Long-term mix-plantation can recover natural recruitment, genetic diversity and functional traits of the threatened dipterocarp species

Abstract

Asian tropical rainforests have suffered tremendous damages due to the cultivation of commercial plantations, which have resulted in severe species losses, including of the Dipterocarpaceae family. Dipterocarps like Hopea hainanensis and Hopea reticulata are now listed as endangered in the international union for conservation of nature (IUCN) Red List, and Vatica mangachapoi is classified as vulnerable. Reintroduction of the threatened plant species by their artificial planting in an original habitat has been widely recognized as effective to recover the threatened species. However, current reintroductions are mostly based on mono-cultures and also short-term which in turn cannot restore natural recruitment, genetic diversity and functional traits of the threatened species. Here, we have addressed this challenge in a > 32 year-long reintroduction program in the rubber plantations in Southern China. Saplings (5000 − 10,000) of the three threatened Dipterocarp species (H. hainanensis, V. mangachapoi, and H. reticulata) were mix-planted with 99 other species, which originally coexisted naturally in this habitat, in the understory of the rubber plantations in Hainan Island. After 32 years, satellite images show a complete transformation of the landscape. Further, the field surveys have revealed that H. hainanensis and V. mangachapoi have successfully recovered as their numbers have now reached to 115,780 and 108,300, respectively. Most of their reintroduced saplings have survived, and the restored forest has further engaged in natural recruitment. Genetic diversity analysis with ddRADSeq and investigations of several functional traits also support the above inferences. Our long-term mix-plantations not only presents the first case of successful recovery of natural recruitment, genetic diversity and functional traits of the threatened Dipterocarps in China, it also provides a framework for restoring threatened species in other plantations throughout the globe.

Keywords

Active restoration / Hopea hainanensis / Reintroduction / Rubber plantation / Threatened Dipterocarpaceae / Vatica mangachapoi

References

[1] Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U. The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol, 2010, 186(2): 281-285

[2] Ashton PS. Dipterocarp biology as a window to the understanding of tropical forest structure. Annu Rev Ecol Evol Syst, 1988, 19: 347-370

[3] Axelsson EP, Abin JV, Lardizabal MLT, Ilstedt U, Grady KC. A trait-based plant economic framework can help increase the value of reforestation for conservation. Ecol Evol, 2022, 12(5): Article ID: e8855

[4] Bansal M, Morley RJ, Nagaraju SK, Dutta S, Mishra AK, Selveraj J, Kumar S, Niyolia D, Harish SM, Abdelrahim OB, Hasan SE, Ramesh BR, Dayanandan S, Morley HP, Ashton PS, Prasad V. Southeast Asian Dipterocarp origin and diversification driven by Africa-India floristic interchange. Science, 2022, 375(6579): 455-460

[5] Chapman CA, Chapman LJ, Jacob AL, Rothman JM, Omeja P, Reyna-Hurtado R, Hartter J, Lawes MJ. Tropical tree community shifts: implications for wildlife conservation. Biol Conserv, 2010, 143(2): 366-374

[6] Chen SF, Guo W, Chen ZX, Liao WB, Fan Q. Strong genetic structure observed in Primulina danxiaensis, a small herb endemic to Mount Danxia with extremely small populations. Front Genet, 2021, 12: 722149

[7] Corlett RT. Impacts of warming on tropical lowland rainforests. Trends Ecol Evol, 2011, 26(11): 606-613

[8] Curran LM, Leighton M. Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecol Monogr, 2000, 70(1): 101-128

[9] Curran LM, Webb CO. Experimental tests of the spatiotemporal scale of seed predation in mast-fruiting Dipterocarpaceae. Ecol Monogr, 2000, 70(1): 129-148

[10] Dai ZC, Si CC, Zhai DL, Huang P, Qi SS, Lin Y, Wang RP, Zhong QX, Du DL. Genetic effects of historical anthropogenic disturbance on a long-lived endangered tropical tree Vatica mangachapoi. J for Res, 2018, 29(2): 291-299

[11] Deb JC, Phinn S, Butt N, McAlpine CA. The impact of climate change on the distribution of two threatened dipterocarp trees. Ecol Evol, 2017, 7(7): 2238-2248

[12] Ding Y, Zang RG, Jiang YX. Effect of hillslope gradient on vegetation recovery on abandoned land of shifting cultivation in Hainan Island, South China. J Integr Plant Biol, 2006, 48(6): 642-653

[13] Earl DA, VonHoldt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour, 2012, 4(2): 359-361

[14] Fuchs EJ, Robles T, Hamrick JL. Spatial distribution of Guaiacum sanctum (Zygophyllaceae) seedlings and saplings relative to canopy cover in Palo Verde National Park. Costa Rica. Rev Biol Trop, 2013, 61(3): 1521-1533

