Climbing strategies of Taiwan climbers

Background The climbing strategies of lianas and herbaceous vines influence climber competition abilities and survival. The aim of this study was to investigate the climbing strategies of each plant species and observe their organs of origin. Results The results showed that all Taiwan climbers were approximately 555 species, accounting for 11% of the native flora. Among the 555 climbers, the twining stem type was the most common, with a total of 255 species (46%), the remaining climbing methods accounted for 300 species. Approximately twenty one climbing methods, including nine combination types, were exhibited, of which the most common type was the twining stem, followed by simple scrambling and twining tendrils. Most species of Fabaceae and Apocynaceae were twining stems in dextrorse, excluding Wisteriopsis reticulata and Alyxia taiwanensis, which were in sinistrorse. The prehensile branch of Fissistigma genus, Ventilago genus, and Dalbergia benthamii, originated from second-order or modified stems. In the simple scrambling type, some climbers were covered spines and prickles to attach the host, and the others were clinging to the supports or creeping on the ground without speculation. The hooks or grapnels of the genus Uncaria are derived from the branches, and a pair of curved hooks or a spine of Artabotrys hexapetalus are originated from the inflorescence to tightly attach to a host. The Piper genus use adhesive roots to climb their hosts. Among the genus Trichosanthes, only Trichosanthes homophylla exhibits a combination of twining modified shoots and adhesive roots. Gentianales includes four families with seven climbing mechanisms, while Fabales includes only Fabaceae, which presents six climbing methods. Conclusions The twining tendrils had nine organs of origin in Taiwan climber, that these opinions of originated organs might be available to the studies of convergent evolution. The data presented herein provide crucial basic information of the climber habits types and origin structures, which are available for terms standardization to improve field investigation. The terminologies would aid in the establishment of climber habits as commonly taxon-specific and the combination of two climber habits could be a characteristic of taxonomic value. Supplementary Information The online version contains supplementary material available at 10.1186/s40529-023-00399-4.


Background
Climbing plants germinate on the ground and develop for a certain period; their stems need external support to sustain themselves mechanically.Climbing plants or climbers were used to describe plants displaying climbing habits, and lianas and vines were used to describe woody and herbaceous climbers, respectively (Sperotto et al. 2020).After establishing themselves on hosts, some climbers still connect to the ground, while others begin to lose their function from the tip of the stem and lose their connection to the ground (Moffett 2000).The latter ultimately loses contact with the soil and becomes epiphytic, which is named the nomadic vine, nomadic climber, or secondary hemiepiphytes (Moffett 2000).
Climbing plants use different climbing strategies to develop and establish their abundance and survival.The stems of climbers have a twining function, which is the most crucial climbing method for climbing plants ( Muthuramkumar and Parthasarathy 2000).Twining stems are divided into two subtypes: dextrorse, which is a left-toright spiral when viewed from the front, and sinistrorse, which is a right-to-left spiral when viewed from the front (Edwards et al. 2007;Beentje 2010;Burnham and Revilla-Minaya 2011;Wang et al. 2013).Twining tendrils are terminal, haptotropic, thread-like structures that are used exclusively for climbing (Darwin 1865;Sousa-Baena et al. 2018).Darwin (1865) proposed that tendrils are filamentous structures that wrap around other objects via helical growth.Therefore, a special structure with a filamentous shape is generally referred to as twining tendrils, and the tendrils of the family Cucurbitaceae developed in the leaf axils are theorized to represent modified flowers (Darwin 1865), leaves (Sensarma 1955), and shoots or secondorder branches (Sensarma 1955;Gerrath et al. 2008).
The thorns or other spines covering the climbers serve a defensive function in addition to helping the hosts climb.For example, the Mimosa genus (Fabaceae) includes several thorny species, not only for climbing but also for protection against predators (Barneby 1991).In shaded regions or the understory of forests, younger plants increase thorn production in Artabotrys hexapetalus to avoid being bitten and increase their climbing abilities (Fisher et al. 2002).
Adventitious roots are a climbing type that can adsorb onto trees and rock walls.The adhesive roots of climbers secrete polysaccharides and proteins from the root hairs on the adventitious roots, and the adventitious roots and root hairs attach to produce an adhesive pad that can be adsorbed on any substrate (Groot et al. 2003).Areas with shorter dry seasons and higher average annual precipitation have more adhesive root species (Durigon et al. 2013).
Taiwan is located in the subtropical monsoon region.The climate is warm and humid throughout the year, with temperatures of approximately 22-24 °C and annual average precipitation of approximately 2000-2500 mm.Owing to their favorable environment, diverse and abundant species are present, including climbing plants, with approximately 52 families and 287 liana species distributed in Taiwan (Yang et al. 2022).The climbing strategies of climbers in central and southern Taiwan have been previously investigated (Chen et al. 2013).In this study, we continued to study the climbing methods of all Taiwan climbers.We hope that diverse climbing modes will become taxonomic features that contribute to plant classification and will ultimately be integrated into conservation research on global climbing plant diversity.

