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Liana species composition differs, in spite of trait similarities, in two adjacent forest types in Central Brazil.

Tropical climates support climbing floras with high species richness, morphological diversity, and phylogenetic diversity. Climber species play essential roles in tropical plant communities, contributing with significant richness to tropical forests (Hergarty & Caballe, 1991; Engel, Fonseca, & Oliveira, 1998), and occurring in both evergreen and seasonal forests. Collectively, climbers show tolerance to large ranges of latitude, altitude, climate, and soil types (Gentry, 1991). At least 133 plant families include the climbing habit, which evolved independently several times; indeed almost 40 % of vascular plant families in Brazil include climbers (Schenck, 1892; Richards, 1952; Gentry, 1991; Araujo & Alves, 2010). Climbers vary from absent or scarce in grasslands, to dominant in "Mata de Cipo" (liana forest), a type of ombrophilous forest in the Southern Amazon basin (Engel et al., 1998; IBGE, 2012). In Central Brazil, climbers are diverse and widely distributed in Cerrado (or Savanna) vegetation (Filgueiras, 2002) and in other seasonal forests (Hora & Soares, 2002; Rezende & Ranga, 2005).

While climbing species may tolerate different soil and climatic conditions, local biotic and abiotic factors may determine the presence and abundance of individual species. These factors include host plant availability, canopy density, and temperature and rainfall seasonality (Putz, 1984; Gentry, 1991). Similarly, morphological variation in life form, climbing mechanism, and dispersal syndrome may be associated with climber distribution: for example herbaceous species are more prevalent in open vegetation while woody species are more common in mature forest. The apical twining mechanism for ascent is the most common mechanism in most studied habitats, and because it is effective on host plants of small diameter, many species are apical twiners where richness is high (Putz & Holbrook, 1991). Wind dispersal (anemochory) is often cited as the most common dispersal strategy for climbers, and increases relative to animal dispersal, especially in dry forests (Gentry, 1991).

Close floristic relationships have been proposed for Cerrado vegetation and fragments of seasonal forest that resulted from climatic and edaphic changes at the end of the Quaternary (Pinheiro & Monteiro, 2010). Cerrado encompasses several vegetation sub-types (Ribeiro & Walter, 1998), ranging from forest (riparian forest and cerradao) to savannas (cerrado sensu stricto, savannah park, palmeiral, vereda), to countryside (disturbed fields, rocky fields, grasslands). Seasonal forests may link savanna to other vegetation types and promote species compositional similarities (OliveiraFilho & Ratter, 2002; Pinheiro & Monteiro, 2010). Seasonal forests are distinct from cerradao in growing on deeper and more fertile soils (Oliveira-Filho & Ratter, 2002; Salis et al., 2004).

This distinction between seasonal forest and cerradao is seen in central Brazil in the Serra de Maracaju, a series of escarpments on the basalt plateau in the Parana basin. The vegetation contact extends from South-Central Brazil to Uruguay, and from Mato Grosso do Sul to the adjacent states of Goias and Mato Grosso (Martins, 2003). The Southern part of the mountain range is rugged with steep hills, harboring several phytophysiognomies of varying floristic composition, which may allow interconnections between seasonal forests and other vegetation types. Previous research in the region (Ramos & Sartori, 2013; Assuncao, Casagrande, & Sartori, 2014) did not include climbing species. High rates of deforestation in the mountain range contribute to a lack of information on the flora and its biogeographical affinities. Knowledge of the species that are restricted to specific environmental conditions (e.g., hills with rocky outcrops or valleys with deeper soils) would provide a better picture of the regional conservation value, the included phytophysiognomies, and their species diversity.

For this study, we predicted that the climber composition in two phytophysiognomies of the Serra de Maracaju would be different, based on differences in the structure of the host vegetation that provides support for climbing plants. This prediction derives from climbing plant data from other fragmented forests, such as seasonal and riparian forests (Rezende & Ranga, 2005; Santos, Kinoshita, & Rezende, 2009; Vargas, Araujo, Schiavini, Rosa, & Hattori, 2013). We aimed to answer these questions: (1) What is the species richness and floristic composition of climbing plants in cerradao versus seasonal deciduous forest?, (2) What degree of floristic compositional difference exists between the two vegetation types?, and (3) Do the two phytophysiognomies differ significantly in climbing mechanisms, life forms, and dispersal syndromes of climbers?

MATERIAL AND METHODS

Study area: Located in the Parana basin plateau, the Serra de Maracaju divides the state of Mato Grosso do Sul between the drainages of the Paraguay River to the West, and the Parana River to the East (Martins, 2003). The Furnas do Dionisio is vegetated by Cerrado, with interspersed fragments of seasonal forest (RADAMBRASIL, 1982; IBGE, 2012). The Seasonal Deciduous Forest (SDF) consists of dense, 12 to 15 m trees forming a closed canopy whose understory includes abundant shrubs and climbers, with grasses and subshrubs on rocky outcrops. The cerradao (a subset of Cerrado) is composed of sparse to dense, twisted trees (up to 4 m tall), with an understory predominantly composed of shrubs, sub-shrubs, and grasses in which climbers are less commonly encountered. The climate of the region is an "Aw" type (Koeppen, 1948), with both rainy (October to March) and dry seasons (April to September). The average annual temperature is 23[degrees]C, average annual rainfall is 1 500 mm (MMA, 2007), and mean altitude is 500 m.a.s.l. SDF and cerradao are found on hillsides of the Serra (20[degrees]05'00"-20[degrees]30'00" S and 54[degrees]45'00"-54[degrees]15'00"W).

