Abstract
Niche complementarity, mass-ratio, and vegetation quantity effects have been identified as major drivers of the biodiversity-ecosystem functioning (BEF) relationships. However, their relative contribution to biomass and productivity is not yet clear in temperate secondary forests. Based on the observations from a 21.12-ha temperate secondary forest plot in northeastern China, we assessed how these mechanisms regulate forest biomass and productivity. The niche complementarity effect was quantified using a functional diversity metric that was calculated from six locally collected functional traits. The mass-ratio effect was described as functional trait composition using community-weighted mean trait values. Vegetation quantity effect was evaluated using vegetation biomass. We performed structural equation modeling to test the alternative mechanisms. Our results provide evidence for all three mechanisms. Functional diversity increased forest productivity, in line with the niche complementarity hypothesis. Acquisitive traits (e.g., greater specific leaf area and leaf nitrogen concentration) enhance productivity, while conservative traits (e.g., greater wood density) enhance the long-term accumulation of biomass, demonstrating the mass-ratio hypothesis. Furthermore, we observed a significant positive relationship between biomass and productivity, confirming the vegetation quantity hypothesis. We conclude that functional traits drive biomass and productivity through multiple mechanisms. Both niche complementarity and the mass-ratio effects play roles in this temperate secondary forest. In addition, we emphasize the importance of preserving sufficient biomass stock to ensure maximum productivity in secondary forests. Our study contributes to the identification of the mechanisms underlying BEF relationships and has practical significance for guiding temperate secondary forest management and conservation.
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References
Ali A, Mattsson E (2018) Wood density is a sustainability indicator for the management of dry zone homegarden agroforests: evidences from biodiversity-ecosystem function relationships. Ecol Ind. https://doi.org/10.1016/j.ecolind.2018.04.024
Ammer C (2019) Diversity and forest productivity in a changing climate. New Phytol 221:50–66. https://doi.org/10.1111/nph.15263
Balvanera P, Quijas S, Pérez-Jiménez A (2011) Distribution patterns of tropical dry forest trees along a mesoscale water availability gradient. Biotropica 43:414–422. https://doi.org/10.1111/j.1744-7429.2010.00712.x
Barber CB, Dobkin DP, Huhdanpaa H (1996) The quickhull algorithm for convex hulls. ACM Trans Math Software 22:469–483
Barrufol M, Schmid B, Bruelheide H, Chi X, Hector A, Ma K, Niklaus PA (2013) Biodiversity promotes tree growth during succession in subtropical forest. PLoS ONE 8:e81246. https://doi.org/10.1371/journal.pone.0081246
Bauhus J, Forrester DI, Pretzsch H, Felton A, Pyttel P, Benneter A (2017) Silvicultural options for mixed-species stands. In: Pretzsch H, Forrester DI, Bauhus J (eds) Mixed-species forests. Springer, Berlin, pp 433–501
Bentler PM (1990) Comparative fit indexes in structural models. Psychol Bull 107:238
Borcard D, Gillet F, Legendre P (2018) Numerical ecology with R. Springer, Berlin
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
Chiang J, Spasojevic MJ, Muller-Landau HC, Sun I, Lin Y, Su S, McEwan RW (2016) Functional composition drives ecosystem function through multiple mechanisms in a broadleaved subtropical forest. Oecologia 182:829–840. https://doi.org/10.1007/s00442-016-3717-z
Chisholm RA, Muller-Landau HC, Abdul Rahman K, Bebber DP, Bin Y, Bohlman SA, Cao H (2013) Scale-dependent relationships between tree species richness and ecosystem function in forests. J Ecol 101:1214–1224. https://doi.org/10.1111/1365-2745.12132
Condit R (1998) Tropical forest census plots. Springer, Berlin
Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Pausas JG (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380. https://doi.org/10.1071/BT02124
Davies GM, Gray A (2015) Don’t let spurious accusations of pseudoreplication limit our ability to learn from natural experiments (and other messy kinds of ecological monitoring). Ecol Evolut 5:5295–5304. https://doi.org/10.1002/ece3.1782
