TAXONOMIC REVISION OF THE SUBFAMILY STERCULIOIDEAE BEILSCHM. IN BANGLADESH

The subfamily Sterculioideae Beilschm. of Malvaceae has been revised for Bangladesh which revealed 16 taxa belonging to five genera, such as Firmiana Marsili, Heritiera Ait. , Pterygota Schott & Endl. , Scaphium Schott & Endl. and Sterculia L. The genus Sterculia is unveiled with the highest number of taxa, whereas both Pterygota and Scaphium are represented with single taxon. Dichotomous bracketed keys to genera and species are constructed for easy identification. Each taxon is presented with an updated nomenclature, description of the taxa along with illustrations, specimens examined, phenology, notes on distribution and economical importance. In most cases, chromosome number has been provided.


Introduction
Understanding on the diversity and inter-relationships of plant life is based primarily upon the comparative data of revisionary studies (Stuessy, 1975). The process of undertaking a taxonomic revision is central to taxonomy. A revision involves restudy of a group to correct or improve its diagnosis, description or phylogeny. Taxonomic revision helps to update the system of classification as taxa are often subjected to phenotypic plasticity (Baur et al., 2014). Sterculioideae Beilschm. is one of the nine subfamilies of Malvaceae representing 13 genera and around 430 species worldwide APG IV, 2016). These 13 genera have been distributed in four major clades (APG IV, 2016), such as (a) Cola clade incorporating Cola Schott & Endl., puberulent, lobes ovate-triangular, ca. 4 mm, apex acute. Petals absent. Androgynophore present, 5-10 mm long, exserted, filamentous short, anthers 10, locules curved. Ovary superior, 5-locular, flask-shaped, glabrous; styles 5, free, short; stigma curved outward. Fruit a follicle, 8-11 x 3-5 cm, oblong with acute apex, follicle stalked, red or purple when mature, foliaceous, tongue-shaped, with apparent venation. Seeds 2, yellow, wrinkled or smooth, globose or ovoid, ca. 1 cm long, ca. 6 mm in diameter.
Economic aspects: Fresh young seeds with an almond flavor are edible. In the Chittagong district of Bangladesh, the bark generates cordage that is used to tie animals and goats. The Chittagong Hill Tracts tribal people use the bark to manufacture bamboo busket straps called "Turung" which they wear on their foreheads. Ethnic people use this plant as a remedy to cholera for its promising anti-diarrheal activities. Besides that, some other diseases and disorders like hysteria, jaundice, urine infection, stomach ache, seminal emission, and spermaturia can be treated using this plant (Ashrafuzzaman and Sarwar, 2021).
Flowering and fruiting: October-February. Chromosome number: 2n = 40 (Raghavan and Arora, 1958). Ecology: The species usually occurs in mixed deciduous forests. Representative specimens: No specimen was available in any herbarium of Bangladesh. Global distribution: Bangladesh, China, Cambodia, India, Japan, Sri Lanka, Taiwan, Thailand, United States of America and Viet Nam. Economic aspects: The species has been widely employed in the pharmaceutical, health-care, food, cosmetics, waste management, paper-textile, composite fiber, and leather sectors. Because the gum exudate, this tree has a high market value, it is popularly referred to as the 'Karaya Gum' tree. Because of its natural availability, economic effectiveness, non-hazardous nature, quick recovery, and physicochemical qualities, karaya gum polymers are an excellent alternative to synthetic ones. Furthermore, tribal communities use the tree for its indigenous cures for oligospermia, leucorrhoea, constipation, body swelling, throat infection, wound healing, and other diseases. Also, the presence of diverse bioactive compounds has made this plant an excellent source to conduct research on Computer Aided Drug Designing (CADD) (Dhiman et al., 2019 Trees, usually with buttress. Leaves alternate, simple or palmately compound, abaxially usually scaly. Inflorescence cymose, paniculate, axillary, many-flowered, hairy or scaly. Flowers unisexual. Calyx campanulate or urceolate, 4-6-lobed. Petals absent. Male flowers with short androgynophore. Anthers 4-15, in 1 or 2 rings at apex of androgynophore, with pistillode. Female flowers with ovary with 3-5 coherent carpels, base with sterile anthers; ovules 1 per carpel. Style very short; stigma very small. Fruit woody or leathery, with keel-like prominence or wing, indehiscent. Seeds without endosperm.  . 2).

