Overstory functional groups indicate the legacy of land use in a secondary tropical forest in southwestern China

Abstract

Anthropogenic disturbances are widespread in tropical forests and influence the species composition in the overstory. However, the impacts of historical disturbance on tropical forest overstory recovery are unclear due to a lack of disturbance data, and previous studies have focused on understory species. In this study, the purpose was to determine the influence of historical disturbance on the diversity, composition and regeneration of overstory species in present forests. In the 20-ha Xishuangbanna tropical seasonal rainforest dynamics plot in southwestern China, the historical disturbance boundaries were delineated based on panchromatic photographs from 1965. Factors that drove species clustering in the overstory layer (DBH ≥ 40 cm) were analyzed and the abundance, richness and composition of these species were compared among different tree groups based on multiple regression tree analysis. The coefficient of variation of the brightness value in historical panchromatic photographs from 1965 was the primary driver of species clustering in the overstory layer. The abundance and richness of overstory species throughout the regeneration process were similar, but species composition was always different. Although the proportion of large-seeded and vigorous-sprouting species showed no significant difference between disturbed and undisturbed forests in the treelet layer (DBH < 20 cm), the difference became significant when DBH increased. The findings highlight that historical disturbances have strong legacy effects on functional group composition in the overstory and the recovery of overstory species was multidimensional. Functional group composition can better indicate the dynamics of overstory species replacement during secondary succession.

Keywords

Historical disturbance / Legacy effects / Secondary forests / Overstory species / Functional groups

References

[1]	Abbas S, Nichol JE, Zhang J, Fischer GA (2019) The accumulation of species and recovery of species composition along a 70 year succession in a tropical secondary forest. Ecol Indic 106:105524. https://doi.org/10.1016/j.ecolind.2019.105524
[2]	Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62(1):245–253. https://doi.org/10.1111/j.1541-0420.2005.00440.x
[3]	Asner GP, Mascaro J (2014) Mapping tropical forest carbon: calibrating plot estimates to a simple LiDAR metric. Remote Sens Environ 140(2):614–624. https://doi.org/10.1016/j.rse.2013.09.023
[4]	Baraloto C, Forget PM (2007) Seed size, seedling morphology, and response to deep shade and damage in neotropical rain forest trees. Am J Bot 94(6):901–911. https://doi.org/10.3732/ajb.94.6.901
[5]	Baraloto C, Paine CET, Poorter L, Beauchene J, Bonal D, Domenach AM, Hérault B, Pati?o S, Roggy JC, Chave J (2010) Decoupled leaf and stem economics in rain forest trees. Ecol Lett 13(11):1338–1347. https://doi.org/10.1111/j.1461-0248.2010.01517.x
[6]	Beven KJ, Kirkby MJ (1979) A physically based, variable contributing area model of basin hydrology. Hydrol Sci J 24(1):43–69. https://doi.org/10.1080/02626667909491834
[7]	Bond WJ, Midgley JJ (2001) Ecology of sprouting in woody plants: the persistence niche. Trends Ecol Evol 16(1):45–51. https://doi.org/10.1016/S0169-5347(00)02033-4
[8]	Bond WJ, Midgley JJ (2003) The evolutionary ecology of sprouting in woody plants. Int J Plant Sci 164(S3):S103–S114. https://doi.org/10.1086/374191
[9]	Bongers F, Poorter L, Hawthorne WD, Sheil D (2009) The intermediate disturbance hypothesis applies to tropical forests, but disturbance contributes little to tree diversity. Ecol Lett 12(8):798–805. https://doi.org/10.1111/j.1461-0248.2009.01329.x
