un Nisa et al. (2019) i.e., two lateral subsidiary on one side and one on the other side of guard cells.
Waviness of epidermis cells is apparent. Blue circle indicates Brachyparahexacytic monopolar variant stoma (see Mitra et al., 2015). B)
Hemiparacytic stoma. Magnification: A, 45 x 10 X and B, Image photographed at 45 x 10 X was enlarged by cropping to show the stoma.

A B

Fig. 27. A) Typical paracytic and anomocytic stomata (yellow circles) in close vicinity with a hemiparacytic stoma on ventral surface
of leaflet (Red circle). B) A brachyparacytic stoma in close association of an anomocytic stoma (Yellow circle), anisocytic stoma (red
circle) and a giant stoma connected with a basal cell of a trichome via an elongated curved subsidiary cell (blue circle).
Magnification: A, 45 x 10 X, zoom 1.6X; B, 45 x 10 X, zoom 1.2X.

A B C D

Fig. 28. Ventral surface of leaflet. A) Giant laterocytic stoma L3 (Originally described by den Hartog née Vanter Tholan & Baas
(1978) for Celastraceae and Surat un Nisa et al. (2019) – Fig. 28A). B) Various types of stomata – paracytic (arrow), anisocytic (red
circle), tetracytic (black circle) and Stephanocytic (Yellow circle). C) Cluster of four stomata arranged on one side of a giant
amphicyclocytic stoma in form of an arch with prominent striations. Bicyclic stephanocytic stoma on costal region with numerous
subsidiary cells, two of them elongated and far-extending (D) SCs connecting with costal cells on either sides. Magnification: A, 45 x
10X, zoom 1.4 x; B, 45 x 10 x, zoom 1.2X; C, 45 x 10X, zoom 1.5X and D, 45 x 10x, zoom 1.4X.
PLEASE INSERT RUNNING TITLE HERE 2365

A B

C D

Fig. 29. Ventral surface of leaflet. A) Staurocytic (single arrow) and hemiparacytic (double arrow). B) Simple Laterocytic stoma. C)
Hemiparacytic and D) Stephanocytic stoma (five subsidiaries of different shape and size) – such stomata are with five subsidiary cells,
with two small placed on one side, and one on the other side of the guard cells. One subsidiary cell is present at each pole.
Magnification: A, 45 x 10X, zoom 1.2 X; B, 45 x 10, zoom 2.0 X; C, 45 x 10x, zoom 1.6X and D, 45 x 10X, zoom 1.4 X.

* *

* *

Fig. 31. A stomatal complex in association with four persistent

arrested initials in vicinity of a large anomocytic stoma. The two
Fig. 30. Ventral surface of young leaflet of S. foetida. Stomatal conjoint walls of the indistinct neighbouring cells may be seen
clusters of five and seven stomata separated by a narrow strip of joining at the poles of the stoma and the other two conjoint
epidermal cells wavy in anticlinal contour. A few persistent radial tangential walls of the neighbouring cells meeting the
stomatal initials are also present in vicinity of stomata (shown poral epidermal wall on lateral side. The large guard cells
inside red circles). Anisocytic stoma in white circle and overlying and partly obscuring neighbouring cells. Image at
hemiparacytic in yellow. Magnification: 45 x 10 X, zoom 1.4 X. magnification 45 x 10 X, zoom 1.6 X.
2366 D. KHAN & RUBINA ABID

A B C

D E F

Fig, 32. Contiguous stomata on the ventral surface of leaf. Juxtaposed type (B, C, D and F,) and more or less at-right- angle type (A
and E). Note highly striated feather-like subsidiary cells. The contiguous stomata (F) are unique being raised above the ground
epidermal cells in form of a flat-topped chimney containing stomata on the top. Magnification: 45 x 10X, zoom 1.4X.

Conclusion Carpenter, K.J. 2005. Stomatal architecture and evolution in

basal angiosperms. Am. J. Bot., 92(10): 1595-1615.
It may be concluded from the results of the present Chanyawiwatkul, J., C.S. Upaparnich and S. Takeungwongtrakul.
2018. Physico-chemical properties and oxidative stability of
study that S. foetida (Family Malvaceae) is quite rich in
oil from Samrong (Sterculia foetida) seed. Int. J. Agricultural
trichomal and stomatal diversity. Tech., 14(7): 1097-1106.
Den Hartog née Vanter Tholan and P. Baas. 1978. Epidermal
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(Received for publication 17 August 2022)