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Inventory • Biota neotrop. 14 (4) • Dec 2014 • https://doi.org/10.1590/1676-06032014006214   copy

Checklist of climbing plants in an Araucaria forest of Rio Grande do Sul State, Brazil

Florística de trepadeiras em uma floresta de Araucária do Estado do Rio Grande do Sul, Brasil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstracts

Climbing plants are remarkable components of forests, highly contributing for the diversity and dynamics of communities. Studies focusing on climbing plants are scarce and for many vegetation types little is known about climbing species composition and their traits relevant for dispersal and establishment. The focus of this study is to provide the first floristic inventory of climbing plants in an Araucaria forest of Brazil, describing the dispersal syndromes and climbing mechanisms of species and comparing these traits and species composition patterns with other study sites in Southern Brazil. We found 104 taxa belonging to 33 families, with Asteraceae (22 spp.) and Apocynaceae (14 spp.) being the richest families. Among climbing mechanisms, stem twiner (50 spp.) is the most common, followed by tendril (20 spp.) and scrambler (12 spp.), while in relation to the dispersal syndromes, anemochoric species (65 spp.) are the most relevant followed by endozoochoric (28 spp.). Three new species registries were found for Rio Grande do Sul State expanding their occurrence range towards South Brazil. The comparison of climbers’ survey sites showed two sharp groups in relation to species composition and traits proportion, Seasonal and Araucaria/Atlantic forest sites, but with no difference of traits frequency between sites. There is a predominance of stem twiners species in all sites, but the relative difference for tendril species increases in Araucaria and Atlantic forest sites. The Asteraceae and Apocynaceae families were the most relevant, contrasting to Seasonal forests of Southeast Brazil. Interesting patterns can be achieved with a more detailed classification of climbing mechanisms and the results found in this study contributes to enhance the knowledge on climbers’ traits and diversity in South Brazil.

Lianas; Vines; Climbing mechanisms; Dispersal syndromes; Floristic of climbers

Trepadeiras são importantes componentes florestais, contribuindo na diversidade e dinâmica de comunidades vegetais. Estudos focados em trepadeiras são escassos e para muitos tipos vegetacionais pouco se sabe sobre a composição de espécies de trepadeiras e seus atributos relevantes para dispersão e estabelecimento. O foco deste estudo é fornecer o primeiro inventário florístico de plantas trepadeiras em uma floresta de Araucária no Brasil, descrevendo as síndromes de dispersão e mecanismos de escalada das espécies e comparando esses atributos e a composição de espécies com outros sítios no Sul do Brasil. Foram encontrados 104 taxa pertencentes a 33 famílias, sendo Asteraceae (22 spp.) e Apocynaceae (14 spp.) as famílias mais ricas. Dentre os mecanismos de escalada, o tipo volúvel (50 spp.) é o mais comum, seguido por gavinhas (20 spp.) e apoiantes (12 spp.), enquanto em relação ès síndromes de dispersão as espécies anemocóricas (65 spp.) são as mais relevantes seguidas por endozoocóricas (28 spp.). Três novos registros de espécies foram encontrados para o Estado do Rio Grande do Sul, expandindo suas extensões de ocorrência para o Sul do Brasil. A comparação entre sítios evidenciou dois grupos nítidos em relação è composição de espécies e proporção de atributos, sítios em florestas sazonais e nas florestas com Araucária e Atlântica, porém não há diferença na frequência dos atributos entre os sítios. Há uma predominância de espécies volúveis em todos os sítios, entretanto a diferença relativa para espécies com gavinhas aumenta nos sítios de floresta com Araucária e Atlântica. As famílias Asteraceae e Apocynaceae foram as mais relevantes, contrastando com florestas sazonais no Sudeste do Brasil. Padrões interessantes podem ser encontrados com uma classificação mais detalhada dos mecanismos de escalada e os resultados encontrados neste estudo contribuem para aumentar o conhecimento sobre os atributos e a diversidade de trepadeiras no Sul do Brasil.

Lianas; Mecanismos de Escalada; Síndromes de dispersão; Florística de Trepadeiras

Introduction

The Araucaria forest, part of Mata Atlântica Biome, is the main forest type of South Brazil (IBGE 2004IBGE. 2004. Mapa de vegetação do Brasil. Instituto Brasileiro de Geografia e Estatística. Rio de Janeiro, Brasil.). It occurs continuously in the highlands of the Southern Brazilian Plateau and in small isolated areas of Argentina, Paraguay, Southeast Brazil and “Serra do Sudeste” formation in Rio Grande do Sul State, Brazil (Hueck 1972HUECK, K. 1972. As florestas da América do Sul: ecologia, composição e importância econômica. Polígono, São Paulo., Carlucci et al. 2011aCARLUCCI, M.B., JARENKOW, J.A., DUARTE, L.D.S. & PILLAR, V.D. 2011a. Conservação da Floresta com Araucária no Extremo Sul do Brasil. Nat. Conservacao 9:11-114.). Timber logging of Araucaria angustifolia (Bertol.) Kuntze and other species was an important economic feature in the last century (Reitz et al. 1983REITZ, R., KLEIN, R.M., & REIS, A. 1983. Projeto Madeira do Rio Grande do Sul. Sellowia 34/35:1-525.), which contributed for reducing the Araucaria forest to less than 12.6% of its original area (Ribeiro et al. 2009RIBEIRO, M.C., METZGER, J.P., MARTENSEN, A.C PONZONI, F.J & HIROTA, M.M. 2009. The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142:1141-1153, 10.1016/j.biocon.2009.02.021.
https://doi.org/10.1016/j.biocon.2009.02... ). In spite of its wide geographic range, studies in the Araucaria forest manly focused on trees’ communities (e.g. Duarte et al. 2012DUARTE, L.D.S., PRIETO, P.V. & PILLAR, V.D. 2012. Assessing spatial and environmental drivers of phylogenetic structure in Brazilian Araucaria forests. Ecography 35:001-009, 10.1111/j.1600-0587.2011.07193.x.
https://doi.org/10.1111/j.1600-0587.2011... ), no study to date has focused on climbing plants.