[10]	Breiman L, Friedman J, Olshen R, Stone C (1984) Classification and regression trees. Wadsworth International Group, California, CA
[11]	Busby PE, Vitousek P, Dirzo R (2010) Prevalence of tree regeneration by sprouting and seeding along a rainfall gradient in Hawai’i. Biotropica 42:80–86. https://doi.org/10.1111/j.1744-7429.2009.00540.x
[12]	Cao M, Zhu H, Wang H, Lan GY, Hu YH, Zhou SS, Deng XB, Cui JY (2008) Xishuangbanna tropical seasonal rainforest dynamics plot: tree distribution maps, diameter tables and species documentation. Yunnan Science and Technology Press, Kunming, China
[13]	Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93(12):2533–2547. https://doi.org/10.1890/11-1952.1
[14]	Chapin FS, BretHarte MS, Hobbie SE, Zhong HL (1996) Plant functional types as predictors of transient responses of arctic vegetation to global change. J Veg Sci 7(3):347–358. https://doi.org/10.2307/3236278
[15]	Chave J, Condit R, Lao S, Caspersen JP, Foster RB, Hubbell SP (2003) Spatial and temporal variation of biomass in a tropical forest: results from a large census plot in Panama. J Ecol 91(2):240–252. https://doi.org/10.1046/j.1365-2745.2003.00757.x
[16]	Chave J, Condit R, Muller-Landau HC, Thomas SC, Ashton PS, Bunyavejchewin S, Co LL, Dattaraja HS, Davies SJ, Esufali S, Ewango CEN, Feeley KJ, Foster RB, Gunatilleke N, Gunatilleke S, Hall P, Hart TB, Hernández C, Hubbell SP, Itoh A, Kiratiprayoon S, LaFrankie JV, De Lao SL, Makana JR, Noor MNS, Kassim AR, Samper C, Sukumar R, Suresh HS, Tan S, Thompson J, Tongco MDC, Valencia R, Vallejo M, Villa G, Yamakura T, Zimmerman JK, Losos EC (2008) Assessing evidence for a pervasive alteration in tropical tree communities. PLOS Biol 6(3):e45. https://doi.org/10.1371/journal.pbio.0060045
[17]	Chave J, Piponiot C, Marechaux I, De Foresta H, Larpin D, Fischer FJ, Derroire G, Vincent G, Hérault B (2020) Slow rate of secondary forest carbon accumulation in the Guianas compared with the rest of the Neotropics. Ecol Appl 30(1):e02004. https://doi.org/10.1002/eap.2004
[18]	Chazdon RL (2003) Tropical forest recovery: legacies of human impact and natural disturbances. Perspect Plant Ecol 6(1):51–71. https://doi.org/10.1078/1433-8319-00042
[19]	Chazdon RL, Norden N, Colwell RK, Chao A (2023) Monitoring recovery of tree diversity during tropical forest restoration: lessons from long-term trajectories of natural regeneration. Philos Trans R Soc B 378(1867):20210069. https://doi.org/10.1098/rstb.2021.0069
[20]	CHCNAV (2021) CHCNAV alphaair 450 user manual v2.0. Shanghai Huace Navigation Technology Ltd. https://www.chcnav.com/product-detail/alphaair-450 [accessed on 18.08.2023]
[21]	Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18(1):117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
[22]	Conrad O (2018) Tool Potential Annual Insolation. SAGA-GIS Tool Library Documentation (v7.6.1). https://saga-gis.sourceforge.io/saga_tool_doc/7.6.1/ta_lighting_7.html [accessed on 04.12.2023]
[23]	De’ath G (2002) Multivariate regression trees: a new technique for modeling species-environment relationships. Ecology 83(4):1105–1117. https://doi.org/10.1890/0012-9658(2002)083[1105:MRTANT]2.0.CO;2
[24]	Del Tredici P (2001) Sprouting in temperate trees: a morphological and ecological review. Bot Rev 67(2):121–140. https://doi.org/10.1007/BF02858075
[25]	Deng Y, Deng XB, Dong JL, Zhang WF, Hu T, Nakamura A, Song XY, Fu PL, Cao M (2020) Detecting growth phase shifts based on leaf trait variation of a canopy dipterocarp tree species (Parashorea chinensis). Forests 11(11):1145. https://doi.org/10.3390/f11111145