We delimited eight 25 x 50 m plots on the slopes of the Serra de Maracaju, over an area of 34 ha, with four plots in each of the two forest types (SDF and cerradao), for a total sample area of 1 ha. Plots in forest fragments were selected randomly in each phyto-physiognomy, therefore spacing between plots was not equal. Plots 1-4 were in seasonal deciduous forest and 5-8 were in cerradao. All plants rooted in the soil and supported by another plant were considered climbers (Gentry, 1991). All plants were collected in fertile condition to enable species identification, with collections made monthly from December 2009 to November 2011 (24 months). A plant species was collected from each plot where it occurred. Climbing stems of all diameters were considered so as to include both herbaceous and woody life forms. The family level classification followed the system of APG III (2009), and species determinations were made using taxonomic literature and advice of family and generic-level specialists. Identified materials were deposited at CGMS herbarium, Federal University of Mato Grosso do Sul, Brazil (UFMS).

Species characterization and statistical analysis: We used the four-part climbing mechanism classification of Hergarty and Caballe (1991): 1) Apical twining: apically winding stems that continuously wrap around the host; 2) Tendrilling: bearing tendrils, a determinate coiling organ derived from leaflets, stipules, petioles, axillary buds, or inflorescence axes; 3) Scandent: bearing hooked spines or thorns only; or 4) Radicant: bearing roots adapted to adhere to the host. Life form was classified following Gentry (1991), with herbaceous climbers bearing thin, flexible stems, versus woody climbers bearing thick, relatively rigid stems. Diaspores were classified according to Van der Pijl (1982) as anemochorous (winged or plumed diaspores), zoochorous (scattered by animals), or autochorous (dispersed by explosion or gravity).

Non-Metric Multidimensional Scaling (NMDS) based on the Jaccard Similarity Index was used to test community similarity of species presence and absence for each plot sampled. A non-parametric analysis of similarity (ANOSIM, Clarke, 1993) with 10 000 permutations was employed to test for significant differences among groupings. Analysis of the differences between the proportions of climbing mechanisms, life forms, and dispersal syndromes were performed using chi-square tests (Zar, 1984).

RESULTS

Richness and floristic composition: Neither species richness nor floristic composition of climbing plants was similar between cerradao and Seasonal Deciduous Forest (SDF) (Fig. 1; NMDS: [R.sup.2]= 0.35, stress= 0.3. ANOSIM: [R.sup.2]= 0.48, p= 0.03). Fifty-five species, belonging to 26 genera and 14 families were found among the eight 25 x 50 m plots sampled. Only 13 species were shared between both vegetation types. The most speciose families were Dioscoreaceae (ten species), followed by Fabaceae (eight), Malpighiaceae (eight), Sapindaceae (seven) and Convolvulaceae (six). In cerradao alone, 31 species (20 genera, 12 families) were found; the most speciose families were Sapindaceae and Fabaceae (five species each), followed by Dioscoreaceae and Malpighiaceae (four each). In SDF, 37 species (19 genera, 12 families) were found; Dioscoreaceae was the most diverse family (six species), followed by Sapindaceae (five), Malpighiaceae and Convolvulaceae (four each). The most species-rich genera overall were Dioscorea (ten species), Ipomoea, Heteropterys, and Serjania (five each); Dioscorea and Serjania were present in both vegetation types, while Heteropterys and Ipomoea were present only in SDF (Table 1).

Individual plots included from 9 to 18 fertile species during the 24 months of collection. SDF plots included 13 to 18 species each, while cerradao had 9 to 14 species per plot. Only one species, Dioscorea sinuata, was found fertile in all four SDF plots, while Serjania caracasana was the only species occurring as a fertile specimen in three cerradao plots. The average number of species occurrences per forest type (fertile specimens) was only 1.07 for SDF and 0.84 for cerradao. Because our survey included only fertile specimens, the total number of species that are shared between the forest types is not known.

Morphological characters: The most commonly encountered individual traits for climber species in the study area were herbaceous habit, apically twining climbing mechanism, and anemochorous dispersal (Fig. 2). This combination of traits was present in 11 species across the two vegetation types. However, the most common combination of character states among all species was herbaceous habit, apical twining, and autochorous dispersal (14 species). No significant difference was found among the distribution of character states from cerradao versus SDF (life form: [x.sup.2]= 1.195, p= 0.32; climbing mechanism: [x.sup.2]= 1.016, p= 0.60; dispersal syndrome: [x.sup.2]= 3.362, p= 0.19).

