Abstract
Young successional tropical forests are crucial in the global carbon cycle because they can quickly sequester large quantities of atmospheric carbon. However, lianas (woody vines) can significantly decrease biomass accumulation in young regenerating forests. Lianas are abundant in tropical dry forests, and thus we hypothesized that lianas reduce biomass accretion in dry forests. Lianas may be particularly detrimental to the growth of young trees, which are vulnerable to competition from lianas. Alternatively, lianas may have a stronger negative effect on the largest trees because lianas seek the high-light environment at the top of the forest canopy. We tested these hypotheses using a liana-removal experiment in 13 dry forest stands that ranged from 1 to 70 years in southwestern Panama. We measured biomass accumulation annually for more than 10,000 stems from 2013 to 2017. Contrary to our expectations, liana removal had no effect on tree biomass accumulation across our successional forests and throughout our study period. Liana removal did not benefit smaller trees or larger trees. Lianas did not increase biomass accumulation on recruits, and did not increase biomass loss due to mortality. Surprisingly, removing lianas had a negative effect on three out of 41 tree species. Lianas had no effect on biomass accumulation and loss, possibly because: (1) trees allocated resources to roots instead of stems, (2) trees and lianas partitioned water, (3) higher irradiance after liana removal reduced soil moisture, or (4) low water availability might have been such a strong stressor that it reduced plant–plant competition.




Similar content being viewed by others
References
Aide TM, Clark ML, Grau HR, López-Carr D, Levy MA, Redo D, Bonilla-Moheno M, Riner G, Andrade-Núñez MJ, Muñiz M (2013) Deforestation and reforestation of Latin America and the Caribbean (2001–2010). Biotropica 45:262–271. https://doi.org/10.1111/j.1744-7429.2012.00908.x
Baccini A, Goetz SJ, Walker WS, Laporte NT, Sun M, Sulla-Menashe D, Hackler J, Beck PSA, Dubayah R, Friedl MA, Samanta S, Houghton RA (2012) Estimated carbon dioxide emissions from tropical deforestation improved by carbon-density maps. Nature Clim Change 2:182–185. https://doi.org/10.1038/nclimate1354
Barker MG, Pérez-Salicrup D (2000) Comparative water relations of mature mahogany (Swietenia macrophylla) trees with and without lianas in a subhumid, seasonally dry forest in Bolivia. Tree Physiol 20:1167–1174. https://doi.org/10.1093/treephys/20.17.1167
Barry KE, Schnitzer SA, van Breugel M, Hall JS (2015) Rapid liana colonization along a secondary forest chronosequence. Biotropica 47:672–680. https://doi.org/10.1111/btp.12259
Bartoń K (2013) Package “MuMIn”: multi-model inference. R Pack Vers 1(9):13
Becknell JM, Kissing Kucek L, Powers JS (2012) Aboveground biomass in mature and secondary seasonally dry tropical forests: A literature review and global synthesis. For Ecol Manage 276:88–95. https://doi.org/10.1016/j.foreco.2012.03.033
Brouwer R (1963) Some aspects of the equilibrium between overground and underground plant parts. Jaarboek Instit Biol Scheikun Onderz Landbouwgewassen 1963:31–39
Brown S, Lugo AE (1982) The storage and production of organic matter in tropical forests and their role in the global carbon cycle. Biotropica 14:161–187. https://doi.org/10.2307/2388024
Caughlin TT, Rifai SW, Graves SJ, Asner GP, Bohlman SA (2016) Integrating LiDAR-derived tree height and Landsat satellite reflectance to estimate forest regrowth in a tropical agricultural landscape. Remote Sens Ecol Conserv 2:190–203. https://doi.org/10.1002/rse2.33
César RG, Holl KD, Girão VJ, Mello FNA, Vidal E, Alves MC, Brancalion PHS (2016) Evaluating climber cutting as a strategy to restore degraded tropical forests. Biol Conserv 201:309–313. https://doi.org/10.1016/j.biocon.2016.07.031