Climbing plants are important components of forests dynamics, contributing with biomass and plant diversity (Schnitzer & Bongers 2011SCHNITZER, S.A. & BONGERS, F. 2011. Increasing liana abundance and biomass in tropical forests: emerging patterns and putative mechanisms. Ecol. Lett. 14:397-406, 10.1111/j.1461-0248.2011.01590.x.
https://doi.org/10.1111/j.1461-0248.2011... ), affecting mortality and growth of trees (Ingwell et al. 2010INGWELL, L.L., WRIGHT, S.J., BECKLUND, K.K., HUBBELL, S.P. & SCHNITZER, S.A. 2010. The impact of lianas on 10 years of tree growth and mortality on Barro Colorado Island, Panama. J. Ecol. 98:879-887, 10.1111/j.1365-2745.2010.01676.x.
https://doi.org/10.1111/j.1365-2745.2010... ), collaborating with treefall gaps formation and preventing trees regeneration on it (Schnitzer & Carson 2010SCHNITZER, S.A. & CARSON, W.P. 2010. Lianas suppress tree regeneration and diversity in treefall gaps. Ecol. Lett. 13:849-857, 10.1111/j.1461-0248.2010.01480.x.
https://doi.org/10.1111/j.1461-0248.2010... ). Climbing species show a diversity of climbing mechanisms/strategies (Hegarty & Caballé 1991HEGARTY, E.E. & G C.A.B.A.L.L.É. 1991. Distribution and abundance of vines in forest communities. In The Biology of Vines (Putz, F.E. & Mooney, H.A., eds.). Cambridge University Press, Cambridge, pp. 313-335.) to reach the best productive position, with full access to sunlight where they reproduce and spread through other trees canopies (Campbell & Newbery 1993CAMPBELL, E.J.F. & NEWBERY, D. 1993. Ecological relationships between lianas and trees in lowland rain forest in Sabah, East Malaysia. J. Trop. Ecol. 9:469-490, 10.1017/S0266467400007549.
https://doi.org/10.1017/S026646740000754... ). Forest structure directly influences the abundance, diversity and distribution of climbers. For instance, forest edges and treefall gaps present high diversity and density of climbers (Laurance et al. 2001LAURANCE, W.F., PÉREZ-SALICRUP, D., DELAMÔNICA, P., FEARNSIDE, P.M., D'ANGELO, S., JEROZOLINSKI, A., POHL, L. & LOVEJOY, T.E. 2001. Rain forest fragmentation and the structure of Amazonian liana communities. Ecology 82:105-116, 10.1890/0012-9658(2001)082[0105:RFFATS]2.0.CO;2.
https://doi.org/10.1890/0012-9658(2001)0... , Londré & Schnitzer 2006LONDRÉ, R.A. & SCHNITZER, S.A. 2006. The distribution of lianas and their change in abundance in temperate forests over the past 45 years. Ecology 87:2973-2978.), strongly determined by light availability on these early successional stages (DeWalt et al. 2000DEWALT, S., SCHNITZER, S.A. & DENSLOW, J.S. 2000. Density and diversity of lianas along a chronosequence in a central Panamanian lowland forest. J. Trop. Ecol. 16:1-19, 10.1017/S0266467400001231.
https://doi.org/10.1017/S026646740000123... ).