de Bello F, Lavorel S, Díaz S, Harrington R, Cornelissen JH, Bardgett RD, da Silva PM (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893. https://doi.org/10.1007/s10531-010-9850-9
Díaz S, Hector A, Wardle DA (2009) Biodiversity in forest carbon sequestration initiatives: not just a side benefit. Current Opin Environ Sustain 1:55–60. https://doi.org/10.1016/j.cosust.2009.08.001
FAO (2015) Global forest resources assessment 2015: how are the world’s forests changing?. Italy, Rome
Finegan B, Peña-Claros M, Oliveira A, Ascarrunz N, Bret-Harte MS, Carreño-Rocabado G, Poorter L (2015) Does functional trait diversity predict above-ground biomass and productivity of tropical forests? Testing three alternative hypotheses. J Ecol 103:191–201. https://doi.org/10.1111/1365-2745.12346
Forrester DI, Bauhus J (2016) A review of processes behind diversity-productivity relationships in forests. Current Forestry Rep 2:45–61. https://doi.org/10.1007/s40725-016-0031-2
Forrester DI, Ammer C, Annighöfer PJ, Barbeito I, Bielak K, Bravo-Oviedo A, Hurt V (2018) Effects of crown architecture and stand structure on light absorption in mixed and monospecific Fagus sylvatica and Pinus sylvestris forests along a productivity and climate gradient through Europe. J Ecol 106:746–760. https://doi.org/10.1111/1365-2745.12803
Fotis AT, Murphy SJ, Ricart RD, Krishnadas M, Whitacre J, Wenzel JW, Comita LS (2018) Above-ground biomass is driven by mass-ratio effects and stand structural attributes in a temperate deciduous forest. J Ecol 106:561–570. https://doi.org/10.1111/1365-2745.12847
Franklin JF (1988) Structural and functional diversity in temperate forests. Biodiversity National Academy Press, Washington, DC, pp 166–175
Gadow KV, Zhang GQ, Durrheim G, Drew D, Seydack A (2016) Diversity and production in an Afromontane Forest. Forest Ecosyst 3:15. https://doi.org/10.1186/s40663-016-0074-7
García-Palacios P, Shaw EA, Wall DH, Hättenschwiler S (2017) Contrasting mass-ratio versus niche complementarity effects on litter C and N loss during decomposition along a regional climatic gradient. J Ecol 105:968–978. https://doi.org/10.1111/1365-2745.12730
Garnier E, Cortez J, Billès G, Navas ML, Roumet C, Debussche M, Neill C (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637. https://doi.org/10.1890/03-0799
Grace JB, Schoolmaster DRJ, Guntenspergen GR, Little AM, Mitchell BR, Miller KM, Schweiger EW (2012) Guidelines for a graph-theoretic implementation of structural equation modeling. Ecosphere 3:1–44. https://doi.org/10.1890/ES12-00048.1
Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910. https://doi.org/10.1046/j.1365-2745.1998.00306.x
Grossiord C, Granier A, Gessler A, Jucker T, Bonal D (2014) Does drought influence the relationship between biodiversity and ecosystem functioning in boreal forests? Ecosystems 17:394–404. https://doi.org/10.1007/s10021-013-9729-1
Hao ZQ, Wang QL, Dai LMT (2000) The importance of the national programme for natural forests conservation on biodiversity conservation in northeast state owned forest areas of China. In: Xu ZH (ed) Go Forward the 21st century’s Chinese biodiversity conservation. China Forestry Press, Beijing, pp 21–26
Hao M, Zhang C, Zhao X, Gadow KV (2018) Functional and phylogenetic diversity determine woody productivity in a temperate forest. Ecol Evolut 8:2395–2406. https://doi.org/10.1002/ece3.3857
Hao M, Ganeshaiah KN, Zhang C, Zhao X, Gadow KV (2019) Discriminating among forest communities based on taxonomic, phylogenetic and trait distances. For Ecol Manage 440:40–47. https://doi.org/10.1016/j.foreco.2019.03.006
Harms KE, Condit R, Hubbell SP, Foster RB (2001) Habitat associations of trees and shrubs in a 50-ha neotropical forest plot. J Ecol 89:947–959. https://doi.org/10.1111/j.1365-2745.2001.00615.x
Houghton RA, Hall F, Goetz SJ (2009) Importance of biomass in the global carbon cycle. J Geophys Res Biogeosci 114:G00E03. https://doi.org/10.1029/2009JG000935
Keeling HC, Phillips OL (2007) The global relationship between forest productivity and biomass. Glob Ecol Biogeogr 16:618–631. https://doi.org/10.1111/j.1466-8238.2007.00314.x
Laliberte E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. https://doi.org/10.1890/08-2244.1
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
Liu J, Yunhong T, Slik JF (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
