Climbing plants of Porto Ferreira State Park , southeastern Brazil

A floristic survey of climbing plants was carried out in an ecotone area of seasonal semideciduous forest (SSF) and forested savanna (CER), in Porto Ferreira State Park (PFSP), Southeastern Brazil. We sampled the reproductive specimens every month during two periods, March 2010 to September 2011 and April and July 2015. The surveys were performed by the walking method, and the sampled individuals were classified by habit, climbing mechanism and dispersal mode. Overall, 109 species, belonging to 67 genera and 29 families, were recorded; 49 species occurred in both, 29 and 31 were exclusive to SSF and CER, respectively. Bignoniaceae and Malpighiaceae were the richest families, with 17 species, followed by Sapindaceae (12 species), Asteraceae and Apocynaceae (8 species each) and Fabaceae (6). The majority of climbers were lianas, twining and anemochoric species, corresponding to 70%, 47% and 66% of all samples, respectively. In this work, we added one new family and 14 species to the Cerrado’s list of climbing plants from São Paulo state, and 10 species to the Brazilian seasonal semideciduous forest’s list. Therefore, we contributed to the understanding of diversity of climbing plants in vegetation types poorly studied for this plant group, mainly in the Cerradão, wherein we found new records for several species.


Introduction
Climbing plants germinate and remain on the ground, requiring external mechanical sustentation provided by others plants for access to light in the forest canopy (Darwin 1867;Putz & Windsor 1987;Gerwing et al. 2006;Lawdig & Meiners 2010;van der Heijden et al. 2013).These plants occur in many climates and vegetation types, representing up to 25% of plant diversity in some tropical forests (Gentry 1991;Engel et al. 1998;Pérez Salicrup et al. 2001).Besides climbing plants playing an important role in biodiversity maintenance, they establish competition for resources with the host tree (phorophyte), and can change dynamic and natural regeneration in different biomes (Laurence et al. 2001;Schnitzer & Bongers 2002).
Porto Ferreira State Park has been the subject of numerous floristic surveys (Bertoni & Martins 1987;Bertoni et al. 2001;Colli et al. 2003;Oliveira 2012;Osaco 2012;Sabino 2013;Marcusso et al. 2016); however, studies on climbing plants have not been performed in this area.The main objective of this study was to survey the climbing flora of an ecotone area, between seasonal semideciduous forest and forested savanna (Cerradão), in Porto Ferreira State Park, São Paulo, Southeastern Brazil.

Study site
Porto Ferreira State Park (PFSP) is located in the municipality of Porto Ferreira, in São Paulo state, Southeastern Brazil (Figure 1).The study area is 611.55 hectares, and has altitudinal variation between 540 and 608 m.a.s.l.(São Paulo 2003).PFSP is located in a geomorphological region of peripheral depression, in the central region of the watershed of Mogi-Guaçu River (São Paulo 2003).
The climate of the region is classified as Aw, according to Köeppen's classification (Bertoni & Martins 1987).The annual mean temperature is 22.3 °C and the annual mean precipitation is 1.497 mm, presenting variation between the rainy (247.9 mm) and dry seasons (26.6 mm) (CEPAGRI 2016).
PFSP has distinct vegetation types according to IBGE (2012), presenting forested savanna (Cerradão) and seasonal semideciduous forest.They are mainly differentiated in the field by their physiognomy (small average height and high density in the Cerradão), and greater average height and lower density in Semideciduous forests), ecological aspects (soil types, deciduousness) and typical and exclusive species of each vegetation type (Durigan et al. 2012).Furthermore, there are ecotonal areas among these vegetation types (Osaco 2012;Sabino 2013), in which a floristic mixture and phytophysiognomic indistinguishability occurs (IBGE 2012).

Data collection
Climbing plants sampling was performed by the walking method (Filgueiras et al. 1994), every month between March 2010 and September 2011.According to Morellato et al. (1996), transitional and final periods between climatic seasons can be related to the flowering and fruiting peaks of climbing plants, especially of the families most abundant in species.In this way, aiming to improve the sample, we performed additional floristic surveys in April and July 2015.The reproductive specimens collected in the field were processed and herborized following the protocols of Fidalgo & Bononi (1984).The vouchers were incorporated in the Herbarium Rioclarense (HRCB).Taxonomic identity was determined through specialized literature, direct comparison with identified specimens in HRCB's collection and by expert taxonomists (cited in the acknowledgements).Synonyms were verified by BFG (2015), and we adopted APG IV (2016) to classify the botanical families.
In this study, we have registered one new family and 14 species for the Cerrado list, and 10 species for the seasonal semideciduous forest list (Table 1).