Key to species of
Vernacular names: Sundari, Sunder. English name: Sundri. A medium-sized evergreen tree, 15-18 m tall, branchlets lepidote, bark grey. Leaves simple, alternate, 10-17 x 3-6 cm, elliptic-lanceolate, tapering to rounded at the base, acute or rounded and mucronate at the apex, glabrous above, adpressed scaly beneath, petioles up to 2 cm long. Flowers small, unisexual, in axillary panicles. Sepals 5 or rarely 4-6 toothed, stellate-hairy inside. Petals absent. Male flowers with 5-10 stamens, united in a column with a ring of 2-celled anthers at the apex. Female flowers with 4-6 carpels, almost free, styles short, stigmas 5 thick, ovule solitary in each carpel. Fruit a cluster of woody, indehiscent, keeled or winged ripe carpel. Fruit a cluster of woody, indehiscent, keeled or winged ripe carpel. Seed solitary without vivipary but can float on the tidal water. Flowering and fruiting: September-December. Chromosome number: 2n = 38 (Das et al., 1995). Ecology: Moderately saline zone, well-drained soil inundated by tidal water of low salinity. Although it is a mangrove species, it can tolerate the conditions of higher altitudes (Ahmed et al., 2009). Global distribution: Bangladesh, India, Myanmar and Thailand. Economic aspects: The plant is used by traditional health practitioners to treat diabetes, hepatic disorders, gastrointestinal disorders, goiter, and skin diseases. It has potent antioxidant, antinociceptive, antihyperglycemic, antibacterial, and anticancer properties. Important chemical ingredients such as saponins, alkaloids, glycosides, tannins, steroids, flavonoids, gums, phytosterols, and reducing sugars have been discovered through phytochemical investigations. Twigs are used in the treatment of oral infections and toothache. Hot decoction of bark is used to get relief from goiter and diabetes. Decoction of leaves and seeds have efficacy to treat various gastrointestinal disorders (Mahmud et al., 2014). Evergreen trees, up to 10-15 m tall; bark grayish-brown, sometimes pinkish-grey, vertically and superficially fissured, rough or smooth, inner bark brown-pink. Sapwood pale yellow. Young branchlets white scurfy scaly, mature branchlets lepidote. Stipules lanceolate, caducous; petiole 1-2 cm; leaf blade simple, alternate, oblong-lanceolate, elliptic, or ovate, 10-20 x 5-10 cm, leathery, abaxially densely silver-white scurfy scaly, adaxially glabrous or nearly so, base obtuse, apex acute or obtuse. Inflorescence paniculate, axillary, ca. 8 cm, densely stellate hairy or with scales. Flowers pale green to pinkish red. Calyx red-brown, campanulate, 4-6 mm, both surfaces stellate hairy, lobes triangular, ca. 2 mm. Male flowers with thin disc, papillate. Androgynophore short and glabrous. Anthers 4 or 5, in 1 ring. Female flowers with carpels 4 or 5; stigmas as many as carpels, short and curved downward. Fruit nutlike, woody, drying yellow-brown, nearly ellipsoid, ca. 6 x 3.5 cm, keeled on back, glabrous. Seeds ovoid, ca. 2 cm.
Economic aspects: The timber is used as a good source of fuel for its high heat-yielding efficiency. Wood is suitable for the production of wrapping, writing and printing papers. Tannins are present in the bark which can be used for toughening fishing nets. Seed extract is used as medicine in the treatment of dysentery and diarrhea (Ahmed et al., 2009;Mitra et al., 2021). The crude methanol extract of leaves possesses free radical scavenging, anti-hemolytic, cytotoxic and anti-bacterial activities (Karim et al., 2020). ( Fig. 4). Vernacular name: Not known. English name: Large leaf looking glass tree. A medium-sized evergreen tree, with umbrella shaped crown, arborescent, up to 30 m in height. Leaves simple, petiolate, petioles cylindrical, pubescent, rusty brown when mature; lamina ovate-oblong or elliptic-oblong, apex acute, base obtuse to slightly cordate sometimes, margin entire mostly, sometimes undulate in dry condition, veined with pinnate parallel venation, veins prominent adaxially, texture subcoriaceous, adaxial surface sometimes rusty brown while abaxial surface silvery. Flowers are unisexual, 3-4 mm across, white-yellowish to pinkish-rose in colour, present in foot-long panicle like cymes, in leaf axils. Male flowers with 6-8 stamens; anthers irregularly clumped on androgynophore. Female flowers with 1 carpel. Fruit a samara, ellipsoid, with one apical fish-tail wing. Flowering and fruiting: November-February. Chromosome number: 2n = 38 (Das et al., 1995). Ecology: Inland zone of mangrove swamps. Representative specimens: Khulna: s. loc, 13 Sep 1949, P. Maheshwari s.n. (DUSH). Global distribution: Bangladesh, Cambodia, China, India, Lao PDR, Myanmar, Thailand and Viet Nam.