César RG, Rother DC, Brancalion PHS (2017) Early response of tree seed arrival after liana cutting in a disturbed tropical forest. Trop Conserv Sci 10:1–7. https://doi.org/10.1177/1940082917723586
Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366. https://doi.org/10.1111/j.1461-0248.2009.01285.x
Chave J, Réjou-Méchain M, Búrquez A, Chidumayo E, Colgan MS, Delitti WBC, Duque A, Eid T, Fearnside PM, Goodman RC, Henry M, Martínez-Yrízar A, Mugasha WA, Muller-Landau HC, Mencuccini M, Nelson BW, Ngomanda A, Nogueira EM, Ortiz-Malavassi E, Pélissier R, Ploton P, Ryan CM, Saldarriaga JG, Vieilledent G (2014) Improved allometric models to estimate the aboveground biomass of tropical trees. Glob Change Biol 20:3177–3190. https://doi.org/10.1111/gcb.12629
Chazdon RL, Letcher SG, van Breugel M, Martínez-Ramos M, Bongers F, Finegan B (2007) Rates of change in tree communities of secondary Neotropical forests following major disturbances. Philo Trans R Soc 362:273–289. https://doi.org/10.1098/rstb.2006.1990
Chazdon RL, Broadbent EN, Rozendaal DMA, Bongers F, Zambrano AMA, Aide TM, Balvanera P, Becknell JM, Boukili V, Brancalion PHS, Craven D, Almeida-Cortez JS, Cabral GAL, de Jong B, Denslow JS, Dent DH, DeWalt SJ, Dupuy JM, Durán SM, Espírito-Santo MM, Fandino MC, César RG, Hall JS, Hernández-Stefanoni JL, Jakovac CC, Junqueira AB, Kennard D, Letcher SG, Lohbeck M, Martínez-Ramos M, Massoca P, Meave JA, Mesquita R, Mora F, Muñoz R, Muscarella R, Nunes YRF, Ochoa-Gaona S, Orihuela-Belmonte E, Peña-Claros M, Pérez-García EA, Piotto D, Powers JS, Rodríguez-Velazquez J, Romero-Pérez IE, Ruíz J, Saldarriaga JG, Sanchez-Azofeifa A, Schwartz NB, Steininger MK, Swenson NG, Uriarte M, van Breugel M, van der Wal H, Veloso MDM, Vester H, Vieira ICG, Bentos TV, Williamson GB, Poorter L (2016) Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics. Sci Adv 2:e1501639. https://doi.org/10.1126/sciadv.1501639
Chen Y-J, Bongers F, Cao K-F, Cai Z-q (2008) Above- and below-ground competition in high and low irradiance: tree seedling responses to a competing liana Byttneria grandifolia. J Trop Ecol 24:517–524. https://doi.org/10.1017/S0266467408005233
Dewalt SJ, Schnitzer SA, Denslow JS (2000) Density and diversity of lianas along a chronosequence in a central Panamanian lowland forest. J Trop Ecol 16:1–19. https://doi.org/10.1017/S0266467400001231
DeWalt SJ, Schnitzer SA, Chave J, Bongers F, Burnham RJ, Cai Z, Chuyong G, Clark DB, Ewango CEN, Gerwing JJ, Gortaire E, Hart T, Ibarra-Manríquez G, Ickes K, Kenfack D, Macía MJ, Makana J-R, Martínez-Ramos M, Mascaro J, Moses S, Muller-Landau HC, Parren MPE, Parthasarathy N, Pérez-Salicrup DR, Putz FE, Romero-Saltos H, Thomas D (2010) Annual rainfall and seasonality predict pan-tropical patterns of liana density and basal area. Biotropica 42:309–317. https://doi.org/10.1111/j.1744-7429.2009.00589.x
Dillenburg LR, Whigham DF, Teramura AH, Forseth IN (1993a) Effects of below- and aboveground competition from the vines Lonicera japonica and Parthenocissus quinquefolia on the growth of the tree host Liquidambar styraciflua. Oecologia 93:48–54. https://doi.org/10.1007/bf00321190
Dillenburg LR, Whigham DF, Teramura AH, Forseth IN (1993b) Effects of vine competition on availability of light, water, and nitrogen to a tree host (Liquidambar styraciflua). Am J Bot 80:244–252. https://doi.org/10.2307/2445347
Estrada-Villegas S, Schnitzer SA (2018) A comprehensive synthesis of liana removal experiments in tropical forests. Biotropica 50:729–739. https://doi.org/10.1111/btp.12571
Estrada-Villegas S, Bailón M, Hall JS, Schnitzer SA, Turner BL, Caughlin T, van Breugel M (2019) Edaphic factors and initial conditions influence successional trajectories of early regenerating tropical dry forests. J Ecol 180:160–174. https://doi.org/10.1111/1365-2745.13263
