Ficus (PROSEA Medicinal plants)

Plant Resources of South-East Asia
Introduction

Protologue: Sp. pl. 2: 1059 (1753); Gen. pl. ed. 5: 482 (1754).

Family: Moraceae

Chromosome number: x= 13; 2n= 26 for the vast majority of species (e.g.F. hispida, F. religiosa), 2n= 52 for few species

Major species

Ficus benghalensis L.,
F. hispida L.f.,
F. religiosa L.,
F. rumphii Blume,
F. septica Burm.f.

Vernacular names

Ficus, fig (En)
Figuier (Fr)
Indonesia: ara, bunut, karet
Malaysia: ara, ara kelumpong (stem figs), ara tanah (geocarpic figs), nunok (strangling figs, Dusun, Sarawak), giwit (geocarpic figs, Dusun, Sarawak)
Philippines: balete (Filipino). Burma (Myanmar): nyaung
Laos: hai
Thailand: sai
Vietnam: chi da, dề, sung.

Origin and geographic distribution

Ficus comprises about 1000 species and occurs in all tropical and subtropical regions, with a few species in warm temperate areas. About half of the species occur in Malesia, which forms the main centre of speciation.

Uses

The latex of many Ficus species is used medicinally, mainly to cover and cure wounds, boils and sores, but also as an antirheumatic, and it is swallowed to cure coughs and colds and to treat diarrhoea. The bark of many species has astringent properties. In India, the dried bark of F. benghalensis and F. religiosa is used as an antidiabetic.

Several of the medicinally used Ficus species yield useful timber, used for e.g. temporary construction, interior work, concrete formwork, small domestic articles, fruit crates, low grade plywood, and firewood. The fruits of some species are edible but are generally not sought after or prized. Some Ficus species have poisonous fruits. The latex has been used as a wax in dyeing batik cloth. The latex is also used as birdlime and in Papua New Guinea for sealing leaks in canoes, whereas that of some species is highly toxic and applied as dart poison. The tough and fibrous bark of a few species is a well-known raw material for rough cordage and matting and formerly for clothing; it is still used for bow strings and fish nets. Young leaves of several species are eaten raw in salads or cooked with meat wrapped in them; the latter dish is considered a delicacy in the highlands of New Guinea. They have also been used as fodder, and leaves of other species are applied as sandpaper or to scour cooking pots. Several Ficus species are well-known for their ornamental value, planted as wayside trees or even grown commercially as pot plants in temperate regions.

F. benjamina L., F. elastica Roxb. ex Hornem., F. minahassae (Teysm. & de Vriese) Miq., F. racemosa L. and F. retusa L.f. are also used medicinally but have other primary uses.

Properties

Bark extracts of various Ficus species (F. benghalensis, F. racemosa, F. religiosa, F. rumphii) display hypoglycaemic effects, which are probably mainly related to the presence of β-sitosterol and its related compounds. A bark extract of F. benghalensis showed in vitro hypoglycaemic activity (the lowering of blood glucose) in both normoglycaemic and moderately diabetic (streptozotocin-induced) rats after oral administration. The extract also enhanced serum insulin levels in both groups of animals. Furthermore, incubating of isolated islets of Langerhans from normal and diabetic animals with the extract stimulated insulin secretion, and reduced the insulinase activity of liver and kidneys. The alcohol extract of F. racemosa also showed hypoglycaemic effects in rats.

The stem bark of F. benghalensis contains β-sitosterol and its glucoside β-sitosterol-D-glucoside. Both compounds have also been isolated from other species: the former from F. rumphii and the latter from the bark of F. religiosa. Stigmasterol and β-sitosterol (both sterols) and lupeol (a related triterpene) have been isolated from the petroleum ether extract of trunk bark of F. religiosa. β-Sitosterol-D-glucoside produced a hypoglycaemic effect in rabbits, which compared favourably with tolbutamide as a positive control. Although the aglycone β-sitosterol is also active, the glucoside is more potent, probably because of its better water solubility and adsorption.