The Araucaria forest is expanding over Campos grasslands since the Holocene (Behling & Pillar 2007BEHLING, H. & PILLAR, V.D. 2007. Late Quaternary vegetation, biodiversity and fire dynamics on the southern Brazilian highland and their implication for conservation and management of modern Araucaria forest and grassland ecosystems. Philos. T. Roy. Soc. B 362:243-251, 10.1098/rstb.2006.1984.
https://doi.org/10.1098/rstb.2006.1984... ), mainly through forest edge expansion (Carlucci et al. 2011bCARLUCCI, M.B., TEIXEIRA, F.Z., BRUM, F.T. & DUARTE, L.S. 2011b. Edge expansion of Araucaria forest over southern Brazilian grasslands relies on nurse plant effect. Community Ecol. 12:196-201, 10.1556/ComEc.12.2011.2.7.
https://doi.org/10.1556/ComEc.12.2011.2.... ) and nucleation process (Duarte et al. 2006DUARTE, L.D.S., DOS SANTOS, M.M.G, HARTZ, S.M. & PILLAR, V.D. 2006. Role of nurse plants in Araucaria forest expansion over grasslands in south Brazil. Austral Ecol. 31:520-528, 10.1111/j.1442-9993.2006.01602.x.
https://doi.org/10.1111/j.1442-9993.2006... ). These expansion processes create a great amount of habitats for climbing species like forest edges and patches with different sizes and light availability, which are similar to fragmented landscapes caused by anthropic action known to positively affect climber’s abundance (Londré & Schnitzer 2006LONDRÉ, R.A. & SCHNITZER, S.A. 2006. The distribution of lianas and their change in abundance in temperate forests over the past 45 years. Ecology 87:2973-2978.). Since climbers are considered pioneer species and play an important role in forest succession (DeWalt et al. 2000DEWALT, S., SCHNITZER, S.A. & DENSLOW, J.S. 2000. Density and diversity of lianas along a chronosequence in a central Panamanian lowland forest. J. Trop. Ecol. 16:1-19, 10.1017/S0266467400001231.
https://doi.org/10.1017/S026646740000123... ), it is important to know their diversity, as well as their traits that might give an important overview of their limitations and capacity of dispersal and establishment at different environments. In this context, the aim of this study is to provide the first survey focused on climbing plants in an Araucaria forest of Southern Brazil and compare species traits (dispersal syndromes and climbing mechanisms) and composition with other study sites belonging to different forest types in South Brazil. We hypothesize that study sites of the same forest type are similar in relation to species composition and traits proportion.

Material and Methods

The floristic survey was carried out at the National Forest of São Francisco de Paula - ICMBIO (“Floresta Nacional de São Francisco de Paula”; FLONA-SFP), a conservation unit of sustainable use, located in São Francisco de Paula municipality in Rio Grande do Sul State (29°25’24”S, 50°23’13”W; Figure 1). FLONA-SFP is composed by a mosaic landscape of Araucaria forest remnants together with ecologically-managed Araucaria angustifolia (Bertol.) Kuntze, Eucalyptus spp. and Pinus spp. plantations and a small area of unmanaged Campos grassland. It covers 1,606 ha, where 36.6 % is covered by Araucaria forest remnants, ranging in altitude from 600 to 923 m a.s.l. The regional climate is characterized as subtropical rainy, with precipitation uniformly distributed throughout the year. The annual mean rainfall reaches 2,252 mm and the annual mean temperature is 14.4 °C with the occurrence of negative temperatures from April to November and rare events of snow (National Institute of Meteorology - INMET).

Figure 1
Location of the National Forest of São Francisco de Paula, RS, Brazil (29°25’24”S, 50°23’13”W) (Source: http://earth.google.com, 2013).

Climbers were monitored monthly from July 2007 to August 2009 along 13 km of trails inside and at the edges of Araucaria forest remnants and planting areas of A. angustifolia. Additionally, another 15 field trips were done from March 2010 to October 2013 at areas not visited before. These extra field trips covered around 70 ha of Araucaria forest remnants and 240 treefall gaps. The total survey comprised around 200 days of field trips. Voucher specimens were deposited at ICN Herbarium (Departamento de Botânica, Instituto de Biociências, Universidade Federal do Rio Grande do Sul). All taxa were classified into families following the APG III system (APG 2009APG III. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161:105-121, 10.1111/j.1095-8339.2009.00996.x.
https://doi.org/10.1111/j.1095-8339.2009... ) and according to its dispersal syndrome and climbing mechanism, using specialized literature and personal observation. Dispersal syndromes were classified according to van der Pijl (1982)VAN DER PIJL, L. 1982. Ecological Dispersal Classes, Established on the Basis of the Dispersing Agents. In Principles of Dispersal in Higher Plants (van der PijlL., ed.). Springer-Verlag, Berlin Heidelberg New York, pp.22-90. into anemochoric, endozoochoric, epizoochoric, autochoric and barochoric. Some species uncertain about their dispersal syndrome and not clearly classified in specialized literature, were classified as anemochoric only when specialized appendices like plumes or wings were present, otherwise were considered as barochoric. The climbing mechanisms were classified according to Hegarty (1991)HEGARTY, E.E. 1991. Vine-host interactions. In The Biology of Vines ( Putz, F.E. & Mooney, H.A. eds.). Cambridge University Press, Cambridge, pp. 357-375. into stem twiner, petiole twiner, secondary shoot twiner, tendril (that coil), clasp tendril, adhesive tendril (terminal adhesive pads), scrambler, hook/spine (also aculeus or trichomes that prevent slipping) and adherent roots. Many species combine different climbing mechanisms, making them difficult to be correctly classified (Hegarty 1991HEGARTY, E.E. 1991. Vine-host interactions. In The Biology of Vines ( Putz, F.E. & Mooney, H.A. eds.). Cambridge University Press, Cambridge, pp. 357-375.). In these cases, we considered the main climbing mechanism the first to appear during species development (personal observation), but we also cite the secondary climbing mechanism. Species abundance was estimated by counting individuals during July 2007 to August 2009 (with an exception for new species found within March 2010 to October 2013) and species were classified as singletons (one individual found), low abundance (two to five individuals) and high abundance (more than 100 individuals).

