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International Journal of Biodiversity Science, Ecosystem Services & Management, 2015 Vol. 11, No. 2, 89–95, http://dx.doi.org/10.1080/21513732.2015.1004196 a b b c d Julia C. Sfair *, André L. C. Rochelle , Juliano van Melis , Andréia A. Rezende , Veridiana de L. Weiser and Fernando R. Martins Departamento de Botânica, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, 1235, Cidade Universitária, Recife, PE, Brazil; Programa de Pós-Graduação em Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas – UNICAMP, Caixa Postal 6109, Campinas, SP 13083-970, Brazil; Departamento de Zoologia e Botânica, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista – UNESP, Rua Cristovão Colombo 2265, São José do Rio Preto, SP 15054-000, Brazil; Departamento de Ciências Biológicas, Faculdade de Ciências, Universidade Estadual Paulista – UNESP, Avenida Eng. Luiz Edmundo Carrijo Coube 14-01, Bauru, SP 17033-360, Brazil (Submitted 13 April 2014; accepted 30 December 2014; edited by James Aronson) Lianas can change forest dynamics, slowing down forest regeneration after a perturbation. In these cases, it may be necessary to manage these woody climbers. Our aim was to simulate two management strategies: (1) focusing on abundant liana species and (2) focusing on the largest lianas, and contrast them with the random removal of lianas. We applied mathematical simulations for liana removal in three different vegetation types in southeastern Brazil: a Rainforest, a Seasonal Tropical Forest, and a Woodland Savanna. Using these samples, we performed simulations based on two liana removal procedures and compared them with random removal. We also used regression analysis with quasi-Poisson distribution to test whether larger lianas were aggressive, i.e., if they climbed into many trees. The procedure of cutting larger lianas was as effective as cutting them randomly and proved not to be a good method for liana management. Moreover, most of the lianas climbed into one or two trees, i.e., were not aggressive. Cutting the most abundant lianas proved to be a more effective method than cutting lianas randomly. This method could maintain liana richness and presumably should accelerate forest regeneration. Keywords: climber; forest disturbance; forest restoration; liana cutting; liana infestation; vine 1. Introduction Liana abundance can in turn change forest dynamics, slowing down forest regeneration after a perturbation, Lianas (woody climbers) are a very abundant growth form and can stall gaps at a low canopy height (Schnitzer in tropical forests, particularly in seasonally dry tropical et al. 2000; Schnitzer & Carson 2010). Where forest forests (Schnitzer 2005; DeWalt et al. 2010). Lianas regeneration in natural areas appears to be jeopardized reduce tree fruit production (Kainer et al. 2006; Fonseca by lianas, it may be necessary to manage these climbers. et al. 2009), inhibit tree growth (Campanello, Garibaldi, et Most studies have focused on economically important al. 2007), and increase tree mortality (Grogan & trees, primarily timber species (Grogan & Landis 2009). Landis 2009; Ingwell et al. 2010). For these reasons, However, cutting lianas considering the forest community most studies focus on the impact lianas exert on particular and dynamics, rather than tree individuals, could accelerate tree species, usually those of some economic importance. forest regeneration. For example, cutting lianas and bam- For example, some studies showed that the liana load boos increases the amount of solar radiation that reaches the decreases the production of Brazilian nut trees (Kainer understory (Campanello, Gatti, et al. 2007), which in turn et al. 2006) and the growth of timber trees (Grogan & increases the mean rate of tree growth (Gerwing 2001)and Landis 2009). contributes to increase the abundance of herbaceous plants, Nevertheless, the importance of lianas is also related to the survival of saplings, and the rates of plant growth in forest disturbance: lianas are more abundant in fragment general (Campanello, Garibaldi, et al. 2007). edges, probably as a consequence of lateral light penetra- Moreover, lianas may play an important role in ecolo- tion and availability of support (Laurance et al. 2001; gical processes, providing arboreal pathways and food for Arroyo-Rodríguez & Toledo-Aceves 2009). This availabil- vertebrates (Emmons & Gentry 1983) and maintaining the ity of light and support also explains why lianas are more diversity of phytophagous beetles (Ødegaard 