Climber Diversity across Vegetational Landscape of North-Eastern Uttar Pradesh , India

The composition and diversity of climbers among grassland, wasteland and forest vegetations was examined with respect to their woodiness, climbing mode and circumnutation pattern across the vegetational landscape of north-eastern Uttar Pradesh during 2011-2015. A total of 111 climbers, constituting 63 lianas and 48 vine species, under 35 families, were recorded. The forest and wasteland vegetation were quite similar in regard with climber diversity. Family Convolvulaceae included a maximum of 19 climbers. Majority of twining climbers showed right-handed twining. The wasteland vegetation was most suitable and quite similar to forest habitat for vines as well as for lianas. The right handed circumnutation was the dominant pattern among the twiners of the region. Local climbing flora provides considerable natural resource to the region. They often create special micro-habitats and increase the complexity of the ecosystem.


Introduction
About half of the families of vascular plants contain climber species (Schenck, 1892).Gentry (1991) predicted a very high diversity of vines and lianas in the tropics with over 8,000 species under 130 families.A global analysis reported approximately 80% and 20% of lianas and vines in tropical regions, while in extra-tropical regions they account for 60% and 40%, respectively (Gallagher and Leishman, 2012).The ecological studies of climbers have dealt primarily with lianas (> 1 cm dbh) occurring in tropical forest communities (Schnitzer and Bongers, 2002;Burnham, 2004;Parthasarathy et al., 2004;Jayakumar and Nair, 2013).However, relatively few studies have included vines (Kokou et al., 2002;Gallagher et al., 2011) which play a significant role in the structure and function of grassland ecosystem (Mao and Zhu, 2006;Zhang et al., 2011).
Climbing plants also show great diversity in their climbing mechanisms (Putz, 1984;Bongers et al., 2005).They include twiners, tendril climbers, root climbers and scramblers.Climbers also have evolved exaggerated form of circumnutation to increase the probability of encountering a support or avoiding hurdles (Darwin, 1875).Documentation on their behaviour and causes of circumnutation of twining and tendrilar climbers has been worked out by many researchers (Darwin, 1875;Brown, 1993;Larson, 2000;Silk and Holbrook, 2005;Gerbode et al., 2012;Silva et al., 2016).Twining plants generally show fixed handedness, either consistently forming right-handed or left-handed helices, as they climb (Hashimoto, 2002;Edwards et al., 2007).However, Davis (1974), exceptionally observed both in Mikania micrantha at different latitudes.Burnham and Revilla-Minaya (2011) presented the handedness of 60 twining taxa of a forest community in Peru and observed both the left and right handed twining in the same individual of a climbing species of family Dilleniaceae.The global trend in plant twining direction was analyzed by Edwards et al. (2007), but they were unable to observe any hand reversal in the same twining plant.
The present study provides an account on the diversity of taxa with climbing habit in different vegetation types of northeastern Uttar Pradesh, India.The study also emphasizes the handedness in twining and tendrilar types of climbers across the vegetation.So far, no information on handedness is available for climbers of India.

Study area
The vegetational landscape of north-eastern Uttar Pradesh lies within the Terai belt of the foot hills of the Himalayas.The area extends between 26 °21' to 27 °32' N latitude and 81 °34' to 83 °57' E longitude.Mean altitude of the study area is 95 m.The climate of the region is generally tropical monsoonic with three distinct seasons viz.summer (March to mid June), monsoon (mid June to mid Oct) and winter (mid Oct to Feb).The total average of annual rainfall is aprox.1,704 mm, most of which (>94%) is received during monsoon and the rest is showed that about 58.6% of climbers were perennials and the remainders were annuals.Among the six dominant families, Convolvulaceae was the most climber-rich (19 species), followed by Papilionaceae (15 Species), Cucurbitaceae (10 species), Asclepiadaceae (9 species), Dioscoreaceae and Menispermaceae (6 each).The remaining 46.85% of climbers represented 29 families, of which 18 families were represented by only one species of climbers.In terms of genera, Papilionaceae was the most dominant (13), while Ipomoea was the most specious genera (11 climbers).
The number of species, genera and family of climbers was highly variable among the three vegetation types (Table 1).The forest and wasteland vegetation were quite similar in climber diversity as compared to grassland vegetation.The species per genus ratio and that of per family ratio was greater in the case of grassland.Among climbing plants, the woody climbers (lianas) were represented by 63 species and herbaceous climbers (vines) by 48 species.There were two parasitic vines e.g.Cuscuta chinensis and C. reflexa.The forest vegetation was largely dominated by lianas and grassland by vines.Wasteland vegetation was found to be the suitable habitat for both categories of climbers (Fig. 1).