Economic aspects: Mainly valued for its timber. The wood is hard with distinct annual rings and uniform medullary rays, joined by fine transverse lines. It takes a fine polish. It is used for posts and poles (Duncan, 2005). A small to medium-sized tree, 10-15 m in height, sometimes up to 30 m tall, arborescent. Young branches stellate-tomentose. Leaves simple, alternate, unifoliolate, 4-16 x 3-17 cm, lanceolate, oblanceolate or oblong to elliptic, base obtuse, obscurely acuminate at the apex, entire, texture coriaceous, petioles ca. 2 mm long, scaly. Flowers in axillary panicles, densely covered with stellate tomentose scales. Sepals 5, calyx campanulate. Petals absent. Male flowers with slender staminal column, anther thecae in a regular ring on an androgynophore. Female flowers with 5-6 sessile ovary, stellate scaly, sterile anther thecae present at the base of the ovary. Fruit a samara, 5-7 cm long, glabrous, 1-seeded.

Heritiera papilio
Flowering and fruiting: April-December. Ecology: Usually occurs in the hilly forests (Alam, 2018). Representative specimen: No specimen was available in any herbarium of Bangladesh. Global distribution: Bangladesh, India and Myanmar. Economic aspects: Timber is hard which takes a fine polish and is used for temporary construction works for the manufacturing of poles, posts as well as agricultural implements (Ahmed et al., 2009 Trees. Leaves cordate, usually entire, but lobed when very young. Inflorescence axillary, racemose or paniculate. Flowers unisexual. Calyx campanulate, 5-lobed to base, lobes reflexed at apex. Petals absent. Male flowers with cylindrical androgynophore, enclosed by calyx. Filaments clustered into 5 groups, staminodes usually present; anthers sessile. Female flowers with very short androgynophore and 5 undeveloped staminodes. Carpels almost free; ovules many per phytochemicals can be used to design potential drugs for biogerontological research. Seeds are medicinally significant, edible and are often eaten after roasting. Seeds possess narcotic properties and often used as a substitute for opium (Agarwal and Jain, 2017). Crude ethanol extract of leaves is reported to have excellent in-vivo and in-vitro antioxidant effects . The leaf extracts contain active compounds showing in-vitro antibacterial activity against multidrug resistant and biofilm forming strains of Staphylococcus spp. (Panda et al., 2020).   (Fig. 6). Vernacular names: Shaogan, Shampan, Pogan, Sugan, Shagan. English name: Water Malva Nut. A deciduous tree, up to 35 m tall. Buttresses often present, 1-2 m tall. Inner bark reddish, fibrous, 10-15 mm thick. Outer bark grey-green to brown, cracked to flaking. Sapwood white. Terminal branches pale brown to brown, striate to smooth, lenticels absent, glabrous. Petiole pale brown, 2-12 cm long, 2-4 mm wide, smooth to striate, glabrous or occasionally stellate hairy, both ends darker. Stipules caducous or persistent only at apex of stalk, rounded to triangular, 2-4 mm long, glabrous or with very minute simple hairs on both surfaces. Leaf lamina sub-leathery to leathery, occasionally papery, ovate, elliptic or elliptic-oblong, symmetric to asymmetric, base rounded to acute (occasionally truncate or slightly cordate), apex acute, 1.3-2.3 times as long as wide, 8-34 cm long, 6-17 cm at widest point, upper surface glabrous, occasionally with gland dots, drying pale brown-tan, shiny, lower surface glabrous, occasionally with gland dots, drying pale brown-tan, dull; midrib raised on both surfaces; basal veins 1-2 pairs. Tertiary veins flat on both surfaces, slightly paler than lamina below, inconspicuous above. Inflorescences 5-12 cm long, densely stellate hairy. Bracts caducous. Flower buds drying brown, ovoid, slightly elongated towards apex, sparsely to densely stellate hairy, lobe margin densely stellate