2000), for abundant (Madeira et al. 2009) and have greater biomass example. In addition, the flowering time of some lianas (Letcher & Chazdon 2009) at intermediate stages of suc- is complementary to that of trees, providing food resources cession. Consequently, the existence of gaps in a forest to pollinators year-round (Morellato & Leitão-Filho 1996). may increase liana density, richness (Schnitzer & Arboreal rodents use lianas as conduits for moving within Carson 2001), and recruitment (Schnitzer et al. 2004). *Corresponding author. Email: email@example.com. © 2015 Taylor & Francis 90 J.C. Sfair et al. the canopy and from the canopy to the ground, and this 20.6ºC, and the mean annual rainfall is 2320 mm. We increases the seed removal rate, i.e., liana density increases surveyed all dead and living plants with perimeter at breast the seed dispersal carried out by arboreal rodents (Kilgore height ≥15 cm and all lianas with stem diameter at breast et al. 2010). Therefore, it is necessary to manage lianas to height (DBH) ≥1 cm (Rochelle 2008; van Melis 2008). lessen the impact on the associated fauna. This area has no evidence of recent large perturbation Different liana management methods can be used to (Rochelle 2008; van Melis 2008). The second site (19° enhance forest regeneration. Most studies propose to ran- 55′–58′ S; 49°31′–32′ W; 400–495 m a.s.l.) is a fragment domly cut all lianas in a plot (Gerwing 2001), which can of 435.73 ha of seasonally dry tropical forest (hereafter be costly (Pérez-Salicrup et al. 2001) and can diminish Seasonal Forest) in the municipality of Paulo de Faria. The liana diversity and carbon stock (Addo-Fordjour climate is Koeppen’s Aw, i.e., hot, humid, tropical, with et al. 2014). Therefore, it is recommended selective liana wet summer and dry winter, with a mean annual tempera- cutting, such as targeting the most abundant species, to ture of 24ºC and a mean annual rainfall of 1245 mm. We maintain liana diversity and ecosystem functioning (Addo- excluded plots with densely tangled lianas, and sampled Fordjour et al. 2013, 2014). In contrast, we simulated two living trees with DBH ≥3 cm and lianas with DBH ≥1cm liana removal procedures, intending to remove as many (Rezende et al. 2007). In the late 1970s, the fragment was lianas as possible while maintaining their species richness. reduced by 30%, and in the mid-1980s, 50 ha was flooded First, we simulated the removal of liana species based on by the construction of a dam. There is no record of their abundance. Focusing on most abundant lianas can be perturbation, such as logging or fire, in this area after advantageous, because rarer species are preserved and the 1981 (Rezende et al. 2007). The third site (22°19′41″– liana richness in a forest decreases only slightly. Second, 21′06″ S; 48°59′49″–49°01′12″ W; 519–603 m a.s.l.) is a we simulated cutting of preferably lianas with larger dia- fragment of 321.71 ha of Woodland Savanna in the muni- meter, which were presumably older and probably had cipality of Bauru. The climate is Koeppen’s Cwa, i.e., hot, already reproduced. These lianas are apparently more with a wet season from September to June and a short dry aggressive as well, i.e., they interconnect many tree season in July and August. The mean annual rainfall is crowns (Vidal et al. 1997). We expected that this second 1331 mm, and the mean annual temperature is 22.6ºC. We procedure would increase the number of trees released sampled all living trees with DBH ≥0.1 cm and all lianas from lianas more efficiently than random cutting, which with stem diameter at soil height ≥0.1 cm (Weiser 2007). removes many lianas attached to a single tree. This area shows signs of cassava plantation (Weiser 2007). Our aim was to simulate these two management stra- In all sites we recorded the trees to which individual lianas tegies: (1) focusing on abundant liana species and (2) were attached and the diameter of each liana, and deter- focusing on the largest lianas, and contrast them with the mined the species identity of lianas and trees according to random removal of lianas. We also aimed to associate the Forzza et al. (2010). largest lianas with the most aggressive ones, assuming that We used these liana and tree data to simulate liana if we focused on the largest and most aggressive lianas, we removal in each site separately. All simulations were made would be able to release more trees in a forest. in the R programming language (version 2.14, R Development Core Team, Vienna, Austria 2011). We simulated two