Abstract
The initiation of a new plant community in a restoration area hinges on the performance of seedlings post-planting. This study aimed to evaluate the impact of species functional traits—specific leaf area (SLA), wood density (WD), seed dry mass (SDM), and potential height (H)—on the seedling performance 25 months after planting, comparing two planting designs (rows and clusters) and the influence of fertilization addition in clusters. The restoration area is a riparian tropical forest located on the coastal plain at Caraguatatuba municipality, São Paulo, Brazil. We monitored 3017 tree seedlings and estimated their survivorship and relative growth rate (RGR) using the diameter, height, and canopy area of the surviving seedlings and the stem biomass for the cluster RGR estimation. Using linear mixed models, we analyzed how the planting designs and the functional traits affect species survival and their RGR. We underscored the significance of slow-growth traits (low SLA, and high SDM and WD) in enhancing species survival, whereas, maximizing species growth entails prioritizing seedlings with greater potential height. Cluster survival and growth improved with a greater abundance of species with low values of SDM (i.e., fast-growth species) and communities with low functional divergence (high similarity). Fertilized clusters improved the RGR of large-seeded species. Accounting for functional traits in restoration is advantageous for enhancing seedling performance at the species level, which is an important consideration for restoration practitioners. To optimize applied nucleation, clusters should target functional diversity at this community level and include competitive species to improve productivity.
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References
Adler PB, Salguero-Gómez R, Compagnoni A, Hsu JS, Ray-Mukherjee J, Mbeau-Ache C, Franco M (2014) Functional traits explain variation in plant life history strategies. Proc Natl Acad Sci 111:740–745. https://doi.org/10.1073/pnas.1315179111
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JDM, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Scheipl F, Grothendieck G (2009) Package ‘lme4’
Bechara FC, Trentin BE, Engel VL, Estevan DA, Ticktin T (2021) Performance and cost of applied nucleation versus high-diversity plantations for tropical forest restoration. For Ecol Manag 491:119088. https://doi.org/10.1016/j.foreco.2021.119088
Bertoncello R, Oliveira AA, Holl KD, Pansonato MP, Martini AM (2016) Cluster planting facilitates survival but not growth in early development of restored tropical forest. Basic Appl Ecol 17:489–496. https://doi.org/10.1016/j.baae.2016.04.006
Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848. https://doi.org/10.1038/nature00812
Carvalho G (2020) Tools for interacting with the Brazilian Flora 2020
Charles LS, Dwyer JM, Smith TJ, Connors S, Marschner P, Mayfield MM (2018) Species wood density and the location of planted seedlings drive early-stage seedling survival during tropical forest restoration. J Appl Ecol 55:1009–1018. https://doi.org/10.1111/1365-2664.13031
Chave J, Andalo C, Brown S, Cairns MA, Chambers JQ, Eamus D, Fölster H, Fromard F, Higuchi N, Kira T (2005) Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia 145:87–99. https://doi.org/10.1007/s00442-005-0100-x
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
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366. https://doi.org/10.1146/annurev.ecolsys.31.1.343
Corbin JD, Holl KD (2012) Applied nucleation as a forest restoration strategy. For Ecol Manag 265:37–46
Díaz S, Kattge J, Cornelissen JH, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Colin Prentice I (2016) The global spectrum of plant form and function. Nature 529:167–171. https://doi.org/10.1038/nature16489
Díaz S, Kattge J, Cornelissen JH, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Prentice IC (2022) The global spectrum of plant form and function: enhanced species-level trait dataset. Sci Data 9:755. https://doi.org/10.1038/s41597-022-01774-9
Flora do Brasil (2020) Flora e Funga do Brasil. Jardim Botânico do Rio de Janeiro, Rio de Janeiro
Fraser LH (2020) TRY—a plant trait database of databases. Glob Change Biol 26:189–190. https://doi.org/10.1111/gcb.14869
Gardiner R, Shoo LP, Dwyer JM (2019) Look to seedling heights, rather than functional traits, to explain survival during extreme heat stress in the early stages of subtropical rainforest restoration. J Appl Ecol 56:2687–2697. https://doi.org/10.1111/1365-2664.13505
Garnier E, Navas M-L, Grigulis K (2016) Plant functional diversity: organism traits, community structure, and ecosystem properties. Oxford University Press, Oxford
Grossnickle SC (2012) Why seedlings survive: influence of plant attributes. New For 43:711–738. https://doi.org/10.1007/s11056-012-9336-6