[26]	Denslow JS, Guzman GS (2000) Variation in stand structure, light and seedling abundance across a tropical moist forest chronosequence. Panama J Veg Sci 11(2):201–212. https://doi.org/10.2307/3236800
[27]	Dietze MC, Clark JS (2008) Changing the gap dynamics paradigm: vegetative regeneration control on forest response to disturbance. Ecol Monogr 78(3):331–347. https://doi.org/10.1890/07-0271.1
[28]	Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leit?o PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schr?der B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36(1):27–46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
[29]	Dou LN, Zhang WF, Deng XB, Cao M, Tang Y (2018) Nine-year seed rain dynamics in Parashorea chinensis forest in Xishuangbanna. Southwest China. Biodiversity Sci 26(9):919–930. https://doi.org/10.17520/biods.2018101. ((in Chinese))
[30]	Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67(3):345–366. https://doi.org/10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2
[31]	Eckert CG (2001) The loss of sex in clonal plants. Evol Ecol 15(4–6):501–520. https://doi.org/10.1023/A:1016005519651
[32]	Filho AAR, Adams C, Manfredini S, Aguilar R, Neves WA (2015) Dynamics of soil chemical properties in shifting cultivation systems in the tropics: a meta-analysis. Soil Use Manage 31(4):474–482. https://doi.org/10.1111/sum.12224
[33]	Florinsky IV (1998) Combined analysis of digital terrain models and remotely sensed data in landscape investigations. Prog Phys Geog 22(1):33–60. https://doi.org/10.1177/0309133398022001
[34]	Frazer GW, Magnussen S, Wulder MA, Niemann KO (2011) Simulated impact of sample plot size and co-registration error on the accuracy and uncertainty of LiDAR-derived estimates of forest stand biomass. Remote Sens Environ 115(2):636–649. https://doi.org/10.1016/j.rse.2010.10.008
[35]	Fukami T (2015) Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol S 46(1):1–23. https://doi.org/10.1146/annurev-ecolsys-110411-160340
[36]	Gómez-Pompa A, Vázquez-Yanes C, Guevara S (1972) The tropical rain forest: a nonrenewable resource. Science 177(4051):762–765. https://doi.org/10.1126/science.177.4051.762
[37]	Guariguata MR, Ostertag R (2001) Neotropical secondary forest succession: changes in structural and functional characteristics. For Ecol Manage 148(1):185–206. https://doi.org/10.1016/S0378-1127(00)00535-1
[38]	Haralick RM (1979) Statistical and structural approaches to texture. Proc IEEE 67(5):786–804. https://doi.org/10.1109/PROC.1979.11328
[39]	Haralick RM, Shanmugam K, Dinstein I (1973) Textural features for image classification. IEEE Transactions on Systems, Man, and Cybernetics SMC 3(6):610–621. https://doi.org/10.1109/TSMC.1973.4309314
[40]	Hattori D, Kenzo T, Irino KO, Kendawang JJ, Ninomiya I, Sakurai K (2013) Effects of soil compaction on the growth and mortality of planted dipterocarp seedlings in a logged-over tropical rainforest in Sarawak, Malaysia. For Ecol Manage 310:770–776. https://doi.org/10.1016/j.foreco.2013.09.023
[41]	Hu YH, Sha LQ, Blanchet FG, Zhang JL, Tang Y, Lan GY, Cao M (2012) Dominant species and dispersal limitation regulate tree species distributions in a 20-ha plot in Xishuangbanna. Southwest China Oikos 121(6):952–960. https://doi.org/10.1111/j.1600-0706.2011.19831.x
[42]	Jakovac CC, Pe?a-Claros M, Kuyper TW, Bongers F (2015) Loss of secondary-forest resilience by land-use intensification in the Amazon. J Ecol 103(1):67–77. https://doi.org/10.1111/1365-2745.12298
[43]	Jakovac CC, Bongers F, Kuyper TW, Mesquita RCG, Pe?a-Claros M (2016) Land use as a filter for species composition in Amazonian secondary forests. J Veg Sci 27(6):1104–1116. https://doi.org/10.1111/jvs.12457