In the State of Rio Grande Sul (RS), 11 studies sampled climbing species (Table 1) in different forest types, but only three of them, besides this survey, strictly focused on climbing plants. For the comparison between sites we selected the studies with more than 40 climbing species (eight sites), considered as reliable surveys. In each study, we compiled the checklist, checked for species synonymies, excluded exotic species, and complemented the survey reviewing species deposited at ICN and PACA (Instituto Anchietano de Pesquisas/UNISINOS) herbariums, assessing herbarium records from speciesLink (CRIA 2014CRIA. 2014. Centro de Referência em Informação Ambiental - speciesLink. http://splink.cria.org.br/ (último acesso em 07/ago/2014).
http://splink.cria.org.br/... ) and consulting taxonomic studies for RS State. Species were classified in relation to their dispersal syndromes and climbing mechanisms following the same classification explained before, combining personal knowledge and specialized literature. To analyze sites relationship according to species composition and traits proportion (dispersal syndromes and climbing mechanisms) we performed separate cluster analyses, using Ward’s clustering criterion and evaluating groups partition sharpness through 10,000 bootstrap resampling (Pillar 1999PILLAR, V.D. 1999. How sharp are classifications? Ecology 80(8):2508-2516.). As resemblance measurements between sites, we used the complement of Jaccard’s similarity for species composition, and a modification of Gower's distance (Pavoine et al. 2009PAVOINE, S., VALLET, J., DUFOUR, A.B., GACHET, S., & DANIEL, H. 2009. On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118(3):391-402.) for traits proportion. We also performed Fisher’s exact tests with 10,000 Monte Carlo test replicates to evaluate whether there was a difference in the frequency of dispersal syndromes and climbing mechanisms between all sites. The modified Gower's distance was calculated in the package ade4 v.1.6-2 (Dray & Dufour 2007DRAY, S. & DUFOUR, A.B. 2007. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22(4):1-20.) in the R Statistical Environment (R Core Team 2014R CORE TEAM. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.
http://www.R-project.org/... ). The complement of Jaccard’s similarity and clustering analyses were performed using MULTIV 3.27b statistical software (by V.D. Pillar; available at http://ecoqua.ecologia.ufrgs.br/software).

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Table 1
Floristic surveys of climbing plant species in Rio Grande do Sul State, Brazil. Forest types: AR - Araucaria forest; AT - Atlantic forest; D - Deciduous forest; R - Restinga forest; SD - Semideciduous forest; †Floristic survey of all plant life forms; Forest types classification is according to IBGE (2012)IBGE. 2012. Manuais Técnicos em Geociências 1 - Manual Técnico da Vegetação Brasileira. 2 ed. Brasil: Instituto Brasileiro de Geografia e Estatística (IBGE), Rio de Janeiro..

Results

A total of 104 taxa were found at FLONA-SFP, belonging to 103 species, 62 genera and 33 families (Table 2). The richest families were Asteraceae (21 species), Apocynaceae (14), Fabaceae (10), Rubiaceae (7), Bignoniaceae and Malpighiaceae (5). Altogether these six families comprise 62 taxa (60% of total richness). Around a half of the families (16) contain two or more taxa, comprising 84% of total richness, while 20 genera containing two or more taxa comprise 62 taxa (60% of total richness). The richest genera were Mikania Willd. with 12 species, Oxypetalum R.Br. and Manettia Mutis ex L. with five. Around 29 species presented low abundance with a maximum of five individuals found and within them, six were singletons (Table 2). Considering the species in reproductive activity during July 2007 to August 2009 (G.D.S. Seger, unpublished data), eight species presented more than 100 individuals, while considering sterile individuals this number rises up to 27 species (Table 2).

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Table 2
Species list, climbing mechanism, dispersal syndrome and the ICN voucher number of climbing species surveyed at the National Forest of São Francisco de Paula, RS, Brazil. Climbing mechanism: STw (Stem Twiner); PTw (Petiole Twiner); SSTw (Secondary Shoot Twiner); Td (Tendril); CTd (Clasp Tendril); ATd (Adhesive Tendril); Sc (Scrambler); HS (Hook/Spine); R (Adherent Roots). Dispersal Syndrome: A (Anemochoric); Z (Endozoochoric); Ep (Epizoochoric); T (Autochoric); B (Barochoric); Anemochoric subtypes (Pg - Pogonochoric; Pt - Pterochoric). Abundance: S (Singleton); L (Low; two to five individuals); H (High; more than 100 individuals). *Voucher deposited at the HUCS Herbarium (Universidade Federal de Caxias do Sul, Rio Grande do Sul State, Brazil).

The most common climbing mechanism is stem twinner (50 taxa) followed by tendril (20), scrambler (12), hook/spine (8), petiole twinner (6), adherent roots (3), clasp tendril (2), secondary shoot twinner (2) and adhesive tendril (1) (Table 2). A secondary climbing mechanism is present in six species. There is a predominance of anemochoric dispersal syndrome (65 taxa) followed by endozoochoric (28), barochoric (6), autochoric (4) and epizoochoric (1). Within anemochory, there are more pogonochoric species (plummed diaspores; 39 species) than pterochoric (winged diaspores; 26 species) (Table 2).

We found three new registries for the State of RS, Matelea dusenii Morillo (Apocynaceae family), Manettia verticillata Wernham (Rubiaceae) and Piptadenia affinis Burkart (Fabaceae) (Figure 2), extending their occurrence range towards South Brazil. P. affinis presented low abundance with only eight individuals found. M. dusenii is very rare with just one sapling and one individual at reproductive stage found, while M. verticillata presented only three individuals.