Materials and methods
In this study, we concentrate solely on flowering plants of Taiwan climbers, although some plants of ferns and lycophytes, Orchidaceae, and Poaceae, conform the definition of lianas.The categorized families table will be arranged according to the APG IV system (Stevens 2001).The climbing strategies we used were based on Sperotto et al. (2020) and were divided into active and passive climbing types.Active climbing types were divided into the following: (1) Twining stem, where the climber stem has a twining function and has two groups: dextrorse and sinistrorse.(2) Twining tendrils, where the tendril is defined as branches, leaves, stipules, and inflorescences specializing in tendril twining around support without stem twining, thin, short, wrapping, or grasping structures with hooks or adhesive pads at the ends.(3) Twining leaf petioles, where petioles were twined around the support.(4) Prehensile branch, where the lateral leaf-bearing branches have a twining function.This is different from using stems, such as tendrils, which function and twine around the support; they do not possess any type of structural modification but originate from shoot-modified or second-order branches.(5) Twining peduncles or inflorescences, where the peduncles or inflorescences are modified to twine with the host.
The passive climbing types were classified as (1) simple scrambling, whereas climbers may or may not have spines, prickles, and thorns to support, and without hooks or grapnels.(2) Hooks or grapnels that plants bear hooks or grapnels to scramble the host; these are specialized structures.(3) Adhesive roots, where the adventitious roots of climbers can be adsorbed onto trees and rock walls.
The origins of the tendrils were divided into two categories with 17 types, as described by Sousa-Baena et al. (2018).The first tendril category originates from ten types of vegetative organs, and the second tendril category originated from seven types of reproductive organs.The first category includes the following: (1) modified terminal leaflets; (2) prolonged midrib; (3) prolonged forked tips of the midribs; (4) modified petioles and a transitory structure that develops other functions, except climbing, in later developmental stages of leaves; (5) modified leaf tip; (6) whole leaf modified into a simple tendril; (7) petiole duplication; (8) modified petioles that develops twining capacity; (9) modified compound leaf rachis that acquires the capacity for helical growth, becoming voluble; and (10) a modified shoot.The second category includes (1) tip of the reduced inflorescence apex; (2) modified whole inflorescences; (3) modified inflorescence apices; (4) modified inflorescence rachis that acquires the capacity for helical growth, becoming voluble; (5) inflorescence lateral branches; (6) inflorescence peduncles; and (7) flower pedicels that acquire the capacity for helical growth.

Results and discussion
Among the 555 Taiwan climbers (Table 1, Additional file 1: Appendix S1), the twining stem type was the most common, with a total of 255 species (46%), including 217 species that were dextrorse and 38 species that were sinistrorse.The remaining climbing methods accounted for 300 species (54%), including 104 species of simple scrambling, 59 species of twining tendrils (33 species of twining modified shoot, 15 species of twining petiole duplication, 10 species of twining terminal leaflets, and 1 species of twining leaf tip), 36 species of adhesive roots, 36 species of twining peduncles or inflorescence, 23 species of twining petioles, seven species of prehensile branch, five species of hooks or grapnels scrambling.The 30 climbers used a combination of two or three climbing mechanisms and a total of ten combination types.Approximately 19 species belonged to the simple scrambling type but were without spines, prickles, or thorns.Most families had only one climbing method; among them, Fabaceae (85 spp.) had the highest number of climbing methods (six).Rubiaceae had five climbing methods but only eighteen species.We then described each climbing mechanism in Taiwan climbers by active and passive climbing types and observed tendril-origin vegetative and reproductive organs.
In the Fabaceae family, 68 species had twining stems in dextrorse, and only one species, Wisteriopsis reticulata, is in sinistrorse (Fig. 1A).The leaf morphologies of Derris laxiflora (Fig. 1B) and W. reticulata were similar and difficult to distinguish, and the climber mechanisms of dextrorse and sinistrorse were available for the identification of these two species.These two mechanisms are also the basis for distinguishing Wisteria sinensis from Wisteria floribunda; the former is dextrorse, and the latter is sinistrorse (Wang et al. 2013).Similarly, 35 species in Apocynaceae are twining stems in dextrorse; only Alyxia taiwanensis is twining stems in sinistrorse; indeed, this sinistrorse type is a diagnostic feature of this species.