Life form: Our census included a total of 32 (58.2 %) herbaceous and 23 (41.8 %) woody climbing species. In cerradao, 20 species (64.5 %) were herbaceous and 11 (35.5 %) were woody. In SDF, 19 species (51.4 %) were herbaceous and 18 (48.6 %) were woody (Table 2, Fig. 2).

Climbing mechanism: We found 35 (63.6 %) apically twining species, 15 (27.3 %) tendrilling species, and five (9.1 %) scandent species; no radicant species were found. In cerradao 17 (54.8 %) were apically twining, 11 (35.5 %) were tendrilling, and three (9.7 %) were scandent, while SDF included 24 (64.9 %) apically twining species, nine (24.3 %) tendrilling, and four (10.8 %) scandent (Table 2, Fig. 2).

Dispersal syndromes: Anemochory occurred in 32 (58.2 %) species overall, followed by autochory in 17 species (30.9 %), and zoochory in six species (10.9 %). In cerradao alone, anemochory occurred in 15 species (48.4 %), autochory in ten (32.3 %), and zoochory in six (19.3 %). The SDF included 23 (62.2 %) anemochorous species, 12 (32.4 %) autochorous, and two (5.4 %) zoochorous (Table 2, Fig. 2).

DISCUSSION

In cerradao and Seasonal Deciduous Forest of the Serra de Maracaju, the most species rich climber family was Dioscoreaceae, followed by Sapindaceae, Fabaceae, and Malpighiaceae. The latter three families are recognized as significant climber-rich families of the neotropics

(Gentry, 1991) and dominants of seasonal forests (Hora & Soares, 2002; Udulutsch, Assis, & Picchi, 2004; Alcala, Franceschi, & Stranghetti, 2006). Fabaceae was especially species-rich in Cerrado of central Brazil (Mendonga et al., 1998; Rezende & Ranga, 2005). In Serra de Maracaju, Fabaceae included six of 37 genera, and eight of 55 species of climbers, while Serjania (Sapindaceae), Heteropterys (Malpighiaceae), and Ipomoea (Convolvulaceae) were represented by five or six species each. This pattern is common in climber floras: a few genera include a large proportion of the species (Gentry, 1991). Dioscorea, with ten species, placed Dioscoreaceae as the richest family of the two vegetation types. This represents the first record of high species richness in Dioscoreaceae among climber floras in Brazil. Dioscorea includes over 325 species worldwide with highest diversity in seasonally wet forests (Gentry, 1991; Caddick, Wilkin, Rudal, Hedderson, & Chase, 2002). Our high diversity of Dioscoreaceae, in comparison to other floras, may be due to include all flowering climber individuals, not just those exceeding the diameter of 1 cm.

The two forest types differed by 70 % in their climbing species, demonstrating floristic heterogeneity in the Serra de Maracaju. This pattern was noted for tree and shrub species of the area (Assuncao et al., 2014). The shared climbing species (30 %) suggest that forest fragments of the broad Cerrado phytophysiognomy may function as corridors for generalist species (Pereira, Venturoli, & Carvalho, 2011), in our case Smilax fluminensis, Manettia cordifolia, Mascagnia cordifolia, and Urvillea laevis, which are found in several vegetation types of Central Brazil (Udulutsch et al., 2004; Santos et al., 2009; Vargas et al., 2013). Cerrado in Brazil is often represented by small, natural or semi-natural fragments, which may serve as corridors that promote gene flow (Scariot & Seville, 2005; Silva-Pereira, Venturoli, & Carvalho, 2011).

Cerradao and Seasonal Deciduous Forest plots in our study included more herbaceous than woody climbing species, differing from most tropical forests previously reported (Udulutsch et al., 2004; Romaniuc-Neto, Godoi, Villagra, Almeida-Scabbia, & Melo, 2012; Vargas et al., 2013). Families represented by numerous herbaceous climbers were Fabaceae, Dioscoreaceae, and Convolvulaceae, whereas families including woody species such as Bignoniaceae, Passifloraceae, and Vitaceae (Gentry, 1991) were less rich. Even within families otherwise known for woody species (e.g., Passifloraceae, Convolvulaceae), the species at the Serra de Maracaju were mostly herbaceous. Compared to SDF, cerradao has widely-spaced trees and shrubs, and an abundant herbaceous understory, consistent with high light availability (Gentry, 1991; Engel et al., 1998). In both cerradao and SDF, the trees and shrubs were small to medium sized and easily climbed by herbaceous species, compared to tall rainforest hosts, where woody climbers predominate (Balfour & Bond, 1993; Burnham, 2004; Homeier, Englert, Leuchner, Weigelt, & Unger, 2010). While abundant herbaceous climber species were noted in our study, they are rarely censured in other forests, thus our results await comparisons with other species-level censuses of stems of all sizes.