Figure 2
. New species occurrences for Rio Grande do Sul State, Brazil. A-D: Piptadenia affinis Burkart; E and F: Manettia verticillata Wernham; G and H: Matelea dusenii Morillo.

The floristic surveys with more than 40 species (eight sites) comprised 286 species, distributed in 131 genera and 49 families. The richest families were Apocynaceae and Asteraceae (36 spp.), Fabaceae (24), Bignoniaceae (18), Cucurbitaceae and Convolvulaceae (16), Malpighiaceae (15), Passifloraceae and Sapindaceae (13) and Rubiaceae (11). These families comprised 69% of total richness. The richest climbing mechanism was stem twiner (144 spp.), followed by tendrils (66), scramblers (31) and hook/spine (21). Anemochoric species (154 spp.) were the most common, followed by endozoochoric (81), barochoric (26) and autochoric (18). The cluster analysis of species composition revealed two major groups that were the only group’s combination supported by group’s partition sharpness analysis, one with the Atlantic and Araucaria forests sites and other with Seasonal forest sites (Figure 3). The cluster analysis of traits proportion showed support for up to four sharp groups (Figure 4), firstly separating the Atlantic and Araucaria forests sites from Seasonal forest sites, the Semideciduous from Deciduous forest sites and the Torres (Tr) site from the FLONA-SFP and Dom Pedro de Alcântara (DP) sites. There is a clear predominance of the anemochoric dispersal syndrome in all sites followed by endozoochoric syndrome (Figure 5). Comparing the most abundant climbing mechanisms (stem twiner, tendrils, scramblers and hook/spines), that together represent between 86 and 95% of total richness in each site, there is a predominance of stem twiners in all sites, followed by trendril climbers (Figure 6). Other interesting patterns are the inversion of scramblers proportion in relation to hook/spine species in the Atlantic forest sites (DP and Tr; Figure 6) and the presence of species that climb with the aid of adherent roots in eastern sites (FLONA-SFP, DP and Tr; Figure 6). Comparing the floristic surveys, the Fisher’s exact test showed no difference for dispersal syndromes (P = 0.94) and climbing mechanisms (P = 0.23). Although there is a trend of observing a lower difference between anemochory and endozoochory in Semidecidual forest sites and a higher difference between stem twiners and tendril climbers in the Atlantic and Araucaria forest sites (Figures 5 and 6). When analyzing climbing mechanisms combining them in four major groups (joining stem twiner species with petiole twiner and secondary shoot twiner; tendril species with clasp tendril and adhesive tendril species; scrambler species with hook/spine species; and the adherent root species), as commonly seen in studies that classify the species’ climbing mechanisms (e.g. Santos et al. 2009SANTOS, K., KINOSHITA, L.S. & REZENDE, A.A. 2009. Species composition of climbers in seasonal semideciduous forest fragments of Southeastern Brazil. Biota Neotrop. 9(4):175-188 http://www.biotaneotropica.org.br/v9n4/pt/abstract?inventory+bn02409042009 (last access at 12/03/2014)., 10.1590/S1676-06032009000400018
http://www.biotaneotropica.org.br/v9n4/p... ), the Fisher’s exact test showed a significant result (P = 0.02).

Figure 3
. Dendrogram of climbers’ survey sites according to species composition in Rio Grande do Sul State, Brazil. Cluster analysis performed using Ward’s clustering criterion and the complement of Jaccard’s similarity as resemblance measure. Sites: De - Derrubadas (Turvo State Park); SM - Santa Maria; MC - Viamão (Morro do Coco); MG - Viamão (Morro Grande); Gb - Guaíba; SFP - National Forest of São Francisco de Paula; DP - Dom Pedro de Alcântara; Tr - Torres (Itapeva State Park).
Figure 4
. Dendrogram of climbers’ survey sites according to climbing mechanisms and dispersal syndromes proportion in Rio Grande do Sul State, Brazil. Cluster analysis performed using Ward’s clustering criterion and a modification of Gower's distance as resemblance measure. For sites abbreviations consult Figures 3 and 5.
Figure 5
. Species proportion at each study site (sites with more than 40 species) at Rio Grande do Sul State, according to its dispersal syndrome. Sites are disposed from west (left) to east (right). Dispersal Syndrome: A (Anemochoric); Z (Endozoochoric); B (Barochoric); T (Autochoric). Sites: De - Derrubadas (Turvo State Park); SM - Santa Maria; MC - Viamão (Morro do Coco); MG - Viamão (Morro Grande); Gb - Guaíba; SFP - National Forest of São Francisco de Paula; DP - Dom Pedro de Alcântara; Tr - Torres (Itapeva State Park).
Figure 6
. Species proportion at each study site (sites with more than 40 species) in Rio Grande do Sul State, according to its climbing mechanism. Sites are disposed from west (left) to east (right). Climbing mechanism: STw (Stem Twiner); Td (Tendril); Sc (Scrambler); HS (Hook/Spine); R (Roots). For sites abbreviations consult Figure 3 and 5.