Petiole duplication
A pair of tendrils of the Taiwan Smilax species (Fig. 1E) originating from petiole duplication is consistent with previous reports.

Modified shoots and adhesive roots
The tendrils of Thladiantha genus were complexes produced by shoots and stipules, and two genera, Neoalsomitra and Trichosanthes, had a combination of modified shoots and adhesive roots (Table 2); however, these characteristics must still be investigated.

Twining peduncles or inflorescence
There are four tendril modes originating from reproductive organs in this study (Table 2).Antigonon leptopus (Polygonaceae) had twining tendrils of the inflorescence apex, and its tendrils originated from a modified inflorescence apex and formed two to three tendrils (Fig. 2B).Cardiospermum halicacabum (Sapindaceae) had a twining tendril of the modified inflorescence rachis that formed a pair of tendrils at the rachis base (Fig. 2C).The peduncles of Passiflora genus (Passifloraceae) were often degenerated or absent, the central axis developed into a tendril, and the secondary axes were reduced to one to two flowers (Wu et al. 1994(Wu et al. -2004)).The twining tendrils of the eight Taiwanese Passiflora species originated from the tip of the reduced inflorescence apex.In the Vitaceae family, the inflorescence rachis of Ampelopsis, Nekemias cantoniensis (Fig. 2D), and Vitis genus had the helical growth capacity to climb hosts and were named modified inflorescence tendrils.The genera Cissus, Tetrastigma, and Parthenocissus tricuspidata modified the inflorescent tendrils combined with adhesive pads (Sousa-Baena et al. 2018).In this study, we did not find any Cissus genus with this combination type; therefore, this needs to be investigated.

Prehensile branch
Prehensile branches were found in Annonaceae, Connaraceae, Fabaceae, and Rhamnaceae.The lateral leaf-bearing branches had a twining function different from that of using the stem; this climbing mechanism was named the prehensile branch or twining lateral branch.In this study, approximately seven species (Table 1) had a prehensile branch, including Fissistigma glaucescens, F. oldhamii (Annonaceae) (Fig. 2E), Connarus subinaequifolius (Connaraceae), Rourea minor (Connaraceae), Dalbergia benthamii (Fabaceae), and Ventilago elegans, V. leiocarpa (Rhamnaceae) (Fig. 2F).The species C. subinaequifolius was only distributed in Lanyu, and few individuals were found, which influenced the observation of the climbing method.According to Sperotto et al. ( 2020), we classified it as a twining lateral branch (prehensile branch).
Plants with adhesive roots can be firmly adsorbed onto the host because adhesive roots with root hairs will produce adhesive pads and can adsorb onto any substrate.For example, the adhesive roots of Hedera helix emit yellowish mucilage that is primarily composed of nanoparticles of arabinogalactan proteins and is high-strength adhesives (Huang et al. 2006).Therefore, the adhesive root groups can be firmly adsorbed onto the host using these mucilages.
Adhesive roots can climb trees of any diameter (Hegarty and Caballe 1991), and later successional forests composed of larger-diameter trees have more adhesive root species (Yang et al. 2018).Plants with twining stems generally prefer small-diameter trees, whereas those with adhesive roots prefer trees with larger diameters, which should also be further investigated.