Also of interest besides the sterols are the flavonoids coumarin and related compounds isolated from Ficus species. A dimethoxy derivative of leucocyanidin-3-O-β-galactosyl-cellobioside, isolated from the bark of F. benghalensis and administered orally (250 mg/kg) decreased blood glucose levels significantly in normal and moderately diabetic (alloxan-induced) rats, and increased serum insulin significantly in the latter group. Furthermore, during one month treatment of the diabetic rats orally (100 mg/kg), a significant decrease in blood and urine sugar was found, as compared with the diabetic controls. A dimethoxy ether of leucopelargonidin-3-O-α-L-rhamnoside (from the bark of F. benghalensis) has also been tested for antidiabetic effects. A medium effective dose (100 mg/kg) administered orally to normal and moderately diabetic (alloxan-induced) dogs, significantly reduced blood glucose and raised serum insulin. Acute and chronic administration in single doses of 0.2-1.8 g/kg to mice, and daily administration of 100-500 mg/kg to rats for a period of one month did not produce observable toxic effects. The antidiabetic effects e.g. low blood glucose levels, glucose tolerance and urinary sugars, were also found in normal and in moderately diabetic rats compared to glibenclamide as a positive control. Finally, in vitro studies showed that insulin secretion by pancreatic β-cells was greater in the presence of the leucopelargonidin derivative than in the presence of the leucocyanidin derivative.

An alcohol extract of the bark of F. religiosa showed parasympatholytic effects and a protective action against acetylcholine and histamine-induced asthma in guinea-pigs. The extract also showed antiprotozoal, protease inhibitor and antiviral activity. Antiprotozoal activity is furthermore reported from the alcohol extract of F. racemosa.

A methanolic extract of the leaves of F. septica displayed intense antibacterial and antifungal activities. This activity is probably related to the presence of 2 indolizidine alkaloids, ficuseptine (4,6-bis-(4-methoxyphenyl)-1,2,3-trihydroindolizidinium chloride) and antofine. A leaf extract of F. religiosa showed antifungal properties against Diplodia natalensis, the agent of stem-end rot of mango fruits. Fruit extracts of F. benjamina, F. benghalensis and F. religiosa also had significant antibacterial activity, but no antifungal activity. Furthermore, the extracts of F. benghalensis and F. religiosa demonstrated activity in the brine shrimp assay (Artemia salina) which indicates toxicity, whereas F. benjamina showed no activity. All the fruit extracts exhibited antitumour activity in the potato disk bioassay, and none of the tested extracts showed any marked inhibition on the uptake of calcium into rat pituitary cells (GH-4C-1). A water extract of dried fruits of F. benghalensis exhibited anti-HIV activity.

The anthelmintic properties of several Ficus species (e.g. F. pumila) can be ascribed to the proteolytic enzyme ficin present in the latex. Excessive amounts of this substance are toxic to humans when administered orally or intravenously. Furthermore, ficin, whether fresh or dry, is highly irritant to the skin and eyes.

Seed extracts of F. deltoidea have been observed to agglutinate human erythrocytes (A, B, AB, 0), and some strains of bacteria including Chlamydia trachomatis, a significant pathogen. Seed extracts of F. racemosa have been found to agglutinate white blood cells from patients with different types of leukaemia.

The popular pot plant F. benjamina may give rise to allergic reactions, e.g. conjunctivitis, rhinitis. Sensitization is believed to occur by inhalation of allergen-enriched dust emanating from the leaves.

Phytochemical investigations of a petroleum ether extract from dried F. hispida bark yielded the acetates of n-triacontanol, β-amyrin and gluanol, whereas the leaves contain bergapten, psoralen (two furanocoumarins, which might give rise to phototoxicity), β-amyrin and β-sitosterol. The leaves of F. pachyrrachis contain 2 tetrahydrobenzylisoquinoline alkaloids, (-)-reticuline and (+)-norreticuline.