Apically twining species are dominant in other climber communities over species with alternative mechanisms, suggesting that it is an easier evolutionary route to climbing, it is more common among all climbing species, or it is a more efficient mechanism for climbing. Apical twining is the most common climbing mechanism in vegetation types from evergreen to dry forest (Gentry, 1991), and in Brazil it is prevalent in cerradao, seasonal forest, and riparian forests (Santos et al., 2009; Vargas et al., 2013). Apically twining climbers do not require specialized structures to climb successfully and have evolved in several families (Hergarty & Caballe, 1991), including those with the largest number of species here: Dioscoreaceae, Fabaceae, Malpighiaceae, and Convolvulaceae. Tendrilling was the second-most prevalent climbing mechanism we found, and in cerradao was almost equivalent in frequency to apical twining. The difference in climbing mechanism observed between the two vegetation types may be a phylogenetic effect of the predominant families for each vegetation type. For example, seven tendrillate species of Bignoniaceae, Passifloraceae, Smilacaceae, and Vitaceae were found in cerradao, whereas only two species from these families were found in SDF. Conversely, the predominantly tendrillate family Sapindaceae included seven species in SDF and only four in cerradao. The Sapindaceae pattern, conformed to expectations, given the larger number of species in SDF.

Anemochory comprised the largest number of climbing species in both vegetation types, paralleling the predominant dispersal mode for climbers in dry forests of other tropical areas (Gentry, 1982; Wikander, 1984; Mantovani & Martins, 1988; Solorzano, Ibarra-Manriquez, & Oyama, 2002). Climber dispersal syndromes were not significantly different between the two forest types; however SDF, with a strongly synchronous leaf fall and higher canopy, did have more anemochory than did cerradao. Gentry (1991) reported a higher proportion of anemochorous climbing plant species than for trees and shrubs, a pattern confirmed here in both forest types (Assuncao et al., 2014). Once climbers reach the canopy, branches of the emergent trees may facilitate dispersal of climbers with aerodynamic seeds or fruits. In addition, synchronous leaf fall and strong winds during periods of decreased precipitation, should allow seed and fruit dehydration, facilitating anemochory (Gentry, 1991; Gallagher, 2015; Schnitzer, Putz, Bongers, & Kroening, 2015). However, phylogenetic history can have an important influence over character traits and may explain why trees differ from climbers in this characteristic. Among climbers of the Serra de Maracaju, just three families included the majority of anemochorous diaspores: Dioscoreaceae (ten species), Malpighiaceae (eight), and Sapindaceae (eight): over 80 % of all anemochorous species observed.

The three most common character states among climber species in the two vegetation types were herbaceous life form, apical twining, and wind dispersal. These three traits are nearly universal in the species-rich Dioscoreaceae. Only two species in that family differ, and these were scored here as woody because of their relatively inflexible stems. These phylogenetically-correlated trait combinations in a flora comprised of just 55 species, can only be the basis for adaptive scenarios if the same traits are more variable in other members of the family that are subject to different environmental circumstances.

Cerradao and Seasonal Deciduous Forest show high species richness in Sapindaceae, Fabaceae, and Malpighiaceae, all recognized as families with high climber diversity elsewhere in the Neotropics. To these three families is added the largely herbaceous Dioscoreaceae, a new addition to botanically dominant climbing families of Brazilian forests. Although the two vegetation types are adjacent, they showed floristic differences, with a large proportion of their respective floras unknown in the other vegetation type. A minority of species may use seasonal forests as corridors between larger biogeographic areas, however more species are restricted to one or the other vegetation type. The morphological characteristics we evaluated probably showed no significant difference for ecological and evolutionary reasons because: 1) the two phytophysiognomies are found in the same climatic conditions, and 2) the small number of dominant families limited the suite of possible characteristics. Variations between the two climber floras in life form may be due to tree canopy height, and in climbing mechanism may be related to support plant girth, and in dispersal mode may be related to foliar deciduousness in host trees.

ACKNOWLEDGMENTS

The first author thanks the Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES) and the third author thanks the Fundacao de Apoio ao Desenvolvimento do Ensino, Ciencia e Tecnologia do Estado de Mato Grosso do Sul (FUNDECT) for granted fellowships, as well as colleagues and friends who assisted field collection. We thank the Pro-Reitoria de Pesquisa e Pos-Graduacao (PROPP), Universidade Federal de Mato Grosso do Sul (UFMS) and the Post-Gradutate Program in Vegetal Biology (UFMS) for logistical support. We thank Vali J. Pott, Arnildo Pott, Maria Ana Farinaccio, Augusto Francener Nogueira Gonzaga, and Diogo Amorim de Araujo for helping with the species identification.

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Zar, J. H. (1984). Bio statistical Analysis (2 Ed.). New Jersey, U. S.: Prentice Hall.

