Relationships of biodiversity and productivity change with forest succession in Changbai Mountains: Insights from species, traits, and phylogeny

doi:10.17520/biods.2025060

Abstract

Abstract:

Aims: Biodiversity serves as a critical foundation for the formation and maintenance of ecosystem functions. Its influence on ecosystem functioning changes dynamically during forest succession. However, the relative contributions of multi-dimensional biodiversity (species, traits, phylogeny) and their variations across forest successional stages remain unclear. This study aims to investigate the impacts of multi-dimensional biodiversity on forest productivity and their variations across forest succession.

Methods: This study explored the biodiversity and productivity relationships of forests at different successional stages in Changbai Mountains, based on the observations from three 5.2-ha forest dynamics plots in secondary poplar-birch forest (early succession stage), secondary conifer-broadleaf mixed forest (middle succession stage), and primary Korean pine-broadleaf forest (late succession stage). Vegetation survey data were used to calculate species diversity, functional diversity, and phylogenetic diversity. Aboveground biomass and forest productivity were employed as ecosystem function indicators. Structural equation modeling was applied to disentangle the impacts of multi-dimensional biodiversity on ecosystem functions and their variations across successional stages.

Results: (1) With forest succession, aboveground biomass increased continuously while productivity decreased. (2) The relationship between biodiversity and biomass and productivity changed with forest succession, generally showing a weakening trend across stages. (3) Compared with functional diversity and phylogenetic diversity, species diversity did not significantly affect ecosystem functions. (4) Abiotic factors dynamically regulated resources during succession and productivity.

Conclusion: This study enhances the understanding of dynamic patterns and ecological mechanisms underlying multi- dimensional biodiversity and ecosystem function relationships during forest succession, providing scientific insights for the ecological restoration and sustainable management of secondary forests in northeastern China.

Key words: species richness, functional diversity, phylogenetic diversity, aboveground biomass, forest productivity, forest succession

Qilong Yu, Minhui Hao, Huaijiang He, Chunyu Zhang, Xiuhai Zhao. Relationships of biodiversity and productivity change with forest succession in Changbai Mountains: Insights from species, traits, and phylogeny[J]. Biodiv Sci, 2025, 33(8): 25060.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.17520/biods.2025060

https://www.biodiversity-science.net/EN/Y2025/V33/I8/25060

Figures/Tables 4

Fig. 1 Clustering tree of functional traits (A) and phylogenetic tree (B) of Changbai Mountains forests

Fig. 2 Differences in the levels of various factors at different succession stages of Changbai Mountains forests. AGB, Aboveground biomass; FD.mpd, Functional diversity; PD.mpd, Phylogenetic diversity; SR, Species richness; BP, Productivity; SPBF, Secondary poplar-birch forest; SCBF, Secondary conifer-broadleaf mixed forest; PKBF, Primary Korean pine-broadleaf forest. Different lowercase letters indicate significant differences among different forest types (P < 0.05).

Fig. 3 广义线性模型拟合结果。* P < 0.0.5; ** P < 0.01; *** P < 0.001。 Results of generalized linear model fitting. AGB, Aboveground biomass; ASP, Aspect; FD.mpd, Functional diversity; PD.mpd, Phylogenetic diversity; SD, Soil depth; SR, Species richness; STP, Soil total phosphorus content; SW, Soil water content.* P < 0.05; ** P < 0.01; *** P < 0.001.

Fig. 4 Results of structural equation models. (A) Secondary poplar-birch forest; (B) Secondary conifer-broadleaf mixed forest; (C) Primary Korean pine-broadleaf forest. AGB, Aboveground biomass; ASP, Aspect; BP, Productivity; ENV, Environmental factor; FD.mpd, Functional diversity; PD.mpd, Phylogenetic diversity; SD, Soil depth; SR, Species richness; STP, Soil total phosphorus content; SW, Soil water content. CFI, Comparative fit index, SRMR, Standardized root mean square residual, they both reflect the goodness of fit of a model. Red path lines represent positive correlations, and blue path lines represent negative correlations. Solid lines indicate significant relationships (P < 0.05), while dashed lines indicate non-significant relationships (P ≥ 0.05). The numbers on the path lines are standardized path coefficients (r), and the thickness of the lines reflects the magnitude of the coefficients.

