Ramachandra T.V, Gouri Kulkarni Akhil C.A, M.D. Subash Chandran
ENVIS[RP], Environmental Information System, Energy and Wetlands Research Group,
Centre for Ecological Sciences, Indian Institute of Science - 560012
envis.ces@iisc.ac.in    tvr@iisc.ac.in      Phone: 080 22933099/22933503

3. Entada rheedei (Fabaceae), the lianous species, is a conspicuous liana in the Western Ghats. It has a wider distribution in the world tropical Africa, India to China, Philippines and northern Australia. In India it occurs from sub-Himalayan tracts through the states of Sikkim and Assam to Bihar and Orissa to the monsoon forests of Western and Eastern Ghats (Brink, and Achigan-Dako, 2012). It is also found in the Andaman Islands. This magnificent liana is seen along river and stream sides of humid forests. Entada rheedei with its angled woody stems racing up even the tallest trees, coiling anti-clockwise and clockwise on support, is a phenomenal species that one could witness in the Western Ghats. Its growth dynamics could be now noticed in the urban ecosystem of Bangalore, by observing a remarkable specimen of Entada, in the Indian Institute of Science, on Silver Oak marg in front of the Centre for Ecological Sciences, introduced from the Western Ghats in late 1980's. Seeds of Entada were collected from the Western Ghats (13^o55'-15^o31'N, 74^o9'- 75^o10'E) about 55 km from the Arabian Sea, at an elevation of 700-800 msl. The region receives 450 cm or more annual rainfall, and during post-monsoon period the wind speed is 8-10 m/s. Following mechanical cracking of the hard testa, the seeds were kept in a coarse cloth bag and floated in pond water for about 20 days before sowing at various places in the campus. Of the seven seeds sown, one buried in the soil close to a tree of Bauhinia purpurea (Fabaceae) has grown into a liana, spreading its canopy on a miniforest of the semi-evergreen tropical trees.

A single plant has unexpectedly attained a gigantic size in 25 years, with its canopy infesting the crowns of nearby trees which covers an area roughly equivalent to 1.6 ha. It has remarkable aerial stolons, of about 15 m long, even crossing over a tar road through the air, without any support, and reaching the trees in a mini-forest on the other side where it is firmly anchored to trees and clumps of bamboos, spreading rapidly (Maheshwari et al., 2009). Frightened with the profuse growth and spread of aerial stolons (with the excuse of possible threat to motorists on the road below) one of the administrator got some stolons cut or pruned. It was noticed water trickled out of stolons, showing how an efficient water conducting system is working through the entanglement of branches.

Different parts of Entada rheedei have been used in native medicine. The folk healers of Araku Valley in the Vishakapatanam district apply seed paste to scabies and boils (Padal and Sathyavathi, 2013). Two new tryptophan derivative compounds from the seed kernels of E. rheedei may offer an alternative as potential therapeutic for cancer and AIDS (Nzowa et al., 2013). In Southeast Asian countries and in India the various parts of the climber are used in different ways to cleanse fresh wounds, heal minor scrapes and burns (Bureau of Plant Industry, 2009). Seed paste of Entada is applied over the affected and the inflamed swellings by the Kanikkar tribe of Agasthyamalai in Kerala, reduce pain due to rheumatism. Its anti-inflammatory property has been proved by Kalpanadevi et al., (2012).

The seeds of Entada from India are coveted items in the Egyptian market because of the medicinal values. Seeds of Entada are rich in potassium (K) and phosphorous (P) (1264 and 1240 mg/100 g respectively), followed by calcium (Ca) and sodium (Na) (199 and 68 mg/100 g respectively). The micro element Iron (Fe) level in the seed was 3.3 mg/100 g. Richness of these elements in the seeds probably accounts for their medicinal as well as dietary values (Okba et al., 2013). Amino acids are also an important constituent in seeds of Entada rheedei. According to the study of Okba et al., 2013 the total percentage of the amino acids in 100 grams of seeds was 23.499 g. Leucine is one of the essential amino acid (2.597 g/100 g seeds), followed by phenylalanine (2.116 g/100 g seeds) and lysine (1.776 g/100 g seeds). Phenyl alanine is useful in treating painful arthritic problems. Its relatively high level in Entada seed may explain its use in folk medicine specially for treating arthritis and other rheumatoid diseases. Glutamic acid (3.737 g/100 g seeds) was the main non-essential amino acid, which is important in the metabolism of sugars and fats and used in treatment of ulcers.