Ana Carolina Souza Brito (1), Alexandre Ferraro (2), Vivian Almeida Assuncao (3), Robyn J. Burnham (4) & Angela Lucia Bagnatori Sartori (5) *

(1.) Department of Plant Biology, Institute of Biology, State University of Campinas, CEP 13083-970, Campinas, SP, Brazil; ana_brito_1987@hotmail.com

(2.) Laboratorio de Anatomia Vegetal, Departamento de Ciencias Biologicas, Escola Superior Agricola "Luiz de Queiroz". Av. Padua Dias, 11, CEP 13418900, Piracicaba, Sao Paulo, Brasil; alxferraro@gmail.com

(3.) Rio de Janeiro Botanical Garden Research Institute (JBRJ), Botanical Sistematics Unity, Rua Pacheco Leao 915 / sala 213, Jardim Botanico, 22460-030, Rio de Janeiro, RJ, Brazil; vivian.bios@gmail.com

(4.) Department of Ecology and Evolutionary Biology, University of Michigan, 1109 Geddes Avenue, Ann Arbor, MI 48109-1079 U.S.A.; rburnham@umich.edu

(5.) Program in Vegetal Biology, Federal University of Mato Grosso do Sul, Caixa Postal 549, 79070-900, Campo Grande, MS, Brazil; albsartori@gmail.com

* Correspondence

Received 06-IX-2016. Corrected 08-V-2017. Accepted 06-VI-2017.

Caption: Fig. 1. Similarity among climber using non-metric multidimensional scaling (NMDS) ordination in plots in cerradao and Seasonal Deciduous Forest in the Serra de Maracaju, Mato Grosso do Sul, Brazil. Plots 1-4: Seasonal Deciduous Forest; plots 5-8: cerradao (number of dimensions k=2).

Caption: Fig. 2. Life form, twining mechanism and dispersal syndrome in cerradao (CE) and Seasonal Deciduous Forest (SDF) in the Serra de Maracaju, Mato Grosso do Sul, Brazil. Life Form: Herbaceous (H), Woody (W); Climbing Mechanism: Apical Twining (AT), Tendrilling (TE), Scandent (SC); Dispersal Syndrome: Anemochory (ANE), Autochory (AUT), Zoochory (ZOO). Seasonal Deciduous Forest (black bars) and cerradao (gray bars).
TABLE 1
Climber species and morphology in two phytophysiognomies in the Serra
de Maracaju, Mato Grosso do Sul state, Brazil

Family                   Climber Species           Phytophysiognomies
                                                            CE

APOCYNACEAE        Mesechites mansoanus (A.DC.)
                   Woodson
                   Tassadia berteroana (Spreng.)            X
                   W.D. Stevens

ASTERACEAE         Dasyphyllum vagans (Gardner)
                   Cabrera

BIGNONIACEAE       Fridericia pubescens (L.)                X
                   L.G. Lohmann

COMBRETACEAE       Combretum rotundifolium Rich.

CONVOLVULACEAE     Ipomoea indivisa (Vell.)                 X
                   Hallier f.
                   Ipomoea ramosissima (Poir.)              X
                   Choisy
                   Ipomoea nil (L.) Roth.
                   Ipomoea cynanchifolia Meisn.
                   Ipomoea cf. rubens Choisy
                   Jacquemontia velutina Choisy             X

DIOSCOREACEAE      Dioscorea cf. sinuata Vell.
                   Dioscorea amaranthoides C.
                   Presl
                   Dioscorea aesculifolia R.
                   Kunth
                   Dioscorea cf. altissima Lam.
                   Dioscorea demourae Uline ex.             X
                   R. Kunth
                   Dioscorea glandulosa                     X
                   (Griseb.) Kunth
                   Dioscorea grandiflora Mart.              X
                   ex Griseb.
                   Dioscorea orthogoneura Uline
                   ex. Hochr.
                   Dioscorea ovata Vell.
                   Dioscorea sincorensis R. Kunth           X

EUPHORBIACEAE      Manihot anomala Pohl
                   Manihot tripartita (Spreng.)             X
                   Mull. Arg.
                   Tragia hieronymi Pax & K.                X
                   Hoffm.

FABACEAE           Camptosema ellipticum (Desv.)            X
(Papilionoideae)   Burkart
                   Centrosema sagittatum                    X
                   (Humb. & Bonpl.

                   ex Willd.) Brandegee
                   Galactia benthamiana Micheli
                   Galactia striata (Jacq.) Urb.            X
                   Leptospron adenanthum
                   (G. Mey.)
                   A. Delgado
                   Rhynchosia edulis Griseb.
                   Ancistrotropis firmula                   X
                   (Mart. Ex Benth.)
                   A. Delgado
                   Ancistrotropis peduncularis              X
                   (Kunth)
                   A. Delgado

MALPIGHIACEAE      Banisteriopsis argyrophylla
                   (A. Juss.)
                   B. Gates
                   Heteropterys cf.                         X
                   cochleosperma A. Juss.
                   Heteropterys dumetorum
                   (Griseb.) Nied.
                   Heteropterys cf. glandulosa
                   A. Juss.
                   Heteropterys cf. intermedia

                   (A. Juss.)
                   Griseb.
                   Heteropterys tomentosa A.                X
                   Juss.
                   Janusia guaranitica (A.                  X
                   St.-Hil.) A. Juss.
                   Mascagnia cordifolia (A.                 X
                   Juss.) Griseb.