[44]	Jeter GW, Carter GA (2016) Habitat change on Horn Island, Mississippi, 1940–2010, determined from textural features in panchromatic vertical aerial imagery. Geocarto Int 31(9):985–994. https://doi.org/10.1080/10106049.2015.1094527
[45]	Jin HF, Yuan YG, Li JM (2021) Host functional traits affect plant responses to pathogen stress: a meta-analysis. Acta Oecol 110:103703. https://doi.org/10.1016/j.actao.2021.103703
[46]	John R, Dalling JW, Harms KE, Yavitt JB, Stallard RF, Mirabello M, Hubbell SP, Valencia R, Navarrete H, Vallejo M, Foster RB (2007) Soil nutrients influence spatial distributions of tropical tree species. Proc Natl Acad Sci U S A 104(3):864–869. https://doi.org/10.1073/pnas.0604666104
[47]	Johnstone JF, Allen CD, Franklin JF, Frelich LE, Harvey BJ, Higuera PE, Mack MC, Meentemeyer RK, Metz MR, Perry GLW, Schoennagel T, Turner MG (2016) Changing disturbance regimes, ecological memory, and forest resilience. Front Ecol Environ 14(7):369–378. https://doi.org/10.1002/fee.1311
[48]	Keuls M (1952) The use of the “studentized range” in connection with an analysis of variance. Euphytica 1:112–122. https://doi.org/10.1007/BF01908269
[49]	Kitajima K (2002) Do shade-tolerant tropical tree seedlings depend longer on seed reserves? Functional growth analysis of three Bignoniaceae species. Funct Ecol 16(4):433–444. https://doi.org/10.1046/j.1365-2435.2002.00641.x
[50]	Kleinman JS, Goode JD, Fries AC, Hart JL (2019) Ecological consequences of compound disturbances in forest ecosystems: a systematic review. Ecosphere 10(11):e02962. https://doi.org/10.1002/ecs2.2962
[51]	Kruger LM, Midgley JJ, Cowling RM (1997) Resprouters vs reseeders in South African forest trees; a model based on forest canopy height. Funct Ecol 11(1):101–105. https://doi.org/10.1046/j.1365-2435.1997.00064.x
[52]	LaFrankie JV, Ashton PS, Chuyong GB, Co L, Condit R, Davies SJ, Foster R, Hubbell SP, Kenfack D, Lagunzad D, Losos EC, Nor NSM, Tan S, Thomas DW, Valencia R, Villa G (2006) Contrasting structure and composition of the understory in species-rich tropical rain forests. Ecology 87(9):2298–2305. https://doi.org/10.1890/0012-9658(2006)87[2298:CSACOT]2.0.CO;2
[53]	Lan GY, Hu YH, Cao M, Zhu H (2011) Topography related spatial distribution of dominant tree species in a tropical seasonal rain forest in China. For Ecol Manage 262(8):1507–1513. https://doi.org/10.1016/j.foreco.2011.06.052
[54]	Letcher SG, Chazdon RL (2009) Rapid recovery of biomass, species richness, and species composition in a forest chronosequence in Northeastern Costa Rica. Biotropica 41(5):608–617. https://doi.org/10.1111/j.1744-7429.2009.00517.x
[55]	Levene H (1960) Robust tests for equality of variances. In: Olkin J, Churye S, Hoeffding W, Madow W, Mann H (eds) Contributions to probability and statistics: essays in honor of harold hotelling. Stanford University Press, Palo Alto, CA, pp 278–292
[56]	Li YW, Deng XB, Cao M, Lei YB, Xia YJ (2013) Soil restoration potential with corridor replanting engineering in the monoculture rubber plantations of Southwest China. Ecol Eng 51:169–177. https://doi.org/10.1016/j.ecoleng.2012.12.081
[57]	Lin LX, Cao M, He YY, Baskin JM, Baskin CC (2006) Nonconstituent species in soil seed banks as indicators of anthropogenic disturbance in forest fragments. Can J for Res 36(9):2300–2316. https://doi.org/10.1139/x06-137
[58]	Liu JJ, Tan YH, Slik JWF (2014) Topography related habitat associations of tree species traits, composition and diversity in a Chinese tropical forest. For Ecol Manage 330:75–81. https://doi.org/10.1016/j.foreco.2014.06.045