[15] Godefroid S, Piazza C, Rossi G, Buord S, Stevens AD, Aguraiuja R, Cowell C, Weekley CW, Vogg G, Iriondo JM, Johnson I, Dixon B, Gordon D, Magnanon S, Valentin B, Bjureke K, Koopman R, Vicens M, Virevaire M, Vanderborght T. How successful are plant species reintroductions?. Biol Conserv, 2011, 144(2): 672-682

[16] Greve P, Roderick ML, Ukkola AM, Wada Y. The aridity index under global warming. Environ Res Lett, 2019, 14(12): 124006

[17] Hoffmann S. Challenges and opportunities of area-based conservation in reaching biodiversity and sustainability goals. Biodivers Conserv, 2022, 31(2): 325-352

[18] Kamvar ZN, Tabima JF, Grünwald NJ. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2014, 2 Article ID: e281

[19] Karam DS, Arifin A, Radziah O, Shamshuddin J, Majid NM, Hazandy AH, Zahari I, Ah NH, Rui TX. Impact of long-term forest enrichment planting on the biological status of soil in a deforested dipterocarp forest in Perak, Malaysia. Sci World J, 2012, 2012: 641346

[20] Kaur S, Kaushal S, Adhikari D, Raj K, Rao KS, Tandon R, Goel S, Barik SK, Baishya R. Different GCMs yet similar outcome: predicting the habitat distribution of Shorea robusta C.F. Gaertn. in the Indian Himalayas using CMIP5 and CMIP6 climate models. Environ Monit Assess, 2023, 195(6): 715

[21] Kettle CJ. Ecological considerations for using dipterocarps for restoration of lowland rainforest in Southeast Asia. Biodivers Conserv, 2010, 19(4): 1137-1151

[22] Kettle CJ. Seeding ecological restoration of tropical forests: priority setting under REDD+. Biol Conserv, 2012, 154: 34-41

[23] Khoo E, Barstow M, Maycock C, Bodos V, Chong KY, Chua LSL, Cicuzza D, Deepu S, Dhyani A, Divina ANRed list of dipterocarpaceae, 2022Richmond, UKBotanic Gardens Conservation International

[24] Kramer AT, Havens K. Plant conservation genetics in a changing world. Trends Plant Sci, 2009, 14(11): 599-607

[25] Luo WJ, Strijk JS, Barstow M, Wee AKS. The role of protected areas in tropical tree conservation post-2020: a case study using threatened Dipterocarpaceae. Biol Conserv, 2022, 272: 109634

[26] Luo LM, Ye P, Lin QQ, Liu M, Hao G, Wei T, Sahu SK. From sequences to sustainability: exploring dipterocarp genomes for oleoresin production, timber quality, and conservation. Plant Sci, 2024, 346: 112139

[27] Malik N, Edwards D, Freckleton RP. Comparative analyses and phylogenetic dependence in traits and trends of the Dipterocarpaceae. Ecol Evol, 2025, 15(1): Article ID: e70784

[28] Moloney DJF, Collins C, Holloway P, O’Riordan R. The conservationist’s toolkit: a critical review of the need for a conceptual framework of both in-situ and ex-situ conservation strategies to ensure the success of restoration ecology. Biol Conserv, 2023, 287: 110345

[29] Pang SEH, De Alban JDT, Webb EL. Effects of climate change and land cover on the distributions of a critical tree family in the Philippines. Sci Rep, 2021, 11: 276

[30] Phiri D, Morgenroth J (2017) Developments in landsat land cover classification methods: a review. Remote Sens 9:967. https://doi.org/10.3390/rs9090967

[31] Polak T, Saltz D. Reintroduction as an ecosystem restoration technique. Conserv Biol, 2011, 25(3): 424-425

[32] Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics, 2000, 155(2): 945-959

[33] Ren H, Jian SG, Liu HX, Zhang QM, Lu HF. Advances in the reintroduction of rare and endangered wild plant species. Sci China Life Sci, 2014, 57(6): 603-609

[34] Rochette NC, Rivera-Colón AG, Catchen JM. Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol, 2019, 28(21): 4737-4754

[35] Sack L, Cowan PD, Jaikumar N, Holbrook NM. The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant Cell Environ, 2003, 26(8): 1343-1356

[36] Seidler TG, Plotkin JB. Seed dispersal and spatial pattern in tropical trees. PLoS Biol, 2006, 4(11): Article ID: e344