PASSIFLORACEAE     Passiflora pohlii Mast.                  X
                   Passiflora tricuspis Mast.               X

RUBIACEAE          Manettia cordifolia Mart.                X

SAPINDACEAE        Serjania hebecarpa Benth.                X
                   Serjania marginata Casar.
                   Serjania caracasana (Jacq.)              X
                   Willd.
                   Serjania erecta Radlk.
                   Serjania perulacea Radlk.                X
                   Serjania setigera Radlk.
                   Urvillea laevis Radlk.                   X
                   Urvillea ulmacea Kunth

SMILACACEAE        Smilax campestris Griseb.                X
                   Smilax fluminensis Steud.                X

VITACEAE           Cissus alata Jacq.                       X
                   Cissus verticillata (L.)                 X
                   Nicolson & C.E. Jarvis

Family                    Climber Species                 Life
                                                    SDF   Form

APOCYNACEAE        Mesechites mansoanus (A.DC.)      X     H
                   Woodson
                   Tassadia berteroana (Spreng.)     X     H
                   W.D. Stevens

ASTERACEAE         Dasyphyllum vagans (Gardner)      X     W
                   Cabrera

BIGNONIACEAE       Fridericia pubescens (L.)               W
                   L.G. Lohmann

COMBRETACEAE       Combretum rotundifolium Rich.     X     W

CONVOLVULACEAE     Ipomoea indivisa (Vell.)          X     H
                   Hallier f.
                   Ipomoea ramosissima (Poir.)             H
                   Choisy
                   Ipomoea nil (L.) Roth.            X     H
                   Ipomoea cynanchifolia Meisn.      X     H
                   Ipomoea cf. rubens Choisy         X     H
                   Jacquemontia velutina Choisy            H

DIOSCOREACEAE      Dioscorea cf. sinuata Vell.       X     H
                   Dioscorea amaranthoides C.        X     H
                   Presl
                   Dioscorea aesculifolia R.         X     H
                   Kunth
                   Dioscorea cf. altissima Lam.      X     W
                   Dioscorea demourae Uline ex.            H
                   R. Kunth
                   Dioscorea glandulosa                    H
                   (Griseb.) Kunth
                   Dioscorea grandiflora Mart.             H
                   ex Griseb.
                   Dioscorea orthogoneura Uline      X     H
                   ex. Hochr.
                   Dioscorea ovata Vell.             X     H
                   Dioscorea sincorensis R. Kunth          W

EUPHORBIACEAE      Manihot anomala Pohl              X     W
                   Manihot tripartita (Spreng.)      X     W
                   Mull. Arg.
                   Tragia hieronymi Pax & K.         X     H
                   Hoffm.

FABACEAE           Camptosema ellipticum (Desv.)           H
(Papilionoideae)   Burkart
                   Centrosema sagittatum             X     H
                   (Humb. & Bonpl.
                   ex Willd.) Brandegee
                   Galactia benthamiana Micheli      X     W
                   Galactia striata (Jacq.) Urb.           H
                   Leptospron adenanthum             X     H
                   (G. Mey.)
                   A. Delgado
                   Rhynchosia edulis Griseb.         X     H
                   Ancistrotropis firmula                  H
                   (Mart. Ex Benth.)
                   A. Delgado
                   Ancistrotropis peduncularis             H
                   (Kunth)
                   A. Delgado

MALPIGHIACEAE      Banisteriopsis argyrophylla       X     W
                   (A. Juss.)
                   B. Gates
                   Heteropterys cf.                  X     W
                   cochleosperma A. Juss.
                   Heteropterys dumetorum            X     W
                   (Griseb.) Nied.
                   Heteropterys cf. glandulosa       X     W
                   A. Juss.
                   Heteropterys cf. intermedia       X     W
                   (A. Juss.)
                   Griseb.
                   Heteropterys tomentosa A.               W
                   Juss.
                   Janusia guaranitica (A.                 H
                   St.-Hil.) A. Juss.
                   Mascagnia cordifolia (A.          X     W
                   Juss.) Griseb.

PASSIFLORACEAE     Passiflora pohlii Mast.                 H
                   Passiflora tricuspis Mast.              H

RUBIACEAE          Manettia cordifolia Mart.         X     H

SAPINDACEAE        Serjania hebecarpa Benth.         X     W
                   Serjania marginata Casar.         X     H
                   Serjania caracasana (Jacq.)       X     W
                   Willd.
                   Serjania erecta Radlk.            X     W
                   Serjania perulacea Radlk.         X     W
                   Serjania setigera Radlk.          X     W
                   Urvillea laevis Radlk.                  W
                   Urvillea ulmacea Kunth            X     W

SMILACACEAE        Smilax campestris Griseb.               W
                   Smilax fluminensis Steud.         X     H

VITACEAE           Cissus alata Jacq.                X     H
                   Cissus verticillata (L.)                H
                   Nicolson & C.E. Jarvis

Family                    Climber Species           Climbing
                                                    Mechanism

APOCYNACEAE        Mesechites mansoanus (A.DC.)        AT
                   Woodson
                   Tassadia berteroana (Spreng.)       AT
                   W.D. Stevens