References 67

[1]	Bao SD (2000) Soil Agricultural Chemistry Analysis. China Agriculture Press, Beijing. (in Chinese)
	[鲍士旦 (2000) 土壤农化分析. 中国农业出版社, 北京.]
[2]	Bartoń K (2020) Package ‘MuMIn’. Version 1.48.11. https://CRAN.R-project.org/package=MuMIn . (accessed on 2025-01-18)
[3]	Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. Journal of Vegetation Science, 16, 533-540. DOI URL
[4]	Burnham KP, Anderson DR (2004) Multimodel inference: Understanding AIC and BIC in model selection. Sociological Methods & Research, 33, 261-304.
[5]	Cadotte MW (2017) Functional traits explain ecosystem function through opposing mechanisms. Ecology Letters, 20, 989-996. DOI PMID
[6]	Cadotte MW, Arnillas CA, Livingstone SW, Yasui SE (2013) Predicting communities from functional traits. Trends in Ecology & Evolution, 30, 510-511. DOI URL
[7]	Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. Proceedings of the National Academy of Sciences, USA, 105, 17012-17017.
[8]	Cadotte MW, Cavender-Bares J, Tilman D, Oakley TH (2009) Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE, 4, e5695.
[9]	Cadotte MW, Jonathan Davies T, Regetz J, Kembel SW, Cleland E, Oakley TH (2010) Phylogenetic diversity metrics for ecological communities: Integrating species richness, abundance and evolutionary history. Ecology Letters, 13, 96-105. DOI PMID
[10]	Chen YT, Xu ZZ (2014) Review on research of leaf economics spectrum. Chinese Journal of Plant Ecology, 38, 1135-1153. (in Chinese with English abstract) DOI URL
	[陈莹婷, 许振柱 (2014) 植物叶经济谱的研究进展. 植物生态学报, 38, 1135-1153.] DOI
[11]	Chiang JM, Spasojevic MJ, Muller-Landau HC, Sun IF, Lin Y, Su SH, Chen ZS, Chen CT, Swenson NG, McEwan RW (2016) Functional composition drives ecosystem function through multiple mechanisms in a broadleaved subtropical forest. Oecologia, 182, 829-840. DOI
[12]	Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science, 199, 1302-1310. DOI PMID
[13]	Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. The American Naturalist, 111, 1119-1144. DOI URL
[14]	Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany, 51, 335-380. DOI URL
[15]	Dexter KG, Pennington RT, Oliveira-Filho AT, Bueno ML, Silva de Miranda PL, Neves DM (2018) Inserting tropical dry forests into the discussion on biome transitions in the tropics. Frontiers in Ecology and Evolution, 6, 104. DOI URL
[16]	Fan XH (2018) Study on the Formation and Evolution Mechanism of Typical Natural Forest Communities in Changbai Mountains. PhD dissertation, Beijing Forestry University, Beijing. (in Chinese with English abstract)
	[范秀华 (2018) 长白山典型天然林群落形成与演变机制研究. 博士学位论文, 北京林业大学, 北京.]
[17]	Finegan B, Peña-Claros M, de Oliveira A, Ascarrunz N, Bret-Harte MS, Carreño-Rocabado G, Casanoves F, Díaz S, Eguiguren Velepucha P, Fernandez F, Licona JC, Lorenzo L, Salgado Negret B, Vaz M, Poorter L (2015) Does functional trait diversity predict above-ground biomass and productivity of tropical forests? Testing three alternative hypotheses. Journal of Ecology, 103, 191-201. DOI URL
[18]	Flynn DFB, Mirotchnick N, Jain M, Palmer MI, Naeem S (2011) Functional and phylogenetic diversity as predictors of biodiversity-ecosystem-function relationships. Ecology, 92, 1573-1581. DOI PMID
[19]	Forrester DI, Bauhus J (2016) A review of processes behind diversity-productivity relationships in forests. Current Forestry Reports, 2, 45-61. DOI URL
[20]	García-Palacios P, Shaw EA, Wall DH, Hättenschwiler S (2017) Contrasting mass-ratio vs. niche complementarity effects on litter C and N loss during decomposition along a regional climatic gradient. Journal of Ecology, 105, 968-978. DOI URL