hairy, more or less distinct. Pedicel absent to 2 mm long, 0.5-1 mm wide, densely stellate hairy. Flowers 5-8 mm long, yellow with purple base, when fresh, drying brown, 5-lobed, lobes 2/3 the length of the calyx, calyx outer surface sparsely stellate hairy, inner surface glabrous (including base), androgynophore 5-8 mm long, protruding, recurved at apex, sparsely simple hairy, sometimes with stellate hairs with long branches on upper half, glabrous on lower half, anthers ca. 10-12, glabrous or sparsely simple hairy, carpels rudimentary and sparsely hairy in male flower, fully developed and densely stellate hairy in female flower, 3-5, free or nearly so; style absent to 0.2 mm long in male flower, 1-1.5 mm long in female flower; stigmas glabrous, as many as carpels, superficially fused. Fruit with 2-5 follicles per flower, follicles papery, 9-26 cm long, inner surface sparsely stellate hairy, shiny, outer surface sparsely to densely stellate hairy (especially dense along venation), dull, follicle stalk to 7-25 mm long. Seeds 1 per follicle, spherical to elliptic, glabrous, seed oriented away from follicle.
Flowering and fruiting: February-May.  Economic aspects: In China, the fruit is used to treat dysentery. The fruit is macerated in water in Cambodia, Thailand, and Malaysia, resulting in a massive increase in the volume of the outer shell or pericarp, generating a big gelatinous mass. Sweetened jelly is served as a delicacy. It also aids in the treatment of diarrhea and dysentery (Ahmed et al., 2009). Studies on biological activities reveals that fruit gel powder of Scaphium scaphigerum exhibit glucose absorption inhibitory effect and antioxidant activity. The quality-controlled fruit gel powder controls the body weight (Phlicharoenphon et al., 2017). Trees or shrubs. Leaves simple, entire or palmately lobed, rarely palmately compound, margin entire or dentate. Inflorescence usually axillary, paniculate, rarely racemose. Flowers unisexual. Calyx 5-lobed or 5-partite. Petals absent. Male flowers with anthers clustered at top of androgynophore, enclosing undeveloped carpels. Female flowers with very short androgynophore, staminodes at top of androgynophore in whorl around base of carpels. Carpels 5; ovules 2 to many per carpel; styles connate at base; stigmas as many as carpels, free. Fruit a group of follicles, usually leathery, less often woody, dehiscent when mature. Seeds 1 to many per follicle, usually with endosperm. A medium-sized tree, young parts rusty tomentose, bark greyish-brown, smooth. Leaves simple, 10-30 x 5-13 cm, oblong-ovate, rounded at the base, apex blunt or acute, densely stellate hairy on both surfaces, petioles 3-5 cm long, swollen at both ends, pubescent. Flowers small, yellow or greenish-purple, fragrant, on stellate hairy panicles, slightly drooping from ends of branches. Calyx campanulate, 5-lobed, 7-10 mm long, pubescent outside, hairy inside. Petals absent. Male flowers with 10 stamens, staminal column ca. 2 mm long, with a group of 2-loculed anthers at the tip, anthers sessile, staminodes 10. Female flowers with 5 carpels, free, hairy with 4-8 ovules; styles cohering, densely hairy; stigmas recurved, 5-lobed. Fruit a follicle, 4-5, oblong, woody, almost sessile, curved with dark brown tomentose surfaces. Seeds 3-6, oblong-ovoid, black, shining.
Flowering and fruiting: November-April. Chromosome number: 2n = 40 (Kumar and Subramaniam, 1986). Ecology: Usually grows in the hot, tropical lowlands and moderate highlands. Also found in the areas with or without a clear dry season. The species prefers a deep, fertile, moist but welldrained soil in a sunny, sheltered position. Global distribution: Bangladesh, Cambodia, China, India, Indonesia, Malaysia, Myanmar, Pakistan, Philippines, Sri Lanka, Thailand, Viet Nam, Eastern Africa and North Australia.