Hooks or grapnels
In this study, two Calamus (Arecaceae) and three Uncaria species (Rubiaceae) exhibited hooks or grapnels to scramble supports.Sperotto et al. (2020) proposed that the hooks or grapnels of these two genera are  (Robbrecht 1988); and (c) modified branches into curved hooks (Sperotto et al. 2020).In the present study, the three Uncaria species (Fig. 3E) generally had paired, stiff, regular, and short spiral hooks derived from branches.The young plagiotropic branch of A. hexapetalus had two inflorescence hooks (Fig. 3F), each with one flower, and an older plagiotropic branch with two inflorescence hooks (Posluszny and Fisher 2000).Therefore, the spiny of A. hexapetalus generally had paired curved hooks derived from the inflorescence.

Combination of two or three climber mechanisms
In Taiwan, 30 climbers exhibited a combination of two or three climbing methods.Reddy and Parthasarathy 2003;Senbeta et al. 2005).Among these species, Artabotrys hexapetalus had two climbing mechanisms, hooks/grapnels and simple scrambling.Most Taiwanese Vitaceae species have tendrils; among them, three species, Parthenocissus tricuspidata, Tetrastigma obtectum var.glabrum, and Tetrastigma obtectum var.obtectum also have adhesive roots.The remaining three Tetrastigma species within these genera are still under investigation.Among the seven Trichosanthes species in Taiwan, we determined that Trichosanthes homophylla exhibited a combination of modified stems (Fig. 3I) and adhesive roots.The remaining species must be observed in the near future.
Four reproductive and five vegetative organs of tendrils were identified (Table 2).Some vegetative organs, for example, prolonged midrib, prolonged forked tips of midribs, modified petioles, whole leaf modified into a simple tendril, and modified compound leaf rachis; or some reproductive organs: inflorescence lateral branches, inflorescence peduncles, and flower pedicels, were not found in this study.The information collected in the present study will provide fundamental evidence for further studies on climber development and survival mechanisms.

Conclusion
In this study, we explored the climbing strategies of Taiwanese climbers and examined their organs of origin.The results revealed approximately 21 climbing methods, including a combination of two or three climbing methods.Approximately 46% of all climbers twined their stems, followed by simple scrambling and twining of tendrils.Most families used only one climbing method; however, Fabaceae had the highest number of climbing types (six), followed by Rubiaceae (five).Apocynaceae and Fabaceae plants had twining stems in dextrorse, and only Alyxia taiwanensis and Wisteriopsis reticulata were sinistrorse, showing that the twining stem type was good evidence for species identification.The prehensile branch of the Fissistigma genus, Ventilago genus, Connarus subinaequifolius, Rourea minor, and Dalbergia benthamii are derived from second-order or modified stems.Some modified tendrils in Cucurbitaceae, such as the modified stems-stipule complex of Thladiantha genus and modified stems with adhesive pads of the genera Neoalsomitra and Trichosanthes, were required for observation.Climbing methods for the genus Tetrastigma in Taiwan include a combination of inflorescence tendrils with adhesive roots, such as T. obtectum var.glabrum and T. obtectum var.obtectum.Whether the other three species have these characteristics should be investigated in future studies.Artabotrys hexapetalus has hooks or grapnels in younger stems and simple scrambling in older stems.This research on the climbing methods of Taiwan climbers will aid in establishing Taiwan climbers as common taxon-specific or planting configuration data.This information is crucial for future climber research to ensure the conservation of biodiversity.

Table 2
Organs of origin of tendrils in Taiwan climbers

Table 3
(Liao 2000)s of E. trifoliatus, H. surattensis, and S. caesia were either curved or recurved.In the family Smilacaceae, Smilax arisanensis, S. bracteata var.bracteata, S. bracteata var.verruculosa, S. china, S. elongato-umbellata, S. horridiramula, S. ocreata, and S. sieboldii had prickles covering the stem, and in the family Dioscoreaceae, Dioscorea collettii, D. cumingii, D. esculenta var.spinosa, and D. matsudae had prickles at their petiole base(Liao 2000).The simple scrambling combined with twining petiole duplication tendrils in Smilaceae and twining stems in Dioscoreaceae have become the basic diagnostic characteristics that aid twining around the host.The indumentum of the Rubia Organs of origin of spiculates in Taiwan climbers

Table 4
Climbers classified as simple scrambling without spiculates

Table 5
List of orders and families of Taiwan climbers that possess climbing strategies