Guimarães ZTM, Dos Santos VAHF, Nogueira WLP, de Almeida NO, Ferreira MJ (2018) Leaf traits explaining the growth of tree species planted in a Central Amazonian disturbed area. For Ecol Manag 430:618–628. https://doi.org/10.1016/j.foreco.2018.08.048
Havrilla CA, Munson SM, Yackulic EO, Butterfield BJ (2021) Ontogenetic trait shifts: seedlings display high trait variability during early stages of development. Funct Ecol 35:2409–2423. https://doi.org/10.1111/1365-2435.13897
Holl KD, Reid JL, Cole RJ, Oviedo-Brenes F, Rosales JA, Zahawi RA (2020) Applied nucleation facilitates tropical forest recovery: lessons learned from a 15-year study. J Appl Ecol 57:2316–2328. https://doi.org/10.1111/1365-2664.13684
Holl KD, Zahawi RA, Cole RJ, Ostertag R, Cordell S (2011) Planting seedlings in tree islands versus plantations as a large-scale tropical forest restoration strategy. Restor Ecol 19:470–479. https://doi.org/10.1111/j.1526-100X.2010.00674.x
Kattge J, Bönisch G, Díaz S, Lavorel S, Prentice IC, Leadley P, Tautenhahn S, Werner GD, Aakala T, Abedi M (2020) TRY plant trait database–enhanced coverage and open access. Glob Change Biol 26:119–188. https://doi.org/10.1111/gcb.14904
Kunstler G, Falster D, Coomes DA, Hui F, Kooyman RM, Laughlin DC, Poorter L, Vanderwel M, Vieilledent G, Wright SJ (2016) Plant functional traits have globally consistent effects on competition. Nature 529:204–207. https://doi.org/10.1038/nature16476
Laliberté E, Legendre P, Shipley B, Laliberté ME (2014). Package ‘fd’. Measuring functional diversity from multiple traits, and other tools for functional ecology, pp 0–12
Larson JE, Sheley RL, Hardegree SP, Doescher PS, James JJ (2016) Do key dimensions of seed and seedling functional trait variation capture variation in recruitment probability? Oecologia 181:39–53. https://doi.org/10.1007/s00442-015-3430-3
Lasky JR, Uriarte M, Boukili VK, Chazdon RL (2014) Trait-mediated assembly processes predict successional changes in community diversity of tropical forests. Proc Natl Acad Sci 111:5616–5621. https://doi.org/10.1073/pnas.1319342111
Laughlin DC (2023) Plant strategies: the demographic consequences of functional traits in changing environments. Oxford University Press, Oxford
Laughlin DC, Gremer JR, Adler PB, Mitchell RM, Moore MM (2020) The net effect of functional traits on fitness. Trends Ecol Evol 35:1037–1047. https://doi.org/10.1016/j.tree.2020.07.010
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. https://doi.org/10.1038/35083573
MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385. https://doi.org/10.1086/282505
Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205. https://doi.org/10.1111/j.1365-2745.2008.01476.x
Manhães AP, Pantaleão LC, Moraes LFD, Amazonas NT, Saavedra MM, Mantuano D, Sansevero JBB (2022) Functional trajectory for the assessment of ecological restoration success. Restor Ecol 30:e13665. https://doi.org/10.1111/rec.13665
Martínez-Garza C, Bongers F, Poorter L (2013) Are functional traits good predictors of species performance in restoration plantings in tropical abandoned pastures? For Ecol Manag 303:35–45. https://doi.org/10.1016/j.foreco.2013.03.046
Mayfield MM, Levine JM (2010) Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Lett 13:1085–1093. https://doi.org/10.1111/j.1461-0248.2010.01509.x
Moles AT, Westoby M (2004) Seedling survival and seed size: a synthesis of the literature. J Ecol 92:372–383. https://doi.org/10.1111/j.0022-0477.2004.00884.x
Mouchet MA, Villéger S, Mason NW, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876. https://doi.org/10.1111/j.1365-2435.2010.01695.x
Oliveira-Filho A (2017) NeoTropTree: tree flora of the neotropical region: a database involving biogeography, diversity and conservation. Universidade Federal de Minas Gerais
Oliveira RS, Eller CB, Barros FDV, Hirota M, Brum M, Bittencourt P (2021) Linking plant hydraulics and the fast–slow continuum to understand resilience to drought in tropical ecosystems. New Phytol 230:904–923. https://doi.org/10.1111/nph.17266
Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE (2016) Corrigendum to: New handbook for standardised measurement of plant functional traits worldwide. Austral J Bot 64:715–716. https://doi.org/10.1071/BT12225_CO
Philipson CD, Dent DH, O’Brien MJ, Chamagne J, Dzulkifli D, Nilus R, Philips S, Reynolds G, Saner P, Hector A (2014) A trait-based trade-off between growth and mortality: evidence from 15 tropical tree species using size-specific relative growth rates. Ecol Evol 4:3675–3688. https://doi.org/10.1002/ece3.1186
Pommerening A, Muszta A (2016) Relative plant growth revisited: towards a mathematical standardisation of separate approaches. Ecol Model 320:383–392. https://doi.org/10.1016/j.ecolmodel.2015.10.015
Poorter H, Lambers H, Evans JR (2014) Trait correlation networks: a whole-plant perspective on the recently criticized leaf economic spectrum. New Phytol 201:378–382