[59]	Lord J, Egan J, Clifford T, Jurado E, Leishman M, Williams D, Westoby M (1997) Larger seeds in tropical floras: consistent patterns independent of growth form and dispersal mode. J Biogeogr 24(2):205–211. https://doi.org/10.1046/j.1365-2699.1997.00126.x
[60]	Maarel E, Franklin J, Wiley J (2013) Vegetation ecology. Wiley Online Library, New York, NY
[61]	Magnago LFS, Edwards DP, Edwards FA, Magrach A, Martins SV, Laurance WF (2014) Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests. J Ecol 102(2):475–485. https://doi.org/10.1111/1365-2745.12206
[62]	Martin PA, Newton AC, Bullock JM (2013) Carbon pools recover more quickly than plant biodiversity in tropical secondary forests. Proc R Soc B 280(1773):20132236. https://doi.org/10.1098/rspb.2013.2236
[63]	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
[64]	Muscolo A, Bagnato S, Sidari M, Mercurio R (2014) A review of the roles of forest canopy gaps. J Forestry Res 25(4):725–736. https://doi.org/10.1007/s11676-014-0521-7
[65]	Nakamura A, Kitching RL, Cao M, Creedy TJ, Fayle TM, Freiberg M, Hewitt CN, Itioka T, Koh LP, Ma K, Malhi Y, Mitchell A, Novotny V, Ozanne CMP, Song L, Wang H, Ashton LA (2017) Forests and their canopies: achievements and horizons in canopy science. Trends Ecol Evol 32(6):438–451. https://doi.org/10.1016/j.tree.2017.02.020
[66]	Newman D (1939) The distribution of range in samples from a normal population, expressed in terms of an independent estimate of standard deviation. Biometrika 31(1/2):20–30. https://doi.org/10.2307/2334973
[67]	Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O'Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, Caceres M, Durand S, Evangelista H, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Cunha E, Smith T, Stier A, Braak C, Weedon J (2022) Vegan: community ecology package. https://cran.r-project.org/web/packages/vegan/index.html [accessed on 18.08.2023]
[68]	Okuda T, Yamada T, Hosaka T, Miyasaku N, Hashim M, Lau AMS, Saw LG (2019) Canopy height recovery after selective logging in a lowland tropical rain forest. For Ecol Manage 442:117–123. https://doi.org/10.1016/j.foreco.2019.03.045
[69]	Osorio F, Vallejos R, Cuevas F, Mancilla D (2022) Tools for assessment the association between two spatial processes. R package version 0.3–8. http://spatialpack.mat.utfsm.cl [accessed on 18.08.2023]
[70]	Ozanne CMP, Anhuf D, Boulter SL, Keller M, Kitching RL, K?rner C, Meinzer FC, Mitchell AW, Nakashizuka T, Dias PLS, Stork NE, Wright SJ, Yoshimura M (2003) Biodiversity meets the atmosphere: a global view of forest canopies. Science 301(5630):183–186. https://doi.org/10.1126/science.1084507
[71]	Palma AC, Goosem M, Fensham RJ, Goosem S, Preece ND, Stevenson PR, Laurance SGW (2021) Dispersal and recruitment limitations in secondary forests. J Veg Sci 32(1):e12975. https://doi.org/10.1111/jvs.12975
[72]	Poorter L, Kitajima K, Mercado P, Chubi?a J, Melgar I, Prins HHT (2010) Resprouting as a persistence strategy of tropical forest trees: relations with carbohydrate storage and shade tolerance. Ecology 91(9):2613–2627. https://doi.org/10.1890/09-0862.1
[73]	Poorter L, Craven D, Jakovac CC, Van der Sande MT, Amissah L, Bongers F, Chazdon RL, Farrior CE, Kambach S, Meave JA, Mu?oz R, Norden N, Rüger N, Van Breugel M, Zambrano AMA, Amani B, Andrade JL, Brancalion PHS, Broadbent EN, De Foresta H, Dent DH, Derroire G, DeWalt SJ, Dupuy JM, Durán SM, Fantini AC, Finegan B, Hernández-Jaramillo A, Hernández-Stefanoni JL, Hietz P, Junqueira AB, N’dja JK, Letcher SG, Lohbeck M, López-Camacho R, Martínez-Ramos M, Melo FPL, Mora F, Müller SC, N’Guessan AE, Oberleitner F, Ortiz-Malavassi E, Pérez-García EA, Pinho BX, Piotto D, Powers JS, Rodríguez-Buriticá S, Rozendaal DMA, Ruíz J, Tabarelli M, Teixeira