Economic aspects: The leaves and seeds of the species possess anti-inflammatory and antinociceptive activities. The seeds are fit for human consumption, representing a good source of fats (30%-36%) and proteins (11.4%). The leaves and bark are often used as diaphoretic, diuretic, and aperient agents and have been applied to the treatment of rheumatism, obesity, gonorrhea, edema, and skin disease. The plant serves as a repository of phytoconstituents, including alkaloids, flavonoids, terpenoids, phenols, and steroids. Therefore, these phytochemicals can serve as useful compounds in the searching of new small drug like potential molecules in the Computer Aided Drug Designing endevors (CADD). The ethanolic seed extracts have been reported to show antioxidant and anticancer activities (Alam et al., 2021). The sweet yellowish cotyledons are eaten after the black seed coat is removed. They are effective for rheumatism relief and are used as a laxative, diuretic, anti-epileptic, purgative and insect repellant. Seed oil is useful for lighting and painting, as well as treating itches and other skin disorders (Ashrafuzzaman and Sarwar, 2021). Vernacular names: Raiphal, Bansal. English name: Not known. A large evergreen tree, young parts rusty stellate tomentose, bark dark green, warty, cracked outside, blaze white, mottled with brown. Leaves simple, ovate, rounded, or slightly cordate at the base, acute or abruptly shortly acuminate at the apex, entire, under surface and petioles tomentose, petioles 2-7 cm long, stipules ensiform, caducous. Flowers white and pale yellow, in terminal, rusty, tomentose, racemiform panicles, pedicels 2-3 mm long, hairy, with an offensive smell. Calyx campanulate, deeply 5-partite, lobes narrowly lanceolate, rusty tomentose outside, glandular and with scattered long hairs inside. Petals absent. Male flowers with 10-12 stamens, staminal column 6-8 mm long, slender, curved, anthers 10-15, sessile, very small, staminodes 10. Female flowers with 5 carpels, free, ovary surmounting the ring of anthers, globose, woolly; styles curved; stigmas 5-lobed. Fruit a follicle, red when ripe, coriaceous, compressed, tomentose outside, smooth and reddish inside, with 3-5 seeds in each follicle. Seeds black and large.

Sterculia guttata
Flowering and fruiting: April-August. Ecology: The species occurs along the margins of evergreen forests, and in semi-evergreen forests. Very rare in moist, low-lying areas.
Flowering and fruiting: February-July. Ecology: Lowland and mixed deciduous forests. Found in a variety of substrates including basalt and calcareous shale.
Representative specimen: No specimen was available in any herbarium of Bangladesh. Global distribution: Bangladesh, Cambodia, India, Malaysia, Myanmar, Thailand and Viet Nam.

Sterculia lanceifolia
Flowering and fruiting: February-August. Ecology: The species is commonly found in the hilly forests.  Economic aspects: Timber serves as the source of fuel. It can also be used for different construction purpose and infrastructure development. Seeds are edible, often used in the form of condiments for seasoning of foods (Uphof, 1959 (Fig. 10). Vernacular name: Ranga Udal. English name: Not known. Large tree with spreading crown, 24-27 m tall, trunk straight, stout, bark grey, branchlets with prominent scars of fallen leaves. Leaves peltate, digitately 5-7 foliate, elliptic-lanceolate, 18.5-28.9 x 4-16 cm, tapering at the base, acute or shortly acuminate at the apex, subcoriaceous, glabrous above, puberulous or glabrescent beneath, petioles 8-15 cm long. Flowers fragrant, orange-yellow or pale-yellow, many, in erect panicles crowded at the ends of branchlets, pedicels short. Calyx campanulate, hairy, ca. 1 cm long, lobes oblong, inflexed. Male flowers with ca. 2 mm long staminal column, curved, filaments short, anthers 2-loculed. Female flowers with 5-lobed ovary, hairy with sterile anthers at the base; styles ca. 2 mm long, villous, curved with radiating sub-peltate stigmas. Fruit a follicle, slightly compressed, coriaceous. Seeds 7-15 mm long, oblong. Global distribution: Bangladesh, India and Myanmar. Economic aspects: Mainly valued for timber. Timber can serve as a useful source of fuel wood for its high heat yielding capacity. Seeds are edible, often eaten after roasting. Fiber obtained from bark is used to make ropes and cordage (Ahmed et al., 2009;Alam, 2018 The plant is also utilized by Indians as traditional remedy for inflammation. Sherbet, prepared from the petiole of the plant along with water and sugar is given in urinary problems and rheumatism. The bark and the petiole are used as a remedy in seminal weakness. White exudates of the tree are used for throat infection. Root infusion is taken as food adjunct while the whole plant extract is useful for skin diseases. The plant also has anthelmintic, antidiabetic, antimicrobial, membrane stabilization and antithrombotic activity. Some chemical constituents like flavonoids, chrysoeriol, diosmetin-7-O-β-D-glucoside and hrysoeriol-7-O-β-D-glucoside have been isolated from the species. These important phytochemicals can be used for computer aided drug discovery against suitable target using molecular docking, ADMET (absorption, distribution, metabolism, excretion and toxicity) and molecular dynamics simulation approaches (Hossain et al., 2013).