Description

Evergreen or sometimes deciduous, woody epiphytic climbers or stranglers, creepers, shrubs or small to large trees up to 40(-50) m tall, or banyans, i.e. trees whose branches send down aerial roots that thicken ("pillar roots") and function as props; bole fairly straight in tree-like species, sometimes fluted, up to 100(-190) cm in diameter, sometimes heavily buttressed; bark surface smooth, often pale grey, sometimes whitish or brown, sometimes lenticellate, inner bark yellowish, exuding white or yellow latex.
Leaves arranged spirally, alternate or opposite, simple to palmately lobed, symmetrical to asymmetrical, dentate to entire, often with glands below in the axil of the lateral or basal veins or abaxial at the apex of the petiole; stipules free or connate.
Inflorescence axillary or ramiflorous to cauliflorous, sometimes subterranean, solitary or clustered, monoecious or gynodioecious, with the flowers set inside an urn-shaped receptacle (syconium; a fig).
Flowers unisexual; tepals 2-8, free or joined; stamens 1-7; ovary unilocular with a single ovule, style single.
Infructescence a subfleshy fig; individual fruit a drupelet.
Seedling with epigeal germination; cotyledons emergent; hypocotyl elongated; all leaves arranged spirally.

Growth and development

The strangling figs start as epiphytic plants and send down aerial roots that eventually form a false trunk composed of a trellis-work of interlacing and anastomosing roots around the trunk of the support tree. The roots of F. religiosa, however, penetrate inside the support trunk, eventually splitting it from within. Many species have more than one kind of leaf (heterophylly).

The symbiotic relation of figs with specialized wasps is well-known. Figs can only be pollinated by female agaonid wasps (Hymenoptera, Chalcidoidae, Agaonidae). The wasp species are highly species-specific. Fig species are divided into 2 groups: monoecious species and gynodioecious ones. In the former the wasps arrive when only female flowers are receptive. They enter the fig via the osteole, a bract-covered apical pore. Once inside, they pollinate the female flowers and deposit their eggs in the ovaries. As style length varies greatly within these figs and because the wasp can only reach the ovary of short-styled flowers, only some of the flowers obtain an egg, while in others the seed develops. Male and female wasps emerge after a few weeks, and mating takes place within the fig. The females then emerge from the fig and, in so doing, pick up pollen from the newly mature anthers. On a single tree figs mature at the same time, while different trees of the same species flower out of synchrony, thus inducing cross-pollination. The gynodioecious fig species either bear hermaphrodite figs or figs with female flowers only. In hermaphrodite figs the styles are uniformly short. Wasps can oviposit every female flower and such trees rear the pollinators' offspring and function as pollen donors. All the flowers of female-flowered figs have long styles. The wasps can only deposit pollen, so such figs produce large amounts of seed.

During daytime the figs are eaten by birds (e.g. pigeons, hornbills, bulbuls, cassowaries), monkeys and squirrels. At night they are visited by bats and civet cats. Cauliflorous figs are eaten by deer and pigs. The latter also uproot the geocarpic figs. Even elephants, rhinoceros, tapir and wild cattle have been reported to feed on figs. As fig fruits are often available year-round, they constitute an extremely important forest food, a so-called keystone resource that sustains frugivorous animals at the famine period of the year when few species, if any, are fruiting.

Other botanical information

In Asia and Australia the large genus Ficus has been subdivided into 4 subgenera, 14 sections and numerous smaller taxonomic groups.

Ecology

Ficus species are common and form an important element of lowland rain forest, both as canopy and understorey trees. Most species prefer per-humid forest, but several are found in areas with a monsoon climate and in teak forest, including locations where the soil dries out. Ficus does not occur in mangrove vegetation but is often present in brackish swamps behind the mangrove. Ficus species are generally found below 1500 m altitude, some between 1500 and 2750 m or rarely up to 3200 m. Many are epiphytic and/or strangling.