HM, De Sá Barretto Sampaio EV, Van der Wal H, Villa PM, Fernandes GW, Santos BA, Aguilar-Cano J, De Almeida-Cortez JS, Alvarez-Davila E, Arreola-Villa F, Balvanera P, Becknell JM, Cabral GAL, Castellanos-Castro C, De Jong BHJ, Nieto JE, Espírito-Santo MM, Fandino MC, García H, García-Villalobos D, Hall JS, Idárraga A, Jiménez-Montoya J, Kennard D, Marín-Spiotta E, Mesquita R, Nunes YRF, Ochoa-Gaona S, Pe?a-Claros M, Pérez-Cárdenas N, Rodríguez-Velázquez J, Villanueva LS, Schwartz NB, Steininger MK, Veloso MDM, Vester HFM, Vieira ICG, Williamson GB, Zanini K, Hérault B (2021) Multidimensional tropical forest recovery. Science 374(6573):1370–1376. https://doi.org/10.1126/science.abh3629
[74]	Powers JS, Marín-Spiotta E (2017) Ecosystem processes and biogeochemical cycles in secondary tropical forest succession. Annu Rev Ecol Evol Syst 48(1):497–519. https://doi.org/10.1146/annurev-ecolsys-110316-022944
[75]	Quesada CA, Phillips OL, Schwarz M, Czimczik CI, Baker TR, Pati?o S, Fyllas NM, Hodnett MG, Herrera R, Almeida S, Dávila EA, Arneth A, Arroyo L, Chao KJ, Dezzeo N, Erwin T, di Fiore A, Higuchi N, Coronado EH, Jimenez EM, Killeen T, Lezama AT, Lloyd G, López-González G, Luizao FJ, Malhi Y, Monteagudo A, Neill DA, Vargas PN, Paiva R, Peacock J, Pe?uela MC, Cruz AP, Pitman N, Priante N, Prieto A, Ramírez H, Rudas A, Salomao R, Santos AJB, Schmerler J, Silva N, Silveira M, Vásquez R, Vieira I, Terborgh J, Lloyd J (2012) Basin-wide variations in amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9(6):2203–2246. https://doi.org/10.5194/bg-9-2203-2012
[76]	R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
[77]	Roberts D (2023) Labdsv: ordination and multivariate analysis for ecology R. Package version 2.1–0. https://CRAN.R-project.org/package=labdsv [accessed on 18.08.2023]
[78]	Rozendaal DMA, Bongers F, Aide TM, Alvarez-Dávila E, Ascarrunz N, Balvanera P, Becknell JM, Bentos TV, Brancalion PHS, Cabral GAL, Calvo-Rodriguez S, Chave J, César RG, Chazdon RL, Condit R, Dallinga JS, De Almeida-Cortez JS, De Jong B, De Oliveira A, Denslow JS, Dent DH, DeWalt SJ, Dupuy JM, Durán SM, Dutrieux LP, Espírito-Santo MM, Fandino MC, Fernandes GW, Finegan B, García H, Gonzalez N, Moser VG, Hall JS, Hernández-Stefanoni JL, Hubbell S, Jakovac CC, Hernández AJ, Junqueira AB, Kennard D, Larpin D, Letcher SG, Licona JC, Lebrija-Trejos E, Marín-Spiotta E, Martínez-Ramos M, Massoca PES, Meave JA, Mesquita RCG, Mora F, Müller SC, Mu?oz R, De Oliveira Neto SN, Norden N, Nunes YRF, Ochoa-Gaona S, Ortiz-Malavassi E, Ostertag R, Pe?a-Claros M, Pérez-García EA, Piotto D, Powers JS, Aguilar-Cano J, Rodriguez-Buritica S, Rodríguez-Velázquez J, Romero-Romero MA, Ruíz J, Sanchez-Azofeifa A, De Almeida AS, Silver WL, Schwartz NB, Thomas WW, Toledo M, Uriarte M, De Sá Sampaio EV, Van Breugel M, Van der Wal H, Martins SV, Veloso MDM, Vester HFM, Vicentini A, Vieira ICG, Villa P, Williamson GB, Zanini KJ, Zimmerman J, Poorter L (2019) Biodiversity recovery of neotropical secondary forests. Sci Adv 5(3):eaau3114. https://doi.org/10.1126/sciadv.aau3114
[79]	Slik JWF, Paoli G, McGuire K, Amaral I, Barroso J, Bastian M, Blanc L, Bongers F, Boundja P, Clark C, Collins M, Dauby G, Ding Y, Doucet JL, Eler E, Ferreira L, Forshed O, Fredriksson G, Gillet JF, Harris D, Leal M, Laumonier Y, Malhi Y, Mansor A, Martin E, Miyamoto K, Araujo-Murakami A, Nagamasu H, Nilus R, Nurtjahya E, Oliveira á, Onrizal O, Parada-Gutierrez A, Permana A, Poorter L, Poulsen J, Ramirez-Angulo H, Reitsma J, Rovero F, Rozak A, Sheil D, Silva-Espejo J, Silveira M, Spironelo W, Ter Steege H, Stevart T, Navarro-Aguilar GE, Sunderland T, Suzuki E, Tang J, Theilade I, Van der Heijden G, Van Valkenburg J, Van Do T, Vilanova E, Vos V, Wich S, W?ll H, Yoneda T, Zang R, Zhang MG, Zweifel N (2013) Large trees drive forest aboveground biomass variation in moist lowland forests across the tropics. Global Ecol Biogeogr 22(12):1261–1271. https://doi.org/10.1111/geb.12092