[21]	Gower JC, Dijksterhuis GB, Le Roux NJ (1996) Analysis of multivariate data. Journal of Applied Statistics, 23, 123-145.
[22]	Grime JP (1977) Evidence for existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist, 111, 1169-1194. DOI URL
[23]	Hao MH (2021) Relationships and Mechanisms between Biodiversity and Ecosystem Functions in Temperate Secondary Coniferous and Broadleaf Mixed Forests. PhD dissertation, Beijing Forestry University, Beijing. (in Chinese with English abstract)
	[郝珉辉 (2021) 温带次生针阔混交林生物多样性与生态系统功能关系及其作用机制. 博士学位论文, 北京林业大学, 北京.]
[24]	Hao MH, Zhang CY, Zhao XH, von Gadow K (2018) Functional and phylogenetic diversity determine woody productivity in a temperate forest. Ecology and Evolution, 8, 2395-2406. DOI PMID
[25]	Harms KE, Condit R, Hubbell SP, Foster RB (2001) Habitat associations of trees and shrubs in a 50-ha neotropical forest plot. Journal of Ecology, 89, 947-959. DOI URL
[26]	He HJ, Yeerjiang B, Zhang CY, Zuo Q, Pi TH, Gao HT (2016) Biomass allocation of twelve tree species in coniferous and broad-leaved mixed forest in Jiaohe, Jilin Province, Northeast China. Journal of Beijing Forestry University, 38(4), 53-62. (in Chinese with English abstract)
	[何怀江, 叶尔江·拜克吐尔汉, 张春雨, 左强, 邳田辉, 高海涛 (2016) 吉林蛟河针阔混交林12个树种生物量分配规律. 北京林业大学学报, 38(4), 53-62.]
[27]	He LJ, Yang WJ, Shi YH, Ashuo K, Fan Y, Wang GY, Li JJ, Shi SL, Yi GH, Peng PH (2024) Effects of plant community phylogeny and functional diversity on Ageratina adenophora invasion under fire disturbance. Biodiversity Science, 32, 24269. (in Chinese with English abstract) DOI URL
	[何林君, 杨文静, 石宇豪, 阿说克者莫, 范钰, 王国严, 李景吉, 石松林, 易桂花, 彭培好 (2024) 火烧干扰下植物群落系统发育和功能多样性对紫茎泽兰入侵的影响. 生物多样性, 32, 24269.] DOI
[28]	Hoyle RH (2012) Handbook of Structural Equation Modeling. Guilford Press, New York.
[29]	Jin Y, Qian H (2019) V.PhyloMaker: An R package that can generate very large phylogenies for vascular plants. Ecography, 42, 1353-1359. DOI
[30]	Kelly S, Grenyer R, Scotland RW (2014) Phylogenetic trees do not reliably predict feature diversity. Diversity and Distributions, 20, 600-612. DOI URL
[31]	Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26, 1463-1464. DOI PMID
[32]	Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology, 91, 299-305 PMID
[33]	Lasky JR, Uriarte M, Boukili VK, Erickson DL, Kress WJ, Chazdon RL (2014) The relationship between tree biodiversity and biomass dynamics changes with tropical forest succession. Ecology Letters, 17, 1158-1167 DOI PMID
[34]	Legendre P, Gauthier O (2014) Statistical methods for temporal and space-time analysis of community composition data. Proceedings of the Royal Society B: Biological Sciences, 281, 20132728.
[35]	Liang JJ, Crowther TW, Picard N, Wiser S, Zhou M, Alberti G, Schulze ED, McGuire AD, Bozzato F, Pretzsch H, de-Miguel S, Paquette A, Hérault B, Scherer-Lorenzen M, Barrett CB, Glick HB, Hengeveld GM, Nabuurs GJ, Pfautsch S, Viana H, Vibrans AC, Ammer C, Schall P, Verbyla D, Tchebakova N, Fischer M, Watson JV, Chen HYH, Lei XD, Schelhaas MJ, Lu HC, Gianelle D, Parfenova EI, Salas C, Lee E, Lee B, Kim HS, Bruelheide H, Coomes DA, Piotto D, Sunderland T, Schmid B, Gourlet-Fleury S, Sonké B, Tavani R, Zhu J, Brandl S, Vayreda J, Kitahara F, Searle EB, Neldner VJ, Ngugi MR, Baraloto C, Frizzera L, Bałazy R, Oleksyn J, Zawiła-Niedźwiecki T, Bouriaud O, Bussotti F, Finér L, Jaroszewicz B, Jucker T, Valladares F, Jagodzinski AM, Peri PL, Gonmadje C, Marthy W, O’Brien T, Martin EH, Marshall AR, Rovero F, Bitariho R, Niklaus PA, Alvarez-Loayza P, Chamuya N, Valencia R, Mortier F, Wortel V, Engone-Obiang NL, Ferreira LV, Odeke DE, Vasquez RM, Lewis SL, Reich PB (2016) Positive biodiversity-productivity relationship predominant in global forests. Science, 354, aaf8957.