The Entada is encompassed of a mix of tree structures and a woody climber, and some unique structures. Its erect trunk is comprised of anticlockwise-twisted pleats. Its climber part comprises of hammock-like, twisted, woody stems. The structure that has spread its canopy from one support tree to another are long, leafless, cable-like stems (stolons) that navigated aerially approximately 15 m above the ground, differentiating foliage upon accessing a living tree.

3.1 Anticlockwise twists in climbing parts: The uncoiled trunk pleats have branched out into hammock-like, highly twisted, woody branches (Figure 1). Yet, no above-ground part has twined around a support tree or its branches, hence Entada is not a twiner. Rather, its branches mostly lie on the host branches for support and are occasionally entangled into them. A striking feature of Entada are the climbing branches shaped into an 'Archimedes screw' with pronounced tangential thickening (Figure 2) (Vogel 2007).

The predominantly anticlockwise helices in Entada prompted to examine the direction of coiling in climbers growing in a nearby miniforest in the campus. Anticlockwise ascend was observed in all climbers. Edwards et al in 2007 reported anticlockwise twining in plants at 17 sites in nine countries in both the northern and southern hemisphere. An exception is the yam Dioscorea, where species have been classified on the basis of stems twining to the left or to the right (Gamble 1935; Punekar and Lakshminarasimhan, 2002). The handedness of growth depends on the orientation in which cortical microfibrils are organized under the control of spiral gene (Hashimoto 2002). However, it is not known whether helical microtubule arrays are the cause or the consequence of organ twisting. We have not observed any thorns, hooks, spines or stem tendrils that could facilitate anchoring of Entada to the supporting tree. Rather, physical support is gained by occasional placing of its branches on those of support trees. Some of its overhanging leafy branches that were exposed to full sunlight during March-April (before monsoon rains begin) produced inflorescence (Figure 1.b).

3.2 Hydraulic supply: The parent and interconnected daughter canopies of Entada are founded on; a single germinated seed and hence on a single root system. Since the aerial stolons ultimately connect to the rooted trunk, these must constitute the hydraulic system for the entire canopy. When aerial stolons (cables) extending across a road junction, posing hazard to motorists were cut, colourless, watery sap trickled from the cut cables. This suggests that water is translocated by root pressure, requiring development of non-destructive methods for investigation of its underground parts. Apparently, the twists in plant structure do not resist the movement of water, making Entada a good material for investigations of pressure-generating capability for water movement, compared to a tree. Following severing, the daughter canopies differentiated by aerial stolons and distributed on surrounding trees dried, confirming that the aerial cables constitute the hydraulic supply system and the structural form for the spread of the canopy on support trees.

3.3 Ecophysiology: Occasionally, a terminal leaflet in the pinnate compound leaves of Entada is modified into a forked tendril. Tendril development may be influenced by the amount of light filtering through the canopy, and its function may only be to orient the leaf for maximal absorption of sunlight by the canopy in natural habitat under cloudy conditions. A visual comparison of the density of Entada foliage with that of the surrounding trees suggests that this liana invests more of photo synthetically fixed carbon in woody branches, which have a capacity to resprout after breakage.

The first sighting of a single 12 inches long, green pod was in May 2003, and again in 2005 2008, 2011 and 2015. It therefore appears that fruiting in the alien environment is a rare phenomenon, for unknown reasons. Although being a leguminous plant, Entada is assumed to be self-pollinated, the lack of a pollinator species could account for its rare fruiting. Further observations are required to determine if flowering and fruiting in the daughter canopies is synchronized with that of the interconnected parent canopy.

The ability to produce large pods with rather large seeds (Brandis 1921, Saldanha and Nicolson 1976) suggests a high photosynthetic rate. It is believed that lianas have a fast growth rate because of their high photosynthetic rate due to elevated CO₂ in the canopy (Granados and Korner 2002). Contrary to popular belief, liana density and growth are unrelated to the mean annual precipitation (Rowe 2004, Granados and Korner 2002, Schnitzer 2005). Schnitzer in 2005 reported that lianas grow nearly twice as much as trees during the wet season, but more than seven times that of trees during the dry season. This observation was corroborated by Swaine and Grace (2007). In view of the requirement of seedling material for experimental investigations in the laboratory, the reproductive biology of Entada assumes special importance.