Discussion

This is the first study focused only on climbing plant species realized in an Araucaria forest in Brazil. Studies focusing on climbing species are scarce in South Brazil (Citadini-Zanette 1997CITADINI-ZANETTE, V., SOARES, J.J. & MARTINELLO, C.M. 1997. Lianas de um remanescente florestal da microbacia do Rio Novo, Orleans, Santa Catarina. Insula 26:45-63., Venturi 2000VENTURI, S. 2000. Florística e fitossociologia do componente apoiante-escandente em uma floresta costeira subtropical. Dissertação de Mestrado, Universidade Federal do Rio Grande do Sul, Porto Alegre., Durigon et al. 2009DURIGON, J., CANTO-DOROW, T.S. & EISINGER, S.M. 2009. Composição florística de trepadeiras ocorrentes em fragmentos de floresta estacional, Santa Maria, Rio Grande do Sul, Brasil. Rodriguésia 60(2):415-422., Durigon & Waechter 2011DURIGON, J. & WAECHTER, J.L. 2011. Floristic composition and biogeographic relations of a subtropical assemblage of climbing plants. Biodivers. Conserv. 20(5):1027-1044, 10.1007/s10531-011-0012-5.
https://doi.org/10.1007/s10531-011-0012-... , Carneiro & Vieira 2012CARNEIRO, J.S. & VIEIRA, A.O.S. 2012. Trepadeiras: florística da Estação Ecológica do Caiuá e chave de identificação vegetativa para espécies do Norte do Estado do Paraná. Acta Scientiarum. Biological Sciences 34(2):217-223, 10.4025/actascibiolsci.v34i2.5892.
https://doi.org/10.4025/actascibiolsci.v... ) and even when climbing habit is included on broad floristic surveys, the species richness is commonly underestimated. Nevertheless, in many cases broad floristic surveys give an important overview of climbers’ richness, contributing for the knowledge of patterns like families’ richness in some regions. Among them, the study of Brack et al. (1985)BRACK, P., BUENO, R.M., FALKENBERG, D.B., PAIVA, M.R.C., SOBRAL, M., STEHMANN, J.R. 1985. Levantamento florístico do Parque Estadual do Turvo, Tenente Portela, Rio Grande do Sul, Brasil. Roessléria 7(1):69-94. at the Seasonal forest of Turvo State Park presented the highest richness of RS State, with around 130 species and since it was not focused only on climber plants, the richness could be even greater. The cluster analysis results partially agreed with our hypothesis that species composition is similar within forest types, showing two sharp groups of Seasonal forests and Araucaria/Atlantic forests, with no clear pattern association of Deciduous and Semideciduous forests. The study of Durigon & Waechter (2011)DURIGON, J. & WAECHTER, J.L. 2011. Floristic composition and biogeographic relations of a subtropical assemblage of climbing plants. Biodivers. Conserv. 20(5):1027-1044, 10.1007/s10531-011-0012-5.
https://doi.org/10.1007/s10531-011-0012-... found that the species composition of Guaíba site, one of the sites analyzed in this study, is similar to the biogeographic expansion line represented by the States from the north border of RS State. Our sites comparison is more detailed in relation to forest types, showing that the Semideciduous forests that are geographically close and present a mixture of floristic contingents of different origins (Waechter 2002WAECHTER J.L. 2002. Padrões geográficos na flora atual do Rio Grande do Sul. Ciência & Ambiente 24:93-10.) are more similar to Deciduous forests than Araucaria/Atlantic forests. It is noteworthy, as cited by Santos et al. (2009)SANTOS, K., KINOSHITA, L.S. & REZENDE, A.A. 2009. Species composition of climbers in seasonal semideciduous forest fragments of Southeastern Brazil. Biota Neotrop. 9(4):175-188 http://www.biotaneotropica.org.br/v9n4/pt/abstract?inventory+bn02409042009 (last access at 12/03/2014)., 10.1590/S1676-06032009000400018
http://www.biotaneotropica.org.br/v9n4/p... that any species richness comparison between these surveys should be done with some caution, since they differ in sampled area and time effort and some studies may be underestimating the real richness of the study areas.