procedures to remove lianas, based on 2. Methods management feasibility. In the first procedure, we simu- lated the removal of lianas based on abundance, eliminat- We sampled lianas and trees rooted within plots at three ing lianas systematically from the most abundant to the different sites (a tropical rain forest, a seasonally dry tropical forest, and a woodland savanna) in the state of rarest species, and quantifying the proportion of individual São Paulo, southeastern Brazil. These sites have different trees without lianas after the removal of the target liana plant formations. Different sampling designs were applied, species. In the second procedure, we simulated the cutting taking into account the characteristics of each community of individual lianas systematically from the thicker to the including average height, diameter, and density of lianas thinner and quantified the proportion of individual trees and trees, and were used to sample adult lianas in each that still had lianas after the removal of the target lianas. vegetation type. For example, adult lianas of woodland Both procedures were compared against the cumulative savanna areas generally have smaller diameter than lianas random removal of lianas, which was performed without of rainforest areas. Therefore, sampling smaller lianas replacement and was repeated 100 times. The first proce- would provide a better analysis of the community in the dure was compared with random removal of liana species; woodland savanna. For each of the three sites, the sampled the second procedure was compared with random removal area was 1 ha. of individual lianas. For each random removal step, we The first site (23°21′54″–59″ S; 45°05′02″–04″ W; calculated the mean and the confidence interval at 95%. 348–394 m a.s.l.) is a tropical rainforest (hereafter We excluded trees that originally did not host lianas from Rainforest) in the municipality of Ubatuba, in the Parque the analysis, since our intention was to examine the pro- Estadual da Serra do Mar, a reserve of 47,500 ha. The portion of trees released from lianas. climate is Af (after Koeppen 1948), i.e., humid tropical In each site, the relationship between the size of a liana with no dry season. The mean annual temperature is and the number of trees it climbed was established using a International Journal of Biodiversity Science, Ecosystem Services & Management 91 regression analysis with quasi-Poisson distribution. This (a) distribution was preferred to Poisson distribution, because our data were underdispersed, i.e., the dispersion para- meter was close to 0.5 (Crawley 2007). The dispersion parameter was calculated by dividing the Pearson’s χ by the degrees of freedom (Crawley 2007). In each site separately, we used the Kolmogorov– 0.1 0.4 0.7 1.0 Smirnov test to compare the liana diameter distribution with a hypothetical uniform diameter distribution. Any (b) deviation from uniform distribution indicates that the sta- tistical distribution of lianas diameters is skewed (Crawley 2007), i.e., most of the lianas have low or large diameter. We sorted each liana individual into classes of aggres- siveness, i.e., the number of trees that one individual liana occupied. The number of lianas in each class of aggres- 0.1 0.4 0.7 1.0 siveness was compared by chi-square test. Regression, (c) Kolmogorov–Smirnov and the chi-square analyses were performed in R programming language (version 2.14, R Development Core Team, Vienna, Austria) and considered each site separately. 3. Results 0.150 0.575 1.000 The Rainforest had 219 species of trees and 66 species of lianas, the Savanna Woodland had 140 species of trees and Proportion of liana species removed 39 species of lianas, and the Seasonal Forest contained 86 Abundance Random species of trees and 45 liana species. The Savanna Woodland showed high density of trees (11,173 trees −1 −1 ha ) and lianas (2793 lianas ha ). The Rainforest had Figure 1. Proportion of trees released from lianas for the three −1 −1 sampled areas: (a) Rainforest, (b) Seasonal Forest, and (c) 1876 trees ha and 526 lianas ha . The Seasonal Forest −1 −1 Woodland Savanna, according to the removal of liana species. had 1416 trees ha and 1427 lianas ha . In the The continuous line represents cutting from the most abundant to Rainforest, 79.7% of the trees did not contain any lianas, the rarest species, and the dots represent random cutting. The whereas in the Seasonal Forest and in the Woodland confidence intervals for the random cutting are very small and Savanna, the percentages of trees without lianas were are not shown. Removing more abundant lianas released more trees than random removal of lianas. 