Poorter L, Rozendaal DM, Bongers F, Almeida DJS, Álvarez FS, Andrade JL, Arreola Villa LF, Becknell JM, Bhaskar R, Boukili V (2021) Functional recovery of secondary tropical forests. Proc Natl Acad Sci 118:e2003405118. https://doi.org/10.1073/pnas.2003405118
Poorter L, Wright SJ, Paz H, Ackerly DD, Condit R, Ibarra-Manríquez G, Harms KE, Licona J, Martinez-Ramos M, Mazer S (2008) Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. Ecology 89:1908–1920. https://doi.org/10.1890/07-0207.1
Rasband W (2012) ImageJ: Image processing and analysis in Java. Astrophysics Source Code Library, p. ascl: 1206.1013
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Reich PB (2014) The world-wide ‘fast–slow’plant economics spectrum: a traits manifesto. J Ecol 102:275–301
Rüger N, Comita LS, Condit R, Purves D, Rosenbaum B, Visser MD, Wright SJ, Wirth C (2018) Beyond the fast–slow continuum: demographic dimensions structuring a tropical tree community. Ecol Lett 21:1075–1084. https://doi.org/10.1111/ele.12974
Silliman BR, Schrack E, He Q, Cope R, Santoni A, van der Heide T, Jacobi R, Jacobi M, van de Koppel J (2015) Facilitation shifts paradigms and can amplify coastal restoration efforts. Proc Natl Acad Sci 112:14295–14300. https://doi.org/10.1073/pnas.1515297112
Toledo-Aceves T, Bonilla-Moheno M, Sosa VJ, López-Barrera F, Williams-Linera G (2022) Leaf functional traits predict shade tolerant tree performance in cloud forest restoration plantings. J Appl Ecol 59:2274–2286. https://doi.org/10.1111/1365-2664.14128
Trinder CJ, Brooker RW, Robinson D (2013) Plant ecology’s guilty little secret: understanding the dynamics of plant competition. Funct Ecol 27:918–929. https://doi.org/10.1111/1365-2435.12078
Vieira BC, Ferreira FS, Gomes MCV (2015) Physical and hydrologial soil properties and the shallow landslides in the serra do mar paulista/propriedades fisicas e hidrologicas dos solos e os escorregamentos rasos na serra do mar paulista. Ra'e Ga. pp 269–288
Violle C, Garnier E, Lecoeur J, Roumet C, Podeur C, Blanchard A, Navas M-L (2009) Competition, traits and resource depletion in plant communities. Oecologia 160:747–755. https://doi.org/10.1007/s00442-009-1333-x
Werden LK, Alvarado JP, Zarges S, Calderón ME, Schilling EM, Gutiérrez LM, Powers JS (2018) Using soil amendments and plant functional traits to select native tropical dry forest species for the restoration of degraded Vertisols. J Appl Ecol 55:1019–1028. https://doi.org/10.1111/1365-2664.12998
Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227
Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159. https://doi.org/10.1146/annurev.ecolsys.33.010802.150452
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1016/j.tree.2010.11.011
Wright SJ, Kitajima K, Kraft NJ, Reich PB, Wright IJ, Bunker DE, Condit R, Dalling JW, Davies SJ, Díaz S (2010) Functional traits and the growth–mortality trade-off in tropical trees. Ecology 91:3664–3674. https://doi.org/10.1890/09-2335.1
Yarranton G, Morrison R (1974) Spatial dynamics of a primary succession: nucleation. J Ecol. https://doi.org/10.2307/2258988
Zimback LB, Prado PI, Pansonato MP, Franco GA, Martini AM (2023) Strong spatial and temporal limitations in seed arrival as complementary mechanisms for species coexistence in a tropical Atlantic coastal forest. Plant Ecol 224:267–281. https://doi.org/10.1007/s11258-023-01294-5
Acknowledgements
We thank the members of LabTrop (São Paulo University—USP) for the execution of seedlings measurements and the members of Plant Ecophysiology Laboratory (Federal Rio de Janeiro University—UFRJ) for helping with the species functional traits measuring (Moab Andrade, Beatriz Camelo). We are thankful to all staff from UTGCA/Petrobras, Jorge Paes and Frederico Machado from CENPES, who helped with logistic issues in fieldwork. We also thank Guilherme Mazzochini for his statistical support.
Funding
Financial support for this research was provided by the Petroleum Brazilian Company (Petrobras S.A.) and the National Agency for Petroleum, Natural Gas, and Biofuels—ANP (Grant #5900.0110930.19.9). JS is supported by a PQ-2 grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
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APM: conceptualization and formal analysis; NTA: data curation and writing—original draft and review & editing; DM: supervision, validation, funding acquisition, and writing—review & editing; AM and MPP: investigation, delineation of experimental methodology, and writing—review & editing; JBB: visualization and writing—review & editing. All authors read and approved the final version of the manuscript.
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Manhães, A.P., Amazonas, N.T., Pansonato, M.P. et al. The effects of nucleation and species functional traits on tree seedling performance in the early stage of ecological restoration. Plant Ecol (2024). https://doi.org/10.1007/s11258-024-01412-x
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DOI: https://doi.org/10.1007/s11258-024-01412-x