Stratification
Quite large number of climbers of the region are under lower strata (78 species) followed by middle strata with 17 species and upper strata with 9 species (Table 2).Tinospora sinensis reached the most distant canopies (29.75), among the minor woody climbers, preferably over Bombax cieba.Combretum decandrum, the massive liana, also reached as high as 28 m.All the 9 climbing species of the upper stratum were twiners except Antigonon leptopus, which reached a relatively lower height.Majority of the middle strata climbers were lianas.The herbaceous and less woody climbers namely Coccinia grandis, Dioscorea bulbifera, Ichnocarpus frutescens, Ipomoea quamoclit and Telosma pallida may also reach this layer through twining over Tinospora sinensis.The climbers of the lower strata layer were generally of tendrilar type.They grow over shrubby plants and various other objects luxuriantly.The twiners of the lower stratum spread over ground in absence of any support.
Few massive lianas, especially straggling-armed climbers formed thickets in different strata.The chief thicket forming species namely, Caesalpinia bonduc, C. cucculata, C. decapetatla Calamus tenuis, Capparis zeylanica, Rosa clinophylla and distributed in the form of occasional showers.The annual mean of relative humidity ranges between 74-87%.The mean maximum temperature during wet summer, winter and dry summer seasons are 34.1 °C, 23.2 °C and 36 °C and mean minimum temperatures are 24.3 °C, 10.3 °C° and 19.7 °C, respectively.The soil of the region is a part of trans-Sarju plain and comprises Gangetic alluvium, ranging from clayey to sandy loam in texture with pH ranging from 6.5 to 7.5.
The major vegetation (physiognomic) types identified in the region are forest, wasteland and grassland (Shukla, 2009).Though regional climax vegetation is semi-evergreen forest (Champion and Seth, 1968), but most of these have been converted into agricultural fields, orchards, human habitations and commercial plantations.

Methods
The current study is based on extensive field survey and analysis of vegetation across the vegetational landscape of the 11 districts of north-eastern Uttar Pradesh during 2011-2015.The identification was done using local and regional flora (Srivastava, 1976;Saini et al., 2010) and online Indian floras.The species of climbers were identified with similar specimen of herbarium of Gorakhpur University.The botanical names and author citations were checked through International Plant Name Index (IPNI).An analysis of species diversity of climbers was made on the basis of taxa composing the vegetation types.The climbing mode, occurrence status and approximate life-span of different species have been tabulated in supplementary Table 1.
Climbing plants were inspected for their height they attained and grouped into upper strata (> 20 m), middle strata (10-20 m) and lower strata (< 10 m).The height was measured with the help of clinometer.The objects including plants which supported their climbing were marked and their circumnutation pattern was also observed.Tendrilar climbers were grouped into simple (or unbranched) and branched types.The pattern of handedness was also compared among individuals growing within different habitats or vegetation types.For common and abundant species, 20 individuals of each species were selected, separately for each vegetation types.However, only 5 individuals per species were inspected in case of rare species.The present study addresses climbers only of wild occurrence.The ornamental or garden climbers were excluded from the observation.