3.4 Spreading strategy: Previously all reported lianas spread their canopy by means of ground stolons which then climb on available support. Entada is unique: it has formed specialized, cable-like, aerial stolons that have extended near-horizontally into air, crossing gaps and spreading canopy from the primary support tree onto the crowns of other support trees. The length of these aerial stolons exceeds 15 m; and there is no evidence of a support tree being present between the inter-support distances, because of a dividing tarred road. The aerial stolons traversing a road junction over a lamp post highlights of an unusual plant type growing in the campus. Following contact with the crown of support trees, the stolons have branched and much of their twisted woody branches appear to support each other (self-support), with this being augmented by the branches that have infiltrated into the trees. A stand of bamboo culms accessed across a gap due to a road is bent down to a greater degree than the uninfested culms, either because of the weight of Entada or because Entada exerted a force to pull them down. Structural adjustments that are required to counter stress and strain as a consequence of tension due to pull need further investigations. The aerial stolons are oriented towards a vegetated tract across a tarred road without crisscrossing, a possibility is that other than phototropism, some volatile chemicals produced by the 'host' trees not only provided a cue for the development of cables, but also directed their extension towards trellises.

This speculation is supported by a recent finding that volatile compounds, alpha-pinene, beta-myrcene, 2-carene, p-cymene, beta-phellandrene, limonene, (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene and an unidentified monoterpene released by tomato plant guide the dodder vine, Cuscuta pentagona (Runyon et al., 2007). Rowe and Speck (2005) have illustrated 'searcher branches' in a woody liana Strychnos sp. (Loganiaceae), having a cable-like appearance and extending horizontally 3-4 m across the canopy gap to locate new support. Upon contact with a neighbouring tree, the Entada cables (stolons) differentiated normal foliage, viz. compound leaves with thick leaflets. The branches of Entada have infiltrated and entangled with that of Bauhinia purpurea, Cassia spectabilis, Broussonetia papyrifera, Tebebuia rosea, Eucalyptus tereticornis, Tectona grandis and Bambusa sp. However, Entada was not observed on dead branches of standing trees, raising the possibility of requirement of living support trees for infestation. Since coiling, bending or flexing and differentiating into morphologically distinct parts occur in response to contact, the phenomenon of thigmomorphogenesis appears to be important in the infiltration and spread of Entada on living trees. It was not observed surface-growing stems in adult Entada. Its aerial stolons changed morphology upon accessing a support tree, suggesting that in addition to light and circumnavigational movement, contact-induced differentiation of foliage is important in mechanistic explanation of Entada spread on crowns of support trees as a straggler. Trellis availability is a major factor determining the success of canopy-bound lianas (Putz 1724).

3.5 Regeneration: Aerial stolons (diameter approximately <10 cm) that had begun to cause obstruction to vehicular traffic were cut. Two to four meter long cut pieces of woody stems (diameter 20-30 cm) were gathered and left in the open. In about 4 weeks the cut stems sprouted one to 1^1/2 m tall shoots with stiff, erect stems producing foliage. Since sprouting occurred during the dry season, this observation signifies that Entada stores considerable water inside the stem tissue. However, the cut stems did not root, and the sprouts dried after the rains ceased. However, the ability of cut stems to re-sprout has implication in its natural habitat where strong wind and rain prevail: The branches that are unable to resist wind-induced breakage or those that are unstable under their own weight may fall on the ground and function as ramets (vegetatively produced, independent plants). This raises the question of the specific contribution of the ramets (broken and fallen branches that resprout and form roots) versus the genets (single individual plants from sexually formed seeds) in the composition of Entada thickets in its natural habitat.

3.6 Paradox of growth in alien environment: Factors that may explain an alien liana thriving in a place which receives only about 95 cm annual rainfall and where the soil surface (red earth) is generally dry, except for the monsoon months (May-September) are:

• Foremost, a safe mode of infiltration on available support trees by means of aerially formed stolons, thereby avoiding risk of injury from trampling by grazing animals.
• Nutrient-rich soil in the campus compared to the soils in rainforests is generally nutrient-poor because of the leaching of nutrients by rains through the millennia (Richards 1972, Terborgh 1992; Van der Heijden and Phillips, 2008).
• Presumed deep root system of Entada allowing access to water table, or water which seeped down from a nearby stream. This is in keeping with a report (Restom and Nepstad 2004) that root systems in excavated liana seedlings of Davilla kunthii (Dilleniaceae) in eastern Amazonia were more than eight times longer than the aboveground stem.
• Higher solar illumination (Heijden et al., 2008).
• Absence of herbivores or pathogens and less competition for resources as more area is available for aerial spread, root growth and nutrient absorption, unlike in dense vegetated tropical forests.

Despite the extensive spread of Entada genet in an alien environment. However, ecologically 'success' is a measure of reproductive efficiency, namely the number of individual genets or ramets per unit area and density of liana growth (Heijden et al., 2008). Success of introduced Entada be assessed by production of new genets or ramets.

Figure 2: Hammock-like branches with twists. b. Spread of E. pursaetha c. The climber-form of E. pursaetha d. tree-form of Entada pursaetha self-supporting trunk in proximity to Bauhinia purpurea.