Propagation and planting

Ficus can be propagated from seed and vegetatively. Per kg there are about 2.1-2.5 million seeds of F. benghalensis. The drupelets are usually the unit of sowing. These cannot be stored without a serious decrease in viability. A 50% germination rate is achieved in 27-37 days in F. deltoidea and in 18-34 days in F. microcarpa. In India, pretreatment with hot water of 60°C for 10 minutes was found to increase the germination rate from 20% to 24% in F. benghalensis and from 19% to 28% in F. racemosa. The tiny seedlings are pricked out twice, first in clumps and later individually. The young seedlings are sensitive to excess of water. Both large and small cuttings are used in vegetative propagation, but small cuttings are less successful. Tissue culture and air layering can also be used for propagation of Ficus . Some species, e.g. F. hispida, easily regenerate naturally in abandoned fields.

Yield

Information on yield of Ficus is rather scarce. Petrol and methanol extraction yielded a residue of 85 g from 1.7 kg powdered leaves of F. septica. Complete isolation yielded 500 mg of ficuseptine and 130 mg of antofine.

Handling after harvest

The bark, roots or leaves of Ficus can be applied fresh or dried. The fresh products are used or sold shortly after harvesting. When dried in shade or sunlight the products can be stored for longer periods.

Genetic resources and breeding

With the exception of some species that are widely planted (these include F. benghalensis and F. benjamina) there are no records of ex situ conservation of Ficus. Some of them have a high ritual or ornamental value and have been translocated within South-East Asia or even on a worldwide scale. As most Ficus species are fairly common and widespread, the risk of genetic erosion seems comparatively low. Breeding efforts are restricted to species with ornamental value, of commercial importance.

Prospects

Some Ficus species are well-known medicinal plants which have been successfully used in the treatment of common illnesses. The promotion of traditionally used plant resources that are widely available or can easily be grown deserves attention from government extension workers, especially in rural areas. Ficin as found in the latex of F. pumila can be used for its anti-inflammatory properties. Its proteolytic activity makes it a potential meat tenderizer in industrial applications.

Literature

Achrekar, S., Kaklij, G.S., Pote, M.S. & Kelkar, S.M., 1991. Hypoglycemic activity of Eugenia jambolana and Ficus bengalensis: mechanism of action. In-Vivo 5(2): 143-147.
Agrawal, S. & Agarwal, S.S., 1990. Preliminary observations on leukaemia specific agglutinins from seeds. Indian Journal of Medicinal Research 92: 38-42.
Baumgartner, B., Erdelmeier, C.A.J., Wright, A.D., Rali, T. & Sticher, O., 1990. An antimicrobial alkaloid from Ficus septica. Phytochemistry 29(10): 3327-3330.
Berg, C.C., 1989. Classification and distribution of Ficus. Experientia 45: 605-611.
Boer, E. & Sosef, M.S.M., 1998. Ficus L. In: Sosef, M.S.M., Hong, L.T. & Prawirohatmodjo, S. (Editors): Plant Resources of South-East Asia No 5(3). Timber trees: Lesser-known timbers. Backhuys Publishers, Leiden, the Netherlands. pp. 232-238.
Bronstein, J.L. & McKey, D., 1989. The fig/pollinator mutualism: a model system for comparative biology. Experientia 45: 601-604.
Cherian, S., Kumar, R.V., Augusti, K.T. & Kidwai, J.R., 1992. Antidiabetic effect of a glycoside of pelargonidin isolated from the bark of Ficus bengalensis L. Indian Journal of Biochemistry and Biophysics 29: 380-382.
Hunter, J.B., Suresh, M.R., Keshvarz, E., Wenman, W.M. & Micetich, R.G., 1986. Purification of lectins from Artocarpus altilis and Ficus deltoidea by gel filtration fast protein liquid chromatography. Biochemical Archives 2(2): 99-106.
Mousa, O., Vuorela, P., Kiviranta, J., Wahab, S.A., Hiltunen, R. & Vuorela, H., 1994. Bioactivity of certain Egyptian Ficus species. Journal of Ethnopharmacology 41(1-2): 71-76.
Verheij, E.W.M. & Coronel, R.E. (Editors), 1991. Plant Resources of South-East Asia No 2. Edible fruits and nuts. Pudoc, Wageningen, the Netherlands. pp. 334-336.

Selection of species

Authors

J.P. Rojo, F.C. Pitargue & M.S.M. Sosef