[80]	Smythe N (1970) Relationships between fruiting seasons and seed dispersal methods in a neotropical forest. Am Nat 104(935):25–35. https://doi.org/10.1086/282638
[81]	Student (1927) Errors of routine analysis. Biometrika 19(1/2):151–164. https://doi.org/10.2307/2332181
[82]	Thomas SC, Appanah S (1995) On the statistical analysis of reproductive size thresholds in dipterocarp forests. J Trop for Sci 7(3):412–418
[83]	Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JWC (2011) Multi-element regulation of the tropical forest carbon cycle. Front Ecol Environ 9(1):9–17. https://doi.org/10.1890/100047
[84]	Turner IM (2001) The Ecology of Trees in the Tropical Rain Forest. Cambridge University Press, Cambridge, UK
[85]	Velho N, Ratnam J, Srinivasan U, Sankaran M (2012) Shifts in community structure of tropical trees and avian frugivores in forests recovering from past logging. Biol Conserv 153:32–40. https://doi.org/10.1016/j.biocon.2012.04.028
[86]	Vesk PA, Westoby M (2004) Sprouting ability across diverse disturbances and vegetation types worldwide. J Ecol 92(2):310–320. https://doi.org/10.1111/j.0022-0477.2004.00871.x
[87]	Vieira DLM, Scariot A (2006) Principles of natural regeneration of tropical dry forests for restoration. Restor Ecol 14(1):11–20. https://doi.org/10.1111/j.1526-100X.2006.00100.x
[88]	Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3(1):89–101. https://doi.org/10.1111/j.2041-210X.2011.00127.x
[89]	Wendt AL, Chazdon RL, Ramirez OV (2022) Successional trajectories of seed dispersal mode and seed size of canopy tree species in wet tropical forests. Front for Glob Chang 5:946541. https://doi.org/10.3389/ffgc.2022.946541
[90]	Wood EM, Pidgeon AM, Radeloff VC, Keuler NS (2012) Image texture as a remotely sensed measure of vegetation structure. Remote Sens Environ 121:516–526. https://doi.org/10.1016/j.rse.2012.01.003
[91]	Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
[92]	Wu ZY (1987) The vegetation of Yunnan. Science Press, Beijing, China ((in Chinese))
[93]	Xu JC, Jefferson F, Lu X, Nancy P, Stephen L, Ai XH (1999) Effects of Swidden cultivation, state policies, and customary institutions on land cover in a Hani Village, Yunnan, China. Mt Res Dev 19(2):123–132. https://doi.org/10.2307/3674253
[94]	Yang H, Liu SR, Cao KF, Wang JX, Li YD, Xu H (2017) Characteristics of typhoon disturbed gaps in an old-growth tropical montane rainforest in Hainan Island, China. J Forestry Res 28(6):1231–1239. https://doi.org/10.1007/s11676-017-0402-y
[95]	Zhang JH, Cao M (1995) Tropical forest vegetation of Xishuangbanna, SW China and its secondary changes, with special reference to some problems in local nature conservation. Biol Conserv 73(3):229–238. https://doi.org/10.1016/0006-3207(94)00118-A
[96]	Zhu H, Cao M, Hu HB (2006) Geological history, flora, and vegetation of Xishuangbanna, Southern Yunnan. China Biotropica 38(3):310–317. https://doi.org/10.1111/j.1744-7429.2006.00147.x
[97]	Zhu H, Zhou SS, Yan LC, Shi JP, Shen YX (2019) Studies on the evergreen broad-leaved forests of Yunnan. Southwestern China Bot Rev 85(2):131–148. https://doi.org/10.1007/s12229-019-09210-1
[98]	Zhu H, Zhang J, Cheuk ML, Hau BC, Fischer GA, Gale SW (2023) Monoculture plantations impede forest recovery: evidence from the regeneration of lowland subtropical forest in Hong Kong. Front for Glob Chang 6:1098666. https://doi.org/10.3389/ffgc.2023.1098666