The richest families sampled at FLONA-SFP are according to other surveys in the Atlantic forest of Southeast Brazil (Lima et al. 1997LIMA, H.C., LIMA, M.P.M., Vaz, A.M.S. & PESSOA, S.V.A. 1997. Trepadeiras da reserva ecológica de Macaé de Cima. In Serra de Macaé de Cima: diversidade florística e conservação em Mata Atlântica (Guedes-Brunini, R.R. & Lima, H.C. eds.). Jardim Botânico do Rio de Janeiro, Rio de Janeiro, p. 75-87., Barros et al. 2009BARROS, A.A.M., RIBAS, L.A. & ARAUJO, D.S.D. 2009. Trepadeiras do Parque Estadual da Serra da Tiririca (Rio de Janeiro, Brasil). Rodriguésia 60:681-694., Villagra & Neto 2010VILLAGRA, B.L.P. & NETO, S.R. 2010. Florística de trepadeiras no Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Revista Brasileira de Biociências 8(2):186-200.), but there is a clear predominance of Apocynaceae and Asteraceae families not only at FLONA-SFP but also in most sites of RS State. In Seasonal forests of Southeast Brazil (Santos et al. 2009SANTOS, K., KINOSHITA, L.S. & REZENDE, A.A. 2009. Species composition of climbers in seasonal semideciduous forest fragments of Southeastern Brazil. Biota Neotrop. 9(4):175-188 http://www.biotaneotropica.org.br/v9n4/pt/abstract?inventory+bn02409042009 (last access at 12/03/2014)., 10.1590/S1676-06032009000400018
http://www.biotaneotropica.org.br/v9n4/p... , Udulutsch et al. 2010)UDULUTSCH, R.G. 2010. Composição florística e chaves de identificação para as lianas da Estação Ecológica dos Caetetus, estado de São Paulo, Brasil. Rodriguésia 61(4):715-730., there is a predominance of species from Bignoniaceae, Fabaceae and Malpighiaceae families, in which the first two are also more representative in Seasonal forests of RS State. This demonstrates that the order of importance of families might not be only ruled by the vegetation type, but by the diversity center of some rich families/genera. In Seasonal forests of Southeast Brazil, Bignoniaceae presents its main diversity center (Lohmann et al. 2013LOHMANN, L.G., BELL, C.D., CALI=, M.F. & WINKWORTH, R.C. 2013. Pattern and timing of biogeographical history in the Neotropical tribe Bignonieae (Bignoniaceae). Bot. J. Linn. Soc. 171:154-170, 10.1111/j.1095-8339.2012.01311.x.
https://doi.org/10.1111/j.1095-8339.2012... ), while in rainforests Asteraceae family increases in importance. The highest richness of Asteraceae family is reported to high altitudes and its great representativeness is driven by Mikania Willd., the sixth world largest genus of climbers (Gentry 1991GENTRY, A.H. 1991. The distribution and evolution of climbing plants. In The Biology of Vines (Putz, F.E. & Mooney, H.A. eds.). Cambridge University Press, Cambridge, pp. 3-49.), that present its main diversity center in the Atlantic forest (Ritter & Waechter 2004RITTER, M.R. & WAECHTER, J.L. 2004. Biogeografia do gênero Mikania Willd. (Asteraceae) no Rio Grande do Sul, Brasil. Acta Bot. Bras. 8(3):643-652.). These phytogeographical patterns directly influences the climbing mechanisms and dispersal syndromes patterns over sites, since both families are anemochoric and Asteraceae is predominantly twiner while Bignoniaceae predominantly presents tendrils that coil. In Seasonal forests of Southeast Brazil, tendril species (encompassing trendrils that coil, clasp and adherent tendrils) overcome twiner species in many sites (Santos et al. 2009SANTOS, K., KINOSHITA, L.S. & REZENDE, A.A. 2009. Species composition of climbers in seasonal semideciduous forest fragments of Southeastern Brazil. Biota Neotrop. 9(4):175-188 http://www.biotaneotropica.org.br/v9n4/pt/abstract?inventory+bn02409042009 (last access at 12/03/2014)., 10.1590/S1676-06032009000400018
http://www.biotaneotropica.org.br/v9n4/p... ) whereas in Seasonal forests of RS State there is a prevalence of stem twiners. Adherent root climbers were more represented in the Araucaria and Atlantic forest sites, confirming their association with areas with high precipitation levels (Durigon et al. 2013DURIGON, J., DURÁN, S.M. & GIANOLI, E. 2013. Global distribution of root climbers is positively associated with precipitation and negatively associated with seasonality. J. Trop. Ecol. 29(4):357-360, 10.1017/S0266467413000308.
https://doi.org/10.1017/S026646741300030... ). The cluster analysis confirmed our hypothesis that species traits proportion were similar within forest types, showing that traits patterns are not modified by species turnover between sites and that it might be ruled by an association of vegetation type and geographic scale.

Not only light availability determines climbers’ distribution, but also the presence of suitable supports, which influences each climbing mechanism. Trelisses density, that is higher on forest edges and treefall gaps, limits climbers’ access to the canopy, since few species are capable to climb supports with more than 10-20 cm of diameter (Putz 1984PUTZ, F.E. 1984. The natural history of lianas on Barro Colorado Island, Panama. Ecology 65:1713-1724., Putz & Holbrook 1991PUTZ, F.E. & HOLBROOK, N.M. 1991. Biomechanical studies of vines. In The Biology of Vines (Putz, F.E. & H.A. Mooney, eds.). Cambridge University Press, Cambridge, pp. 73-97.). In this way, each climbing mechanism has support limitations that direct its occurrence and abundance to different successional stages with particular vegetation structure and/or forest disturbance regimes (Schnitzer & Bongers, 2002SCHNITZER, S.A. & BONGERS, F. 2002. The ecology of lianas and their role in forests. Trends Ecol. Evol. 17:223-230, 10.1016/S0169-5347(02)02491-6.
https://doi.org/10.1016/S0169-5347(02)02... ). The trendril climbers’ group formed by species with clasp tendrils, adhesive tendrils and tendrils that coil, present different support limitations which determine its success on climbing supports with high diameters and different types of bark. Tendrils are usually limited to supports with a maximum of 10 cm of diameter (Putz 1984PUTZ, F.E. 1984. The natural history of lianas on Barro Colorado Island, Panama. Ecology 65:1713-1724.), while clasp and adherent tendril’s species do not have any support limitation, climbing trees with large diameters. These limitations also occur with the twiner’s group that climbs through shoot tips, secondary shoots and petioles. Our sites comparison revealed that the frequency of climbing mechanisms did not change over sites when using a detailed classification, while grouping species in major categories showed a significant result, indicating a difference between sites. So, it is interesting to classify the species as more specific as possible instead of grouping on major categories, to capture these strategies that directly influence species distribution in different environments. It is also important to pay attention on species that combine different climbing mechanisms, developing a secondary mechanism (e.g. adherent roots), which clearly gives them an advantage to firmly attach on their supports.