Estrada-Villegas S, Hall JS, van Breugel M, Schnitzer SA (2020) Lianas reduce biomass accumulation in early successional tropical forests. Ecology. https://doi.org/10.1002/ecy.2989
FAO (2015) Global forest resources assessment 2015: how are the world’s forests changing?, Rome
Fisher RA (1921) Some remarks on the methods formulated in a recent article on “The Quantitative Qnalysis of Plant Growth.” Ann Appl Biol 7:367–372. https://doi.org/10.1111/j.1744-7348.1921.tb05524.x
Gałecki A, Burzykowski T (2013) Linear mixed-effects models using R: a step-by-step approach. Springer Science and Business Media, New York
Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873. https://doi.org/10.1002/sim.3107
Grime JP (2002) Plant strategies, vegetation processes, and ecosystem properties. John Wiley and Sons, New York
Griscom HP, Griscom BW, Ashton MS (2009) Forest regeneration from pasture in the dry tropics of panama: effects of cattle, exotic grass, and forested Riparia. Restor Ecol 17:117–126. https://doi.org/10.1111/j.1526-100X.2007.00342.x
Griscom HP, Connelly AB, Ashton MS, Wishnie MH, Deago J (2011) The structure and composition of a tropical dry forest landscape after land clearance; Azuero Peninsula, Panama. J Sustainable For 30:756–774. https://doi.org/10.1080/10549811.2011.571589
Grogan J, Landis RM (2009) Growth history and crown vine coverage are principal factors influencing growth and mortality rates of big-leaf mahogany Swietenia macrophylla in Brazil. J Appl Ecol 46:1283–1291. https://doi.org/10.1111/j.1365-2664.2009.01720.x
Heckadom-Moreno S (1984) Panama's expanding cattle front: the Santeño campesinos and the colonization of the forests. Doctoral dissertation, University of Essex, UK
Holdridge LR (1964) Life zone ecology. Centro Científico Tropical San José (Costa Rica)
Ingwell LL, Joseph Wright S, Becklund KK, Hubbell SP, Schnitzer SA (2010) The impact of lianas on 10 years of tree growth and mortality on Barro Colorado Island, Panama. J Ecol 98:879–887. https://doi.org/10.1111/j.1365-2745.2010.01676.x
Jakovac ACC, Bentos TV, Mesquita RCG, Williamson GB (2014) Age and light effects on seedling growth in two alternative secondary successions in central Amazonia. Plant Ecol Diver 7:349–358. https://doi.org/10.1080/17550874.2012.716088
Kuzee ME, Bongers F (2005) Climber abundance, diversity and colonisation in degraded forests of different ages in Côte d’Ivorie. In: Bongers F, Parren MPE, Traoré D (eds) Forest climbing plants of west Africa: diversity, ecology and management. Cabi Publishing, Oxford, pp 73–88
Lai HR, Hall JS, Turner BL, van Breugel M (2017) Liana effects on biomass dynamics strengthen during secondary forest succession. Ecology 98:1062–1070. https://doi.org/10.1002/ecy.1734
Lebrija-Trejos E, Pérez-García EA, Meave JA, Poorter L, Bongers F (2011) Environmental changes during secondary succession in a tropical dry forest in Mexico. J Trop Ecol 27:477–489. https://doi.org/10.1017/S0266467411000253
Letcher SG (2015) Patterns of liana succession in tropical forests. In: Schnitzer SA, Bongers F, Burnham RJ, Putz FE (eds) Ecology of lianas. John Wiley and Sons, Oxford, pp 116–130
Letcher SG, Chazdon RL (2009) Lianas and self-supporting plants during tropical forest succession. For Ecol Manage 257:2150–2156. https://doi.org/10.1016/j.foreco.2009.02.028
Murphy PG, Lugo AE (1986) Ecology of tropical dry forest. Annu Rev Ecol Syst 17:67–88. https://doi.org/10.1146/annurev.es.17.110186.000435
Pérez-Salicrup DR (2001) Effect of liana cutting on tree regeneration in a liana forest in Amazonian Bolivia. Ecology 82:389–396. https://doi.org/10.2307/2679867
Pérez-Salicrup DR, Barker MG (2000) Effect of liana cutting on water potential and growth of adult Senna multijuga (Caesalpinioideae) trees in a Bolivian tropical forest. Oecologia 124:469–475. https://doi.org/10.1007/pl00008872