Climber diversity
A total of 111 climbing species representing 81 genera under 35 families were encountered across the vegetational landscape of north-eastern Uttar Pradesh.The life-span data Ziziphus oenoplia constituted the lower strata.Acacia concinna, Bridelia stipularis and Capparis zeylanica, however, formed thickets and were the components of middle strata.These species often entangled with twiners and acted as a safe repository for rare plants and small mammals.

Climbing and circumnutation
All the twining and tendrilar climbers showed general pattern of handedness irrespective of the vegetation types.Of the 26 tendrilar climbers, 14 species had simple un-branched tendrils, while remaining had branched tendrils.In 9 such species the tendrils were bifid and in 3 species, namely Antigonon leptopus, Naravelia zeylanica and Trichosanthes cucumerina were trifid (Supplementary Table 2).Every tendril showed both the left-handed as well as right-handed coiling.The two species namely, Smilax perfoliata and S. zeylanica bore two simple tendrils in the axils of leaves.The growth of the bifid tendrils of Cayratia trifolia was typical.The branches of the tendrils of the species arise at different distances.One of the bifid branch terminates, while the other one again becomes bifid.Branching of tendril was similarly repeated up to 4th node (Fig. 3).Each terminating tendril ends into a knob like structure.The lower part of the tendrils of A. leptopus shows distinct node and internodes.The 4 nodes bent alternately on opposite sides to form a zig-zag pattern (Fig. 4A, B).Among twiners, majority of the species (91%) showed twining in righthanded direction along the support (Fig. 5A).Only in five species, namely Dioscorea bulbifera, D. echinata, D. pentaphylla, Merremia dissecta and Mikania micrantha left-handed twining was observed (Fig. 5B, Supplementary Table 3).

Commonness vs. rarity
The number and share of exclusive climber species as well as those common to grassland, wasteland and forest vegetation types has been presented in Venn diagram (Fig. 6).Twelve (12) species were exclusive to wasteland and 26 to forest vegetation.Only 4 species, namely Ipomoea aquatica, Lathyrus aphaca, L. odoratus and L. sativus were exclusive to grassland vegetation.Quite a greater number of species of climbers was common to wasteland and forest vegetation.All the three vegetation types A few rare climbers occurred in only one vegetation type but some other rare ones occurred in more than one type.The rare exclusive species were Acacia concinna, Ampelocissus  The result indicates clear differences in the occurrence and diversity of climbers among different vegetation.The wasteland and forest vegetation were nearly similar in the composition of climbing species.Lianas were distributed in all the three vegetation but most diverse in forest vegetation.This may probably due to the greater support diameter.In absence of support, the pliable stems of the liana grow only up to the 1.5 meter in height (Putz, 1984).Lianas have to climb on trees, if not, and then they continue to grow very slowly in the low light of the understory (Putz, 1984).The anchoring strategies and stem anatomical features favours their growth over upright trees (Garrido-Perez and Burnham, 2010).Convolvulaceae was the most specious family of climbing plants as also reported from the southern Western Ghats of Coimbatore (Sarvalingan and Rajendran, 2015).Twining was the most prominent mode of climbing that has also been cited for other (DeWalt et al., 2000;Parthasarathy et al., 2004).

Stratification and thicket
Due to greater proportion of weak stems of twining, tendrilar and straggling-unarmed climbers lower strata shows maximum number of species.The species reaching to middle and upper strata were mostly lianas.In the absence of suitable support they grow with lower strata (Putz, 1984).The supports on which climbers ascend were not species-specific.They are the highest peak where a species of climber reached.Several studies demonstrated earlier that the lianas and trees are not in species-specific relation (Perez-Salicarp et al., 2001;Malizia and Garau, 2006).Tinospora sinensis is the most frequent climbing plant of all the three vegetation types and also provides support for various herbaceous climbers like  Climbers also have various resource value of ecological and economic importance (Tra Bi et al., 2005;Khare, 2007;Parthasarathy et al., 2015).The straggling-armed climbers e.g., Caesalpinia bonduc, C. cucculata, C. decapetala, Calamus tenuis, Capparis zeylanica, Rosa clinophylla and Ziziphus oenoplia form dense thickets.These lower strata thickets create suitable micro-habitat for rare plant taxa like Baccopa monierii, Gloriosa superba, Helminthostachys zeylanica, Pergularia foetida, Oxystelma secamone, Rauwolfia serpentina and many other shade tolerant species as also reported by Pandey and Shukla (2003).Gonzalez-Teuber and Gianoli (2008) reported greater reproductive output in Convolvulus chilensis that were associated with thorny shrubs.These thickets are also safe house for rodents and other small mammals which provide dispersal of the plant propagules during migration from one thicket to the others.Thus, thickets provide conservation of these special micro-habitats for conservation of small species.