Discussion
Taxonomic revisions are required to keep track of potential changes and implications, as every new species discovered has an impact on the currently accepted system of classification (Stuessy, 1975). Phenotypic plasticity further necessitates the need of taxonomic revision as it is responsible for the expression of different types of phenotypes from the same genotype depending on the environmental effect (DeWitt et al., 1998). The present revisionary studies in the subfamily Sterculioideae with 16 taxa is the first on its nature in Bangladesh. Sterculioideae in Bangladesh incorporates a good number of economically and medicinally important taxa (Alam, 2018). Several attempts have been made worldwide to shed light on the current state of the member taxa of Sterculioideae. Taylor (1989) revised neotropical taxa of Sterculia L. which solved the controversy regarding the sexuality of the two floral types. The genus Brachychiton was previously included under Sterculia and its generic status was ambiguous. Later, Guymer (1988) resolved it into a distinct genus using characteristic features of follicles, seed coats and embryo. The problem of species delimitation in the genus Scaphium was solved by Wilkie (2009) with recognition of eight species which was four in the previous revision conducted by Kostermans (1953).
Several floristic studies have reported the occurrence of the member taxa of Sterculioideae throughout the country but no detailed revisionary studies have been carried out so far. The present investigation revealed five genera of Sterculioideae in Bangladesh such as Firmiana, Heritiera, Pterygota, Scaphium and Sterculia with two, four, one, one and eight taxa, respectively. Among the taxa studied, four taxa belonging to three genera could not be examined because of inavailability of these species and no specimens belonging to these species were deposited in any herbaria of the country. These four taxa were Firmiana simplex, Heritiera papilio, Sterculia balanghas and Sterculia parviflora. Firmiana simplex was reported as Sterculia urens Roxb. by Mia et al. (2011) based on the specimen examined by Hooker & Thomson in 1850, where no specific location was mentioned. Ahmed et al. (2009) stated the occurrence of Heritiera papilio from the forests of Sylhet district. Sterculia balanghas was reported by Raizada (1941) from the Chittagong Hill Tracts. Hooker (1874) reported Sterculia parviflora from the territory which at present falls under Sylhet region.
Based on the field observations, herbarium specimens and relevant literature (Ahmed et al., 2009;IUCN, 2012;Mia et al, 2011;Rahman et al., 2012;Alam, 2018;Ashrafuzzaman and Sarwar, 2021) the status of the taxa of the subfamily Sterculioideae has been determined. Among the studied taxa, Sterculia villosa and S. lanceifolia var. coccinea (= Sterculia hamiltonii) were found as common and considered as Least Concern (LC). Firmiana colorata, Sterculia foetida, Pterygota alata, Heritiera fomes, H. littoralis and H. macrophylla are rarely found in nature and going to be Near Threatened (NT). Scaphium scaphigerum was found as Vulnerable (VU), while Firmiana simplex, Sterculia guttata and Sterculia versicolor were found to be Endangered (EN). In the recent past, Ara et al. (2013) reported Sterculia versicolor as Endangered in Bangladesh that was supported by the present study. As a continuation of the current revision, we aim to apply the techniques of molecular systematics including DNA barcoding and phylogenetic analyses which would further strengthen the systematic position of the taxa of Sterculioideae in Bangladesh.