Pinheiro J, Bates D, DebRoy S, Sarkar D (2018) nlme: linear and nonlinear mixed effects models. R package version 3.1–137
Poorter H, Jagodzinski AM, Ruiz-Peinado R, Kuyah S, Luo Y, Oleksyn J, Usoltsev VA, Buckley TN, Reich PB, Sack L (2015) How does biomass distribution change with size and differ among species? An analysis for 1200 plant species from five continents. New Phytol 208:736–749. https://doi.org/10.1111/nph.13571
Poorter L, Bongers F, Aide TM, Almeyda Zambrano AM, Balvanera P, Becknell JM, Boukili V, Brancalion PHS, Broadbent EN, Chazdon RL, Craven D, de Almeida-Cortez JS, Cabral GAL, de Jong BHJ, Denslow JS, Dent DH, DeWalt SJ, Dupuy JM, Durán SM, Espírito-Santo MM, Fandino MC, César RG, Hall JS, Hernandez-Stefanoni JL, Jakovac CC, Junqueira AB, Kennard D, Letcher SG, Licona J-C, Lohbeck M, Marín-Spiotta E, Martínez-Ramos M, Massoca P, Meave JA, Mesquita R, Mora F, Muñoz R, Muscarella R, Nunes YRF, Ochoa-Gaona S, de Oliveira AA, Orihuela-Belmonte E, Peña-Claros M, Pérez-García EA, Piotto D, Powers JS, Rodríguez-Velázquez J, Romero-Pérez IE, Ruíz J, Saldarriaga JG, Sanchez-Azofeifa A, Schwartz NB, Steininger MK, Swenson NG, Toledo M, Uriarte M, van Breugel M, van der Wal H, Veloso MDM, Vester HFM, Vicentini A, Vieira ICG, Bentos TV, Williamson GB, Rozendaal DMA (2016) Biomass resilience of Neotropical secondary forests. Nature 530:211–214. https://doi.org/10.1038/nature16512
Reid JP, Schnitzer SA, Powers JS (2015) Short and long-term soil moisture effects of liana removal in a seasonally moist tropical forest. PLoS ONE 10:e0141891. https://doi.org/10.1371/journal.pone.0141891
Rodríguez-Ronderos ME, Bohrer G, Sanchez-Azofeifa A, Powers JS, Schnitzer SA (2016) Contribution of lianas to plant area index and canopy structure in a Panamanian forest. Ecology 97:3271–3277. https://doi.org/10.1002/ecy.1597
Schnitzer SA (2005) A mechanistic explanation for global patterns of liana abundance and distribution. Am Nat 166:262–276. https://doi.org/10.1086/431250
Schnitzer SA (2015) Increasing liana abundance in neotropical forests: causes and consequences. In: Schnitzer SA, Bongers F, Burnham RJ, Putz FE (eds) Ecology of lianas. John Wiley and Sons, Oxford, pp 451–464
Schnitzer SA, Bongers F (2011) Increasing liana abundance and biomass in tropical forests: emerging patterns and putative mechanisms. Ecol Lett 14:397–406. https://doi.org/10.1111/j.1461-0248.2011.01590.x
Schnitzer SA, Carson WP (2010) Lianas suppress tree regeneration and diversity in treefall gaps. Ecol Lett 13:849–857. https://doi.org/10.1111/j.1461-0248.2010.01480.x
Schnitzer SA, van der Heijden GMF (2019) Lianas have a seasonal growth advantage over co-occurring trees. Ecology 100:e02655. https://doi.org/10.1002/ecy.2655
Schnitzer SA, Kuzee ME, Bongers F (2005) Disentangling above- and below-ground competition between lianas and trees in a tropical forest. J Ecol 93:1115–1125. https://doi.org/10.1111/j.1365-2745.2005.01056.x
Schnitzer SA, Rutishauser S, Aguilar S (2008) Supplemental protocol for liana censuses. For Ecol Manage 255:1044–1049. https://doi.org/10.1016/j.foreco.2007.10.012
Schnitzer SA, van der Heijden GMF, Mascaro J, Carson WP (2014) Lianas in gaps reduce carbon accumulation in a tropical forest. Ecology 95:3008–3017. https://doi.org/10.1890/13-1718.1
Smith-Martin CM, Bastos CL, Lopez OR, Powers JS, Schnitzer SA (2019) Effects of dry-season irrigation on leaf physiology and biomass allocation in tropical lianas and trees. Ecology 100:e02827. https://doi.org/10.1002/ecy.2827
Smith-Martin CM, Xu X, Medvigy D, Schnitzer SA, Powers JS (2020) Allometric scaling laws linking biomass and rooting depth vary across ontogeny and functional groups in tropical dry forest lianas and trees. New Phytol 226:714–726. https://doi.org/10.1111/nph.16275
Toledo-Aceves T (2015) Above- and belowground competition between lianas and trees. In: Schnitzer SA, Bongers F, Burnham RJ, Putz FE (eds) Ecology of lianas. John Wiley and Sons, Oxford, pp 147–163