The three new occurrences for RS State found at FLONA-SFP had their occurrence range expanded towards South Brazil. The species M. dusenii was endemic to Paraná State (PR; Koch et al. 2013KOCH, I., RAPINI, A., KINOSHITA, L.S., SIMõES, A.O. & SPINA A.P. 2013. Apocynaceae. In : Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB4699 (último acesso em 10/Jan/2014)
http://floradobrasil.jbrj.gov.br/jabot/f... ), P. affinis was endemic to Santa Catarina State (SC; Burkart 1979BURKART, A. 1979. Leguminosas Mimosoideas. In Flora Ilustrada Catarinense. (Reitz, P.R., ed.). Herbário Barbosa Rodrigues, Itajaí, p. 1-304.) and M. verticillata was registered for SC, PR, Minas Gerais and Rio de Janeiro States (Marinero et al. 2012MARINERO, F.E.C., WILLIAM, A.R. & CERVI, A.C. 2012. Manettia (Rubiaceae) no estado do Paraná, Brasil. Rodriguésia 63(3):635-647, 10.1590/S2175-78602012000300012.
https://doi.org/10.1590/S2175-7860201200... ). Based on this information we indicate these species to be included in future evaluations of the red list of threatened flora of RS State and Brazil.

As the definition of climber says it has to germinate and always keep contact with soil, some species can be confounded with hemiepiphytes, specifically the root-climber species. In this survey Begonia fruticosa A. DC., Pentacalia desiderabilis(Vell.) Cuatrec. and Griselinia ruscifolia (Clos) Taub. were considered climbers even though they can present a hemiepiphytes/epiphyte habit (Falkenberg & Voltolini 1995FALKENBERG, D.B. & VOLTOLINI, J.C. 1995. The montane cloud forest in southern Brazil. In Tropical Montane cloud forests (Lawrence, S.H., James, O.J. & Scatena, F.N., eds.). Springer, US, p. 138-149., Orihuela & Waechter 2010)ORIHUELA, R.L.L. & J.L, WAECHTER. 2010. Host size and abundance of hemiepiphytes in a subtropical stand of Brazilian Atlantic Forest. J. Trop. Ecol. 26:119-122, 10.1017/S0266467409990496.
https://doi.org/10.1017/S026646740999049... . The first species was always found as a climber, while the second was found a few times as a hemiepiphyte and the latter the majority of times as a hemiepiphyte (personal observation). Other example is Mandevilla atroviolacea (Stadelm.) Woodson, which was found just once with an epiphyte habit but was observed as a climber many times in adjacent areas near FLONA-SFP (i.e. Centro de Proteção e Conservação da Natureza Pró-Mata; personal observation). Another similar issue occurs with scrambler species that can be found at initial growth stages as shrubs or with a prostrate habit. The species Fuchsia regia(Vell.) Munz was found just three times as scrambler at FLONA-SPF, while in adjacent areas (i.e. CPCN Pró-Mata) this is the common habit. The species Mimosa niederleinii Burkart was commonly found as a prostrate herb, but in some cases it clearly climbs the vegetation, scrambling up to three meters of height.

An important issue at FLONA-SFP is the impact of the invasive climbing species Hedera helix L. and Lonicera japonica Thunb. that spreads over the edges and inside of tree plantations, preventing the recruitment and establishment of native species (personal observation). Their management and control is very difficult, being dispersed mainly by birds and may cause in a short time a great loss of habitat for many climbing species. In spite of this threat for climbing diversity, the great amount of forest edges, the unmanaged trees plantations where the understory is not periodically removed, and the Araucaria plantations that provide a high incidence of sunlight in the understory due to its canopy structure, allow a great establishment and development of climbers. These landscape features are only possible since FLONA-SFP is a conservation unit of sustainable use, and future management strategies of tree plantations in the area should consider the impact it may cause in climber species.

Acknowledgments

We are thankful to FAPERGS and CAPES for the scholarship to G.D.S Seger and CNPq for the researcher grant to S.M. Hartz (306816/2010-5); to Instituto de Biociências (UFRGS), Edenice B. S. Avila and the entire team of the São Francisco de Paula National Forest for all logistical support provided; Frediny B. Colla, Elisa V. Salengue and Evelise Bach for field work help; the graphic designer Victória D. Seger for species image treatment; Taís Guimarães for geoprocessing help; all the staff of ICN Herbarium; and the following taxonomists for the help on identifications: Mara R. Ritter, Renato A. Záchia, Martin Grings, Luis F. P. Lima, Silvia T. S. Miotto, Luis R. M. Baptista, João Iganci, Lilian Mentz, Édson L. Soares, Maria Ana Farinaccio, Angelo A. Schneider, Jaqueline Durigon, Priscila P. A. Ferreira, Jorge E. A. Mariath, Leila F. N. Macias, João A. Jarenkow, Cláudio A. Mondin, Rosangela S. Bianchini and Felipe Marinero.

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Publication Dates

  • Publication in this collection
    Dec 2014

History

  • Received
    12 Apr 2014
  • Reviewed
    04 Oct 2014
  • Accepted
    06 Oct 2014
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