38.5% and 69.3%, respectively. Removing liana species from most abundant to most rare proved to be a better method than removing them randomly for the three sites (Figure 1). For example, sites were thin: Rainforest (D =1; P < 0.01; Figure 4), when we removed 50% of the most abundant lianas in the Seasonal Forest (D =1; P < 0.01; Figure 4), and Rainforest, fewer trees with lianas remained than when we Woodland Savanna (D = 0.35; P < 0.01; Figure 4). removed lianas randomly (Figure 1). If the intention is to The regression analysis with quasi-Poisson distribution remove 50% of the lianas, we can focus on few and indicated that larger lianas occupied more trees than smal- ler lianas in the Rainforest (t = 8.08; P < 0.01) and in the dominant species (about seven in the Rainforest and four Woodland Savanna (t = 24.07; P < 0.01), but not in the in the Seasonal Forest and Woodland Savanna, Figure 2). Seasonal Forest (t = 0.36; P = 0.72). Moreover, most of The most abundant lianas were Adenocalymma comosum −1 the lianas was not aggressive and climbed few trees in the (Cham.) DC. (Bignoniaceae; 61 individuals ha or 10.93% Rainforest (χ = 1863.2; d.f. = 5; P < 0.01), in the of all individual lianas) in the Rainforest; Dolichandra Seasonal Forest (χ = 2885.3; d.f. = 5; P < 0.01), and in quadrivalvis (Jacq.) L.G.Lohmann (Bignoniaceae; 188 indi- −1 the Woodland Savanna (χ = 5691.3; d.f. = 5; P < 0.01; viduals ha or 13.17% of all individuals) in the Seasonal Figure 5). Forest; and Serjania lethalis A.St.-Hil. (Sapindaceae; 420 −1 individuals ha or 15.03% of all individuals) in the Woodland Savanna. 4. Discussion The resulting number of trees without lianas was simi- lar when the removal procedure focused on large lianas To reduce the overall costs, Vidal et al. (1997) suggested and when it was carried out randomly. This result was cutting lianas based on aggressiveness, i.e. lianas climbing consistent for all three sites (Figure 3). The Kolmogorov– many trees, being on tree crown or trunk. Nevertheless, Smirnov test indicated that most of the lianas in all three our results indicate that, considering the size of lianas and Proportion of trees with lianas 0.0 0.5 1.0 0.0 0.5 1.0 0.0 0.5 1.0 92 J.C. Sfair et al. (a) (a) 1.0 0.8 0.6 0.4 0.2 0.0 010 20 30 40 (b) (b) 1.0 0.8 0.6 0.4 0.2 0.0 0 1020304050 (c) (c) 1.0 0.8 0.6 0.4 0.2 0.0 Diameter of lianas (cm) 0 10203040 Number of liana species removed Size Random Figure 2. Proportion of trees released after cutting lianas spe- cies for (a) Rainforest, (b) Seasonal Forest, and (c) Woodland Figure 3. Proportion of trees with lianas after cutting lianas Savanna. from thicker to thinner for (a) Rainforest, (b) Seasonal Forest, Cutting the most abundant species released most of the trees. The and (c) Woodland Savanna. horizontal line represents 50% of trees released from lianas. The continuous line represents cutting from the thickest to the thinnest lianas and the dashed line represents random cutting. The confidence intervals for the random cutting are very small the number of trees to which they are attached, cutting the and are not shown. Removing larger lianas procedure is similar to random removal of lianas on occupied trees. aggressive lianas would not be a good procedure. In fact, in the Seasonal Forest, there was no relationship between liana size and the number of trees climbed by one liana. Based on our consistent results for three different vegeta- leading to different liana species dominance after manage- tion types, we recommend the procedure that performed ment (Addo-Fordjour et al. 2014). Liana diversity recovers better than random removal, i.e., cutting lianas from the in long term (Addo-Fordjour et al. 2013, 2014), indicating most abundant to the rarest species. We speculate that that liana management may take long cycles of cutting removing abundant lianas would not drive liana species (e.g., more than 40 years as indicated in a tropical forest in to local extinction, given that some individuals – primarily Malaysia (Addo-Fordjour et al. 2014)). Nevertheless, con- the slenderest ones – are often missed (Pérez-Salicrup tinuous monitoring of liana abundance is recommended by et al. 2001). In addition, many lianas reproduce clonally, Addo-Fordjour et al. (2013) to control proliferation. a trait that may be associated with high disturbance We hypothesize that trees released from lianas could regimes such as gaps (Gerwing & Uhl 