Circumnutation pattern
Several authors mentioned that twining handedness can be constant within a species but differ between species (Sachs, 1882;Ornduff, 1991;Hashimoto, 2002;Lubkin, 2004).However, Davis (1974) observed both the left-handed and right-handed twining stem in Mikania micrantha at different latitudes.The current results confirm the verified principle that most of the twining plants ascend their host by forming righthanded helices.We observed 93% right-handed twining.Edwards et al. (2007) reported 92.5% of the twining stem in the same direction.Though, their data on twining direction is not based at species level.Burnham and Revilla-Minaya (2011) reported 83% taxa at species level that were dextral (right handed) in direction.Our results further indicate a general pattern of twining direction irrespective of the three vegetations and similar pattern was also claimed by Edwards et al. (2007) at wide range of vegetation types and geographical location across the globe.Burnham and Revilla-Minaya (2011) reported ambidextrous twining phenomenon in members of the family Dilleniaceae.They observed stem circumnutation in one direction, and after 2-3 revolutions they further noticed the changes in direction for 2-3 revolutions in the same individuals.Darwin (1875), Dufor (1902), Ornduff (2004) also reported this reversal in handedness in several species.In the present study no such reversal was observed.The species of genus Dioscorea showed both the left-handed and right-handed direction.Baillaud (1962) also reported that the species of this genus twin either right-handed or left-handed direction.
Among tendrilar climbers, 56% had simple un-branched tendril.The branched tendrilar climbers were either bifid or trifid.The branches may provide greater probability to find support and also may give greater chance to attach on the support under disturbed environment.This may probably makes the plant very flexible to their attachment under strain.Both the left-handed and right-handed circumnutations were observed in every tendril of a species.The two directions of handedness were separated by tendril perversion in successive manner.Tendril perversion is the change in the helix structure to hemi-helix structure (Liu et al., 2014).This helical coiling axially shortens the tendril, pulling the plants towards the attachment point (Gerbode et al., 2012).Tendril perversion provides quite greater flexibility than a regular coiled tendril in a plant (Aziz et al., 2016).The alternate turns of mature tendrils of Antigonon leptopus provides additional flexibility.During external pull on plants these alternate turns become relaxed and thus conquer its detachment from the support.
Common, exclusive and rare climbers It has been observed that the exclusive climber diversity increases as the complexity of the vegetation changes from grassland to wasteland, to forest.The species occurring in all the three vegetation types are also very common in the region, except Oxystelma secamone.Some species like Antigonon leptopus, Bauhinia vahlii are abundant and frequent climbers of wasteland and forest vegetation types, respectively.The wasteland and forest share most of the climbing species (35%) and their diversity was also quite similar.Wasteland represented suitable habitat for both the vines and lianas.This was probably due to the greater protection of their propagules and availability of support in this vegetation type.
Grassland vegetation, represented by 34 climbing species, is the most disturbed vegetation across the landscape.Several species namely, Cajanus scarabaeoides, Cayratia trifolia, Cissampelos pareira, Coccinia grandis, Ichnocarpus frutescens, Ipomoea cairica, Momordica dioica, Operculina turpethum, Teramnus labialis, Trichosanthes cucumerina and Trichosanthes nervifolia have either rhizomatous or tuberous roots or woody rootstock that is helpful in the survival and growth of these climbers in disturbed habitat.Some herbaceous climbers like Lathyrus aphaca, L. odoratus, L. sativa and Vicia hirsuta were also present as common weeds in adjacent agricultural fields.Some rare climbers occurred in one or two vegetation types.A few climbers like Oxystelma secamone, Rhynchosia minima and Spatholobus parviflorus which are quite rare in this region are, however, included in the Least Concern category of Red Data Book (Lansdown 2011;Chadburn 2012;Poveda 2012).Dioscorea deltoidea is categorized as Vulnerable in India (Nayar and Sastry, 1990).
Several climbers of grassland vegetation are known to produce secondary metabolites which repel their herbivores (Subramanayam et al., 2007).These plant species have evolved traits to tolerate or resist disturbance (Diaz et al., 2007Dobarro et al., 2013).A number of climbers are used locally in various ways.The aerial bulbs of D. bulbifera and D. oppositifolia are consumed as food.The leaves of Bauhinia vahlii are used as meal plate by rural poor.The natural ingredient of seeds of Mucuna pruriens (L-DOPA) is valuable in the treatment of Parkinson disease (Dymock and Warden, 1980).In past, jewellers used the seeds of Abrus precatorius (Ratti) as weight measures.An herbaceous climber, Mikania micrantha, on the other hand, is one of the 100 worst invasive alien species in the world (Lowe et al., 2001).It has been reported as a problematic weed in the plantation forests of north-east and south-west India (Parker, 1972).Due to recurrent disturbances and degradation of forest and wastelands, most of the valuable climbers have currently become much scarce.