[36]	Liu XJ, Ma KP (2015) Plant functional traits—Concepts, applications and future directions. Scientia Sinica Vitae, 45, 325-339. (in Chinese with English abstract) DOI URL
	[刘晓娟, 马克平 (2015) 植物功能性状研究进展. 中国科学: 生命科学, 45, 325-339.]
[37]	Liu XJ, Swenson NG, Zhang JL, Ma KP (2013) The environment and space, not phylogeny, determine trait dispersion in a subtropical forest. Functional Ecology, 27, 264-272. DOI URL
[38]	Lohbeck M, Poorter L, Martínez-Ramos M, Bongers F (2015) Biomass is the main driver of changes in ecosystem process rates during tropical forest succession. Ecology, 96, 1242-1252. PMID
[39]	Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature, 412, 72-76. DOI URL
[40]	Mann KH (1976) Review of the book Primary Productivity of the Biosphere, edited by H. Lieth & R. H. Whittaker. Limnology and Oceanography, 21, 633-635.
[41]	Mokany K, Ash J, Roxburgh S (2008) Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. Journal of Ecology, 96, 884-893. DOI URL
[42]	Mori AS, Lertzman KP, Gustafsson L (2017) Biodiversity and ecosystem services in forest ecosystems: A research agenda for applied forest ecology. Journal of Applied Ecology, 54, 12-27. DOI URL
[43]	Mouchet MA, Villéger S, Mason NWH, Mouillot D (2010) Functional diversity measures: An overview of their redundancy and their ability to discriminate community assembly rules. Functional Ecology, 24, 867-876. DOI URL
[44]	Paquette A, Joly S, Messier C (2015) Explaining forest productivity using tree functional traits and phylogenetic information: Two sides of the same coin over evolutionary scale? Ecology and Evolution, 5, 1774-1783. DOI PMID
[45]	Paquette A, Messier C (2011) The effect of biodiversity on tree productivity: From temperate to boreal forests. Global Ecology and Biogeography, 20, 170-180. DOI URL
[46]	Poorter L, McDonald I, Alarcón A, Fichtler E, Licona JC, Peña-Claros M, Sterck F, Villegas Z, Sass-Klaassen U (2010) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytologist, 185, 481-492. DOI PMID
[47]	Purschke O, Schmid BC, Sykes MT, Poschlod P, Michalski SG, Durka W, Kühn I, Winter M, Prentice HC (2013) Contrasting changes in taxonomic, phylogenetic and functional diversity during a long-term succession: Insights into assembly processes. Journal of Ecology, 101, 857-866. DOI URL
[48]	Rees M, Condit R, Crawley M, Pacala S, Tilman D (2001) Long-term studies of vegetation dynamics. Science, 293, 650-655. DOI URL
[49]	Rosseel Y (2012) lavaan: An R package for structural equation modeling. Journal of Statistical Software, 48(2), 1-36.
[50]	Stephenson NL, Das AJ, Condit R, Russo SE, Baker PJ, Beckman NG, Coomes DA, Lines ER, Morris WK, Rüger N, Álvarez E, Blundo C, Bunyavejchewin S, Chuyong G, Davies SJ, Duque Á, Ewango CN, Flores O, Franklin JF, Grau HR, Hao ZQ, Harmon ME, Hubbell SP, Kenfack D, Lin Y, Makana JR, Malizia A, Malizia LR, Pabst RJ, Pongpattananurak N, Su SH, Sun IF, Tan S, Thomas D, van Mantgem PJ, Wang XG, Wiser SK, Zavala MA (2014) Rate of tree carbon accumulation increases continuously with tree size. Nature, 507, 90-93.
[51]	Suding KN, Lavorel S, Chapin FS III, Cornelissen JHC, Díaz S, Garnier E, Goldberg D, Hooper DU, Jackson ST, Navas ML (2008) Scaling environmental change through the community-level: A trait-based response-and-effect framework for plants. Global Change Biology, 14, 1125-1140. DOI URL