van Breugel M, Martínez-Ramos M, Bongers F (2006) Community dynamics during early secondary succession in Mexican tropical rain forests. J Trop Ecol 22:663–674. https://doi.org/10.1017/S0266467406003452
van Breugel M, van Breugel P, Jansen P, Martínez-Ramos M, Bongers F (2012) The relative importance of above- versus belowground competition for tree growth during early succession of a tropical moist forest. Plant Ecol 213:25–34. https://doi.org/10.1007/s11258-011-0003-3
van Breugel M, Hall JS, Craven D, Bailon M, Hernandez A, Abbene M, van Breugel P (2013) Succession of ephemeral secondary forests and their limited role for the conservation of floristic diversity in a human-modified tropical landscape. PLoS ONE 8:e82433. https://doi.org/10.1371/journal.pone.0082433
van der Heijden GMF, Powers JS, Schnitzer SA (2015) Lianas reduce carbon accumulation and storage in tropical forests. Proc Natl Acad Sci 112:13267–13271. https://doi.org/10.1073/pnas.1504869112
van der Heijden GMF, Powers JS, Schnitzer SA (2019) Effect of lianas on forest-level tree carbon accumulation does not differ between seasons: results from a liana removal experiment in Panama. J Ecol 107:1890–1900. https://doi.org/10.1111/1365-2745.13155
Visser MD, Schnitzer SA, Muller-Landau HC, Jongejans E, Kroon H, Comita LS, Hubbell SP, Joseph WS (2018) Tree species vary widely in their tolerance for liana infestation: a case study of differential host response to generalist parasites. J Ecol 106:781–794. https://doi.org/10.1111/1365-2745.12815
Acknowledgements
This research was supported by The Grantham Foundation for the Protection of the Environment and the Smithsonian Tropical Research Institute’s Agua Salud Project. We are grateful to the private landowners who allowed us to work on their land. Edwina von Gal and Vernon Scholey provided useful background information and logistical support. We are grateful to the staff of the Achotines Laboratory of the Inter-American Tropical Tuna Commission (IATCC) and Eco Venao for their generosity during field visits. Research was conducted under a series of research permits issued to JSH by the Ministry of the Environment of Panama. This work could not have been completed without the dedication and hard work by numerous individuals participating in field work over the years. We are particularly grateful to Mario Bailón, Andres Hernandez, Carlos Diaz, Johana Balbuena, Anabel Rivas, Guillermo Fernandez, Miguel Nuñez, Edwin Garcia, Cristina Barber, Julia González, Yuriza Guerrero, Oldemar Valdes, Boris Bernal, Avelino Valdes, Erick Díaz, Jeremy La-Che, Megan Walentowski, William Walker, Kenneth Contreras, Silfredo Tascon, Rigoberto Rivera Camaña, Eric Valdes, Edwin Peres and Estrella Yanguas for help with field work. SE-V thanks Katherine Sinacore for invaluable help during data analysis and for logistical support. SE‐V was supported by a fellowship from the Departamento Administrativo de Ciencia, Tecnología e Innovación COLCIENCIAS, and by the Cullman Fellowship from the School of the Environment at Yale University and the New York Botanical Garden. SAS was supported by NSF DEB 1019436 and a Way Klingler Scholarship from Marquette University.
Author information
Authors and Affiliations
Contributions
SE-V, JSH, MvB and SAS conceived and designed the experiment, SE-V, JSH, MvB and SAS collected the data, and SE-V, JSH, MvB and SAS contributed to write the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Forest Isbell.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Estrada-Villegas, S., Hall, J.S., van Breugel, M. et al. Lianas do not reduce tree biomass accumulation in young successional tropical dry forests. Oecologia 195, 1019–1029 (2021). https://doi.org/10.1007/s00442-021-04877-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-021-04877-z