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. https://doi.org/10.1890/14-0472.1
Martin PA, Newton AC, Bullock JM (2013) Carbon pools recover more quickly than plant biodiversity in tropical secondary forests. Proceed Royal Soc B Biol Sci 280:20132236. https://doi.org/10.1098/rspb.2013.2236
Mokany K, Ash J, Roxburgh S (2008) Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J Ecol 96:884–893. https://doi.org/10.1111/j.1365-2745.2008.01395.x
Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579. https://doi.org/10.1046/j.1461-0248.2003.00471.x
Ouyang S, Xiang W, Wang X, Xiao W, Chen L, Li S, Lei P (2019) Effects of stand age, richness and density on productivity in subtropical forests in China. J Ecol 107:2266–2277. https://doi.org/10.1111/1365-2745.13194
Pacala S, Kinzig AP (2002) Introduction to theory and the common ecosystem model. In: Kinzig AP, Pacala SW, Tilman D (eds) Functional consequences of biodiversity: empirical progress and theoretical extensions. Princeton University Press, Princeton, pp 169–174
Paquette A, Messier C (2011) The effect of biodiversity on tree productivity: from temperate to boreal forests. Glob Ecol Biogeogr 20:170–180. https://doi.org/10.1111/j.1466-8238.2010.00592.x
Peña-Claros M, Fredericksen TS, Alarcón A, Blate GM, Choque U, Leaño C, Putz FE (2008) Beyond reduced-impact logging: silvicultural treatments to increase growth rates of tropical trees. For Ecol Manage 256:1458–1467. https://doi.org/10.1016/j.foreco.2007.11.013
Pillai P, Gouhier TC (2019) Not even wrong: the spurious measurement of biodiversity’s effects on ecosystem functioning. Ecology 100:e02645. https://doi.org/10.1002/ecy.2645
Prado-Junior JA, Schiavini I, Vale VS, Arantes CS, van der Sande MT, Lohbeck M, Poorter L (2016) Conservative species drive biomass productivity in tropical dry forests. J Ecol 104:817–827. https://doi.org/10.1111/1365-2745.12543
Randolph JC, Green GM, Belmont J, Burcsu T, Welch D (2005) Forest ecosystems and the human dimension. In: Moran EF, Ostrom E (eds) Seeing the forest and the trees: human-environment interactions in forest ecosystems. MIT Press, Cambridge, pp 105–125
Ratcliffe S, Liebergesell M, Ruiz-Benito P, Madrigal González J, Muñoz Castañeda JM, Kändler G, Zavala MA (2016) Modes of functional biodiversity control on tree productivity across the European continent. Glob Ecol Biogeogr 25:251–262. https://doi.org/10.1111/geb.12406
Ricotta C, Moretti M (2011) CWM and Rao’s quadratic diversity: a unified framework for functional ecology. Oecologia 167:181–188. https://doi.org/10.1007/s00442-011-1965-5
Roscher C, Schumacher J, Gubsch M, Lipowsky A, Weigelt A, Buchmann N, Schulze ED (2012) Using plant functional traits to explain diversity-productivity relationships. PLoS ONE 7:e36760. https://doi.org/10.1371/journal.pone.0036760
Rosenfield MF, Müller SC (2019) Plant traits rather than species richness explain ecological processes in subtropical forests. Ecosystems. https://doi.org/10.1007/s10021-019-00386-6
Rosseel Y (2012) lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36
Ruiz-Benito P, Gómez-Aparicio L, Paquette A, Messier C, Kattge J, Zavala MA (2014) Diversity increases carbon storage and tree productivity in Spanish forests. Glob Ecol Biogeogr 23:311–322. https://doi.org/10.1111/geb.12126
Ruiz-Benito P, Ratcliffe S, Zavala MA, Martínez-Vilalta J, Vilà-Cabrera A, Lloret F, Jump AS (2017) Climate- and successional-related changes in functional composition of European forests are strongly driven by tree mortality. Glob Change Biol 23:4162–4176. https://doi.org/10.1111/gcb.13728
Schleuter D, Daufresne M, Massol F, Argillier C (2010) A user’s guide to functional diversity indices. Ecol Monogr 80:469–484. https://doi.org/10.1890/08-2225.1
Staples TL, Dwyer JM, England JR, Mayfield MM (2019) Productivity does not correlate with species and functional diversity in Australian reforestation plantings across a wide climate gradient. Glob Ecol Biogeogr 28:1417–1429. https://doi.org/10.1111/geb.12962
Stephenson NL, van Mantgem PJ (2005) Forest turnover rates follow global and regional patterns of productivity. Ecol Lett 8:524–531. https://doi.org/10.1111/j.1461-0248.2005.00746.x
Sun X, Canby K, Liu L (2016) China’s logging ban in natural forests: impacts of extended policy at home and Abroad. Forests trends information brief. Forest Trends, Washington, DC
Tan L, Fan