[52]	Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science, 277, 1300-1302. DOI URL
[53]	van der Plas F (2019) Biodiversity and ecosystem functioning in naturally assembled communities. Biological Reviews, 94, 1220-1245. DOI URL
[54]	van der Sande MT, Peña-Claros M, Ascarrunz N, Arets EJ, Licona JC, Toledo M, Poorter L (2017) Abiotic and biotic drivers of biomass change in a neotropical forest. Journal of Ecology, 105, 1223-1234. DOI URL
[55]	Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos, 116, 882-892. DOI URL
[56]	Wang JJ, Pei TF (2004) Effects of climate change on forest succession. Chinese Journal of Applied Ecology, 15, 1722-1730. (in Chinese with English abstract)
	[王纪军, 裴铁璠 (2004) 气候变化对森林演替的影响. 应用生态学报, 15, 1722-1730.]
[57]	Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science, 304, 1629-1633. DOI PMID
[58]	Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annual Review of Ecology and Systematics, 33, 475-505. DOI URL
[59]	Wu YN, Hao MH, He HJ, Zhang CY, Zhao XH (2025) Relationships between functional diversity and aboveground carbon sink functions and their changes with forest succession in Changbai Mountains, China. Chinese Journal of Plant Ecology, 49, 232-243. (in Chinese with English abstract) DOI URL
	[吴闫宁, 郝珉辉, 何怀江, 张春雨, 赵秀海 (2025) 长白山森林功能多样性与地上碳汇功能的关系及其随演替的变化. 植物生态学报, 49, 232-243.] DOI
[60]	Xia MJ, Wang XX, Hao MH, Zhao XH, Zhang CY (2021) Distribution pattern of functional traits and its response to topographic factors in a conifer and broad-leaved mixed forest in Jiaohe, Jilin Province. Acta Ecologica Sinica, 41, 2794-2802. (in Chinese with English abstract)
	[夏梦洁, 王晓霞, 郝珉辉, 赵秀海, 张春雨 (2021) 吉林蛟河针阔混交林功能性状分布格局及其对地形因素的响应. 生态学报, 41, 2794-2802.]
[61]	Yu DP, Zhou WM, Zhou L, Dai LM (2019) Exploring the history of the management theory and technology of broad-leaved Korean pine (Pinus koraiensis Sieb. et Zucc.) forest in Changbai Mountain region, Northeast China. Chinese Journal of Applied Ecology, 30, 1426-1434. (in Chinese with English abstract)
	[于大炮, 周旺明, 周莉, 代力民 (2019) 长白山区阔叶红松林经营历史与研究历程. 应用生态学报, 30, 1426-1434.] DOI
[62]	Yuan HY, Hao MH, He HJ, Zhang CY, Zhao XH (2024) Impact of species richness and composition on productivity and its changes with forest succession in Changbai Mountains, China. Chinese Journal of Plant Ecology, 48, 1602-1611. (in Chinese with English abstract) DOI
	[袁鹤洋, 郝珉辉, 何怀江, 张春雨, 赵秀海 (2024) 长白山物种丰富度与物种组成对森林生产力的影响及其随演替的变化. 植物生态学报, 48, 1602-1611.] DOI
[63]	Yuan ZQ, Ali A, Jucker T, Ruiz-Benito P, Wang SP, Jiang L, Wang XG, Lin F, Ye J, Hao ZQ, Loreau M (2019) Multiple abiotic and biotic pathways shape biomass demographic processes in temperate forests. Ecology, 100, e02650.
[64]	Yuan ZQ, Wang SP, Gazol A, Mellard J, Lin F, Ye J, Hao ZQ, Wang XG, Loreau M (2016) Multiple metrics of diversity have different effects on temperate forest functioning over succession. Oecologia, 182, 1175-1185. PMID
[65]	Yue QM, He HJ, Zhang CY, Zhao XH, Hao MH (2024) Response of phylogenetic and functional diversity to harvesting disturbance in the Korean pine-broadleaved forest. Acta Ecologica Sinica, 44, 8617-8626. (in Chinese with English abstract)
	[岳庆敏, 何怀江, 张春雨, 赵秀海, 郝珉辉 (2024) 吉林蛟河阔叶红松林谱系多样性和功能多样性对采伐干扰的响应. 生态学报, 44, 8617-8626.]
[66]	Zhang CY, Zhao YZ, Zhao XH, von Gadow K (2012) Species-habitat associations in a northern temperate forest in China. Silva Fennica, 46, 501-519.
[67]	Zhang QG, Zhang DY (2003) Biodiversity and ecosystem function: Recent advances and trends. Biodiversity Science, 11, 351-363. (in Chinese with English abstract) DOI URL
	[张全国, 张大勇 (2003) 生物多样性与生态系统功能: 最新的进展与动向. 生物多样性, 11, 351-363.] DOI