Conclusions
Local climbing flora provides considerable natural resource to the region.They often create special micro-habitats and increase the complexity of the ecosystem.But in recent past, recurrent disturbances in the form of habitat destruction, grazing, trampling and fire across the landscape have wiped out a number of climbers.The basic information on their diversity, distribution and circumnutation or climbing handedness pattern may be used to emphasize the need of their conservation at regional level.

Fig. 1 .
Fig. 1.Number of vines and lianas within different vegetation types Fig. 2. The occurrence (%) of climbing species as per climbing modes within terrestrial landscape (Abbr.Tw: twining; Td: tendrilar; Str-A: straggling armed; Str-UA: straggling unarmed; AR: aerial root) latifolia, Aristolochia indica, Ipomoea nil, Naravelia zeylanica, Spatholobus parviflorus and Vallaris solanacea.The rare species, occurring in more than one vegetation types were Abrus precatorius, Cardiospermum helicacabum, Clitoria ternatea Dioscorea pentaphylla and Gloriosa superba.DiscussionThe present study aims to examine the composition and diversity of climbers among three vegetation types with respect to their woodiness, climbing mode and circumnutation pattern.Such studies with respect to Terai landscape are still lacking.Considerable investigations have been made on the diversity of lianas of forest vegetation in India(Reddy and Parthasarathy, 2003;Parthasarathy et al., 2004;Jayakumar and Nair, 2013), Recently,Aziz et al. (2016), observed the growth pattern of tendril in Lagenaria sicereria.The vines need attention especially with respect to their climbing pattern along the support.

Fig. 4 .
Fig. 4. The zig-zag pattern of tendrils in Antigonon leptopusEach tendril has four nodes.A. The twig with tendril (the young upper tendrils are without any turn).The lower mature tendril has alternate turns(1)(2)(3)(4).B. The developmental stages of turns (I-IV) in maturing tendril.The abbreviations LH, TP and RH stand same as in figure5

Fig. 5 .
Fig. 5.The two species show their direction of twining. A. Dioscorea bulbifera stem twining in the left-hand direction and B. Basella alba stem in the right-hand direction

Table 1 .
The number of species, genera and families of climbers and their ratio across the terrestrial landscape of north-eastern Uttar Pradesh