ASTERACEAE         Dasyphyllum vagans (Gardner)        SC
                   Cabrera

BIGNONIACEAE       Fridericia pubescens (L.)           TE
                   L.G. Lohmann

COMBRETACEAE       Combretum rotundifolium Rich.       AT

CONVOLVULACEAE     Ipomoea indivisa (Vell.)            AT
                   Hallier f.
                   Ipomoea ramosissima (Poir.)         AT
                   Choisy
                   Ipomoea nil (L.) Roth.              AT
                   Ipomoea cynanchifolia Meisn.        AT
                   Ipomoea cf. rubens Choisy           AT
                   Jacquemontia velutina Choisy        AT

DIOSCOREACEAE      Dioscorea cf. sinuata Vell.         AT
                   Dioscorea amaranthoides C.          AT
                   Presl
                   Dioscorea aesculifolia R.           AT
                   Kunth
                   Dioscorea cf. altissima Lam.        AT
                   Dioscorea demourae Uline ex.        AT
                   R. Kunth
                   Dioscorea glandulosa                AT
                   (Griseb.) Kunth
                   Dioscorea grandiflora Mart.         AT
                   ex Griseb.
                   Dioscorea orthogoneura Uline        AT
                   ex. Hochr.
                   Dioscorea ovata Vell.               AT
                   Dioscorea sincorensis R. Kunth      AT

EUPHORBIACEAE      Manihot anomala Pohl                SC
                   Manihot tripartita (Spreng.)        SC
                   Mull. Arg.
                   Tragia hieronymi Pax & K.           AT
                   Hoffm.

FABACEAE           Camptosema ellipticum (Desv.)       AT
(Papilionoideae)   Burkart
                   Centrosema sagittatum               AT
                   (Humb. & Bonpl.
                   ex Willd.) Brandegee
                   Galactia benthamiana Micheli        AT
                   Galactia striata (Jacq.) Urb.       AT
                   Leptospron adenanthum               AT
                   (G. Mey.)
                   A. Delgado
                   Rhynchosia edulis Griseb.           AT
                   Ancistrotropis firmula              AT
                   (Mart. Ex Benth.)
                   A. Delgado
                   Ancistrotropis peduncularis         AT
                   (Kunth)
                   A. Delgado

MALPIGHIACEAE      Banisteriopsis argyrophylla         AT
                   (A. Juss.)
                   B. Gates
                   Heteropterys cf.                    AT
                   cochleosperma A. Juss.
                   Heteropterys dumetorum              AT
                   (Griseb.) Nied.
                   Heteropterys cf. glandulosa         AT
                   A. Juss.
                   Heteropterys cf. intermedia         AT
                   (A. Juss.)
                   Griseb.
                   Heteropterys tomentosa A.           AT
                   Juss.
                   Janusia guaranitica (A.             SC
                   St.-Hil.) A. Juss.
                   Mascagnia cordifolia (A.            SC
                   Juss.) Griseb.

PASSIFLORACEAE     Passiflora pohlii Mast.             TE
                   Passiflora tricuspis Mast.          TE

RUBIACEAE          Manettia cordifolia Mart.           AT

SAPINDACEAE        Serjania hebecarpa Benth.           TE
                   Serjania marginata Casar.           TE
                   Serjania caracasana (Jacq.)         TE
                   Willd.
                   Serjania erecta Radlk.              TE
                   Serjania perulacea Radlk.           TE
                   Serjania setigera Radlk.            TE
                   Urvillea laevis Radlk.              TE
                   Urvillea ulmacea Kunth              TE

SMILACACEAE        Smilax campestris Griseb.           TE
                   Smilax fluminensis Steud.           TE

VITACEAE           Cissus alata Jacq.                  TE
                   Cissus verticillata (L.)            TE
                   Nicolson & C.E. Jarvis

Family                    Climber Species           Dispersal   Voucher
                                                    syndrome     CGMS

APOCYNACEAE        Mesechites mansoanus (A.DC.)        ANE       41360
                   Woodson
                   Tassadia berteroana (Spreng.)       ANE       41361
                   W.D. Stevens

ASTERACEAE         Dasyphyllum vagans (Gardner)        ANE       41419
                   Cabrera

BIGNONIACEAE       Fridericia pubescens (L.)           ANE       41364
                   L.G. Lohmann

COMBRETACEAE       Combretum rotundifolium Rich.       ANE       41365

CONVOLVULACEAE     Ipomoea indivisa (Vell.)            AUT       41367
                   Hallier f.
                   Ipomoea ramosissima (Poir.)         AUT       41371
                   Choisy
                   Ipomoea nil (L.) Roth.              AUT       41369
                   Ipomoea cynanchifolia Meisn.        AUT       41370
                   Ipomoea cf. rubens Choisy           AUT       41372
                   Jacquemontia velutina Choisy        ANE       41363