Discussion
The present study showed elevated richness of climbing plants in Cerradão, compared to other studies carried out in Cerrado sensu stricto in São Paulo state, where 41 (Mantovani & Martins 1993) and 15 species (Weiser & Godoy 2001) were recorded.On the other hand, in a Cerradão in Bauru, 52 species of climbers were recorded (Weiser 2007), corroborating our results that the Cerradão is richer in climbing plants than Cerrado sensu stricto.Although these studies had different sample time spans, the richness recorded in the present study can be considered high by the fact that the studies carried out in Cerrado sensu stricto had very similar sample times to ours (16 to 22 months, Mantovani & Martins 1993;Weiser & Godoy 2001, respectively), while the study in Cerradão considered a much larger sample time (51 months, Weiser 2007).However, the last considered a smaller area than the present study (1 versus 169 hectares, respectively).In this way, it is likely that other Cerradão areas are as rich in this vegetation type as that recorded in the present study.
Otherwise, the number of species found in Seasonal Semideciduous Forest can be considered low compared to the average for this vegetation type (e.g.Morellato & Leitão-Filho 1998;Udulutsch et al. 2004;Rezende & Ranga 2005;Tibiriçá et al. 2006;Carneiro & Vieira 2012).However, we did not sample months with the same frequency, as we collected one more time during transitional months and those at the end of the climatic season (rainy and dry season), and these reproductive periods are considered the peak of flowering and fruiting for climbing plants (Morellato & Leitão-Filho 1996).This was also the case in the study of Udulutsch et al. (2010), so much that these surveys showed a similar number of species (74 species) to the present study (78 species).Furthermore, floristic surveys are usually carried out for different time spans and in areas with different sizes, which compromises comparisons of diversity and the relationships between flora of different sites (e.g.Forzza et al. 2014).In this way, we suggest that floristic studies are made considering equal sample frequency during the year, considering the reproductive stages of the plants.Therefore, it may be that the Seasonal Semideciduous Forest of PFSP is so rich as those in other studies which have reported high values for richness (e.g.Morellato & Leitão-Filho 1998; Udulutsch et al. 2004;Tibiriçá et al. 2006).
In general, the reasonably substantial number of climbing plant species recorded in this study is perhaps associated with the ecotonal condition of this area, where the floristic elements of both vegetation types (seasonal semideciduous forest and Cerradão) contribute to the richness.Although for climbing plants this aspect is poorly known, this has already been documented for vascular epiphytes (e.g.Kersten 2010;Bonnet et al. 2011;Marcusso & Monteiro 2016) and trees (e.g.Pinheiro & Monteiro 2008).This elevated richness and abundance of species in an ecotone is related to the meeting of adjacent areas, and thus encompasses the diversity of the community around it (Odum 1969;Kent et al. 1997;Kark 2012).This transitional area shares environmental conditions but also establishes the particular conditions of an ecotone, allowing coexistence of species from the surrounding vegetation, as well as rare and endemic species (Kark & Rensburg 2006;Kark 2012).
We found a prevalence of lianas in the study area.Although an equal proportion of lianas and herbaceous climbing plants is expected in tropical forests (Gentry & Dodson 1987;Gentry 1991;Durigon et al. 2009), studies of climbing plants realized in semideciduous forest found 64% (Udulutsch et al. 2004) and 60% (Vargas et al. 2013) lianas, contradicting this estimation.On the other hand, herbaceous vines can represent almost 85% of the richness in subtropical and temperate forests (Durigon et al. 2014).
The pattern of climbing mechanism registered for tropical forests was corroborated in this study, wherein twining was the predominant mechanism, followed by tendril climbing (e.g.Gentry 1991;Araujo & Alves 2010;Vivek & Parthasarathy 2015).Despite some species having specialized structures to assist in colonization of the phorophyte, such as tendrils modified with adhesive pads and hooks, improving their colonization success (Gentry 1979;Lohmann 2006), this climbing mechanism has not been the most encountered in tropical forests (Gentry 1991).In this study, we recorded Scleria latifolia and Senegalia polyphylla with a twining habit.In general, these species are not included in climbing plant floristic surveys, but in PFSP these species were observed with this growth mode; perhaps they use scabrous and thorn features to ascend in the phorophyte.
In general, anemochory (72 species) was the most commonly found dispersal mode among climbing plants (lianas + herbaceous vines) (Durigon & Waechter 2011;Gallagher et al. 2011;Vargas et al. 2013), which is associated with environments with pronounced climatic seasonality (Dewalt et al. 2010;Schnitzer & Bongers 2011).According to Morellato & Leitão-Filho (1996), the pattern of dispersion can be considered complementary in forest phenology, wherein in periods with a smaller amount of annual precipitation, the tree community totally or partially loses its leaves (Montovani & Martins 1998), and climbing plants can use wind currents to disperse their seeds (Morellato & Leitão-Filho 1998).Although, when considering only herbaceous vines, this relation can be altered by the predominance of zoochory, thus their fruits mature during the rainy season (Morellato & Leitão-Filho 1996).
Despite floristic inventories of climbing plants increasing, they are concentrated in semideciduous forest (e.g.Hora & Soares 2002;Tibiriçá et al. 2006;Rezende et al. 2007;Udulutsch et al. 2010;Vargas et al. 2013), to the detriment of those realized in the Cerrado (Weiser & Godoy 2001;Weiser 2007;Oliveira et al. 2014).However, this study included new registers of species for both vegetation types.This is because climbing plants comprise a very diverse group, so much so that they are considered key to innovation throughout evolution, increasing angiosperm diversity (Gianoli 2015;Gianoli et al. 2016).For this reason, we highlight the importance of including climbing plants in community research (Durigon et al. 2014;Schnitzer et al. 2015), and realizing floristic inventories that include or integrate climbing plants.
The present study reveals the considerable richness of this sinusia in Porto Ferreira State Park, with a similar number of species between the vegetation types.The mainly contribution is relation to diversity, recorded species, like Scleria latifolia and Senegalia polyphylla, as climbing plants.Both to vegetation types showed new records to the climbing plants checklist.Thus, we encourage the initiatives of floristic surveys with climbing plants, with similar frequency of sample, in these vegetation types, mainly in the Cerradão, in view of the importance of its floristic richness and to filling out the remaining gaps.

Figure 1 .
Figure 1. A. Brazilian Atlantic Forest and the Cerrado and the location of São Paulo state; B. location of Porto Ferreira State Park; C. Porto Ferreira State Park and the main vegetation types studied.