2002): after a grow faster (Campanello, Garibaldi, et al. 2007), increase disturbance, lianas may fall from their hosts and grow biomass and carbon gain (van der Heidjen & new roots (Nabe-Nielsen & Hall 2002). Moreover, canopy Phillips 2009), have increased survival probability openings would favor seed germination, including that of (Grogan & Landis 2009), and produce more fruits liana seeds (Gerwing 2006). Although the response to (Kainer et al. 2006) compared to trees with lianas. These logging varies according to the liana species in ways effects could be more important in slow-growing trees, related to reproduction (Gerwing 2006), different lianas which generally have more lianas than do pioneer species species are able to reproduce vigorously after cutting, (Putz 1980, 1984; Campanello, Garibaldi, et al. 2007). In Proportion of trees with lianas 0.0 0.5 1.0 0.0 0.5 1.0 0.0 0.5 1.0 Proportion of trees with lianas 0.0 0.5 1.0 0.0 0.5 1.0 0.0 0.5 1.0 International Journal of Biodiversity Science, Ecosystem Services & Management 93 (a) (a) 1 2 3 4 5 6 or + (b) (b) 1 2 3 4 5 6 or + (c) (c) 1 2 3 4 5 6 or + Class of aggressiveness Figure 5. Proportion of lianas in each class of aggressiveness, i.e., the number of trees climbed by lianas in the (a) Rainforest, (b) Seasonal Forest, and (c) Woodland Savanna. Most of the lianas climbed one or two trees. Figure 4. Boxplot for liana diameter distribution for the (a) Rainforest, (b) Seasonal Forest, and (c) Woodland Savanna. From bottom to top: the smallest diameter, lower quartile, med- ian, upper quartile, and largest diameter. In this study, we have provided a theoretical model for liana management. Empirical works have previously pro- posed random cutting of all lianas in a plot addition, liana abundance can be related to forest succes- (Gerwing 2001), a procedure that decreases liana abun- sion: lianas can be more abundant at the intermediate dance when compared to control plots (Gerwing & stages of succession, in which both support and light are Vidal 2002). The method we propose reduces the impact available (Madeira et al. 2009). A well-structured forest, of liana removal on community, for it focuses only on the with tall trees and a closed canopy, also has few lianas due most abundant species, avoiding the removal of all lianas. to the shady environment (Madeira et al. 2009). In liana- The suggestion to cut abundant, primarily dominant lianas dominated patches, the successional transition to a higher may be applied to at least three different types of vegeta- forest occurs very slowly (Gerwing 2001). Therefore, liana tion: rainforest, seasonal dry tropical forests, and wood- cutting could eventually accelerate a well-structured forest land savanna. Future research should evaluate the formation. In fact, 20 years after liana cutting, the density applicability of this method to other types of vegetation, of tree saplings and seedlings was higher than untreated as well its costs and feasibility. forest in a tropical forest in Malaysia (Addo-Fordjour et al. 2013). However, cutting lianas may lead to another consequence: lianas may fall, killing tree seedlings and saplings, and providing fuel for fires (Gerwing 2001; Acknowledgements Pérez-Salicrup 2001). This effect would alter forest regen- We thank Monica Martins for reviewing the English, Bruno eration by decreasing recruitment of tree species. In addi- Aranha for helping with R programming language, Robyn Burnham for her review of the English and her comments on tion, cutting may release some amount of atmospheric the text, Hock Keong Lua for his helpful comments on liana carbon, which may take long to be stocked as liana management, and the two reviewers for important suggestions. woody biomass (Addo-Fordjour et al. 2014). Empirical We also thank T. Lewinsohn, P.R. Guimarães Jr, M. Almeida- researches should test the balance of the positive and Neto, F. Maluf, and F.N. Ramos for reviewing the manuscript negative effects of liana removal to forest dynamics. and making useful suggestions. Diameter (cm) 024 06 3 Proportion of lianas 0.0 0.4 0.8 0.00 0.35 0.70 0.00 0.35 0.70 94 J.C. Sfair et al. and mortality on Barro Colorado Island, Panama. J Ecol. Funding 98:879–887. 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International Journal of Biodiversity Science, Ecosystem Services & Management – Taylor & Francis
Published: Apr 3, 2015
Keywords: climber; forest disturbance; forest restoration; liana cutting; liana infestation; vine
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