DIOSCOREACEAE      Dioscorea cf. sinuata Vell.         ANE       41374
                   Dioscorea amaranthoides C.          ANE       41373
                   Presl
                   Dioscorea aesculifolia R.           ANE       41379
                   Kunth
                   Dioscorea cf. altissima Lam.        ANE       41408
                   Dioscorea demourae Uline ex.        ANE       41380
                   R. Kunth
                   Dioscorea glandulosa                ANE       41381
                   (Griseb.) Kunth
                   Dioscorea grandiflora Mart.         ANE       41382
                   ex Griseb.
                   Dioscorea orthogoneura Uline        ANE       41383
                   ex. Hochr.
                   Dioscorea ovata Vell.               ANE       41384
                   Dioscorea sincorensis R. Kunth      ANE       41407

EUPHORBIACEAE      Manihot anomala Pohl                AUT       41385
                   Manihot tripartita (Spreng.)        AUT       41386
                   Mull. Arg.
                   Tragia hieronymi Pax & K.           AUT       41403
                   Hoffm.

FABACEAE           Camptosema ellipticum (Desv.)       AUT       41387
(Papilionoideae)   Burkart
                   Centrosema sagittatum               AUT       41389
                   (Humb. & Bonpl.
                   ex Willd.) Brandegee
                   Galactia benthamiana Micheli        AUT       50235
                   Galactia striata (Jacq.) Urb.       AUT       41391
                   Leptospron adenanthum               AUT       41390
                   (G. Mey.)
                   A. Delgado
                   Rhynchosia edulis Griseb.           AUT       41392
                   Ancistrotropis firmula              AUT       41393
                   (Mart. Ex Benth.)
                   A. Delgado
                   Ancistrotropis peduncularis         AUT       41394
                   (Kunth)
                   A. Delgado

MALPIGHIACEAE      Banisteriopsis argyrophylla         ANE       41395
                   (A. Juss.)
                   B. Gates
                   Heteropterys cf.                    ANE       41397
                   cochleosperma A. Juss.
                   Heteropterys dumetorum              ANE       41398
                   (Griseb.) Nied.
                   Heteropterys cf. glandulosa         ANE       41400
                   A. Juss.
                   Heteropterys cf. intermedia         ANE       41401
                   (A. Juss.)
                   Griseb.
                   Heteropterys tomentosa A.           ANE       41402
                   Juss.
                   Janusia guaranitica (A.             ANE       41396
                   St.-Hil.) A. Juss.
                   Mascagnia cordifolia (A.            ANE       50236
                   Juss.) Griseb.

PASSIFLORACEAE     Passiflora pohlii Mast.             ZOO       41405
                   Passiflora tricuspis Mast.          ZOO       41404

RUBIACEAE          Manettia cordifolia Mart.           AUT       41406

SAPINDACEAE        Serjania hebecarpa Benth.           ANE       41410
                   Serjania marginata Casar.           ANE       41409
                   Serjania caracasana (Jacq.)         ANE       41411
                   Willd.
                   Serjania erecta Radlk.              ANE       41412
                   Serjania perulacea Radlk.           ANE       41413
                   Serjania setigera Radlk.            ANE       41414
                   Urvillea laevis Radlk.              ANE       41415
                   Urvillea ulmacea Kunth              ANE       41416

SMILACACEAE        Smilax campestris Griseb.           ZOO       50237
                   Smilax fluminensis Steud.           ZOO       41417

VITACEAE           Cissus alata Jacq.                  ZOO       41420
                   Cissus verticillata (L.)            ZOO       41421
                   Nicolson & C.E. Jarvis

Phytophysiognomies: CE, Cerradao; SDF, Seasonal Deciduous Forest;
Life Form: H, Herbaceous; W, Woody; Climbing Mechanism: AT, Apical
Twining; TE, Tendrilling; SC, Scandent; Dispersal syndrome: ANE,
Anemochory; AUT, Autochory; ZOO, Zoochory.

TABLE 2
Morphological characters of 55 climber species in cerradao and SDF
(Seasonal Deciduous Forest) in the Serra de Maracaju, Mato Grosso do
Sul state, Central Brazil

                 Life forms

            Herbaceous       Woody

Cerradao    20 (64.5 %)   11 (35.5 %)
SDF         19 (51.4 %)   18 (48.6 %)
Total       32 (58.2 %)   23(41.8 %)

                      Climbing mechanism

            Apical Twining   Tendrilling   Scandent

Cerradao     17 (54.8 %)     11 (35.5 %)   3 (9.7 %)
SDF          24 (64.9 %)     9 (24.3 %)    4 (8.1 %)
Total        35 (63.6 %)     15 (27.3 %)   5 (7.3 %)

                      Dispersal syndrome

            Anemochoric   Autochoric    Zoochoric

Cerradao    15 (48.4 %)   10 (32.3 %)   6 (19.4 %)
SDF         23 (62.2 %)   12 (32.4 %)   2 (5.4 %)
Total       32 (58.2 %)   17 (30.9 %)   6 (10.9 %)
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Author:Souza Brito, Ana Carolina; Ferraro, Alexandre; Almeida Assuncao, Vivian; Burnham, Robyn J.; Bagnator
Publication:Revista de Biologia Tropical
Date:Sep 1, 2017
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