[37] Singh AK, Liu WJ, Zakari S, Wu JN, Yang B, Jiang XJ, Zhu XA, Zou X, Zhang WJ, Chen CF, Singh R, Nath AJ. A global review of rubber plantations: impacts on ecosystem functions, mitigations, future directions, and policies for sustainable cultivation. Sci Total Environ, 2021, 796: 148948

[38] Stewart FEC, Volpe JP, Taylor JS, Bowman J, Thomas PJ, Pybus MJ, Fisher JT. Distinguishing reintroduction from recolonization with genetic testing. Biol Conserv, 2017, 214: 242-249

[39] Tang L, Duan JY, Cai Y, Wang WN, Liu YB. Low genetic diversity and small effective population size in the endangered Hopea reticulata (Dipterocarpaceae) on Hainan Island, China. Glob Ecol Conserv, 2024, 50 Article ID: e02846

[40] Taylor G, Canessa S, Clarke RH, Ingwersen D, Armstrong DP, Seddon PJ, Ewen JG. Is reintroduction biology an effective applied science?. Trends Ecol Evol, 2017, 32(11): 873-880

[41] Tuck SL, O’Brien MJ, Philipson CD, Saner P, Tanadini M, Dzulkifli D, Godfray HCJ, Godoong E, Nilus R, Ong RC, Schmid B, Sinun W, Snaddon JL, Snoep M, Tangki H, Tay J, Ulok P, Wai YS, Weilenmann M, Reynolds G, Hector A. The value of biodiversity for the functioning of tropical forests: insurance effects during the first decade of the Sabah biodiversity experiment. Proc Biol Sci, 2016, 283(1844): 20161451

[42] Veryard R, Wu JH, O’Brien MJ, Anthony R, Both S, Burslem DFRP, Chen B, Fernandez-Miranda Cagigal E, Godfray HCJ, Godoong E, Liang SL, Saner P, Schmid B, Sau Wai Y, Xie J, Reynolds G, Hector A. Positive effects of tree diversity on tropical forest restoration in a field-scale experiment. Sci Adv, 2023, 9(37): eadf0938

[43] Volis S. Conservation-oriented restoration–a two for one method to restore both threatened species and their habitats. Plant Divers, 2019, 41(2): 50-58

[44] Wang C, Ma X, Ren MX, Tang L. Genetic diversity and population structure in the endangered tree Hopea hainanensis (Dipterocarpaceae) on Hainan Island, China. PLoS ONE, 2020, 15(11): Article ID: e0241452

[45] Wang R, Liu CN, Segar ST, Jiang YT, Zhang KJ, Jiang K, Wang G, Cai J, Chen LF, Chen S, Cheng J, Compton SG, Deng JY, Ding YY, Du FK, Hu XD, Hu XH, Kang L, Li DH, Lu L, Li YY, Tang L, Tong X, Wang ZS, Xu WW, Yang Y, Zang RG, Zu ZX, Zhang YY, Chen XY. Dipterocarpoidae genomics reveal their demography and adaptations to Asian rainforests. Nat Commun, 2024, 15: 1683

[46] Warren-Thomas E, Dolman PM, Edwards DP. Increasing demand for natural rubber necessitates a robust sustainability initiative to mitigate impacts on tropical biodiversity. Conserv Lett, 2015, 8(4): 230-241

[47] Wilcove DS, Giam X, Edwards DP, Fisher B, Koh LP. Navjot’s nightmare revisited: logging, agriculture, and biodiversity in Southeast Asia. Trends Ecol Evol, 2013, 28(9): 531-540

[48] Wyka TP, Oleksyn J, Zytkowiak R, Karolewski P, Jagodziński AM, Reich PB. Responses of leaf structure and photosynthetic properties to intra-canopy light gradients: a common garden test with four broadleaf deciduous angiosperm and seven evergreen conifer tree species. Oecologia, 2012, 170(1): 11-24

[49] Yu HZ, Pei XC, Zhang H. Threat categories of Vatica mangachapoi should be reassessed. Front for Glob Change, 2024, 7: 1356104

[50] Zhang H, Chen HYH, Lian JY, John R, Li RH, Liu H, Ye WH, Berninger F, Ye Q. Using functional trait diversity patterns to disentangle the scale-dependent ecological processes in a subtropical forest. Funct Ecol, 2018, 32(5): 1379-1389

[51] Zhu H. Ecological and biogeographical studies on the tropical rain forest of South Yunnan, SW China with a special reference to its relation with rain forests of Tropical Asia. J Biogeogr, 1997, 24(5): 647-662

[52] Zhu XL, Luo WJ, Chai SF, Tang JM, Wei X, Wee AKS, Kang M. Potential risk of dipterocarps in the marginal Asian rainforests: low population size and high genomic erosion. BMC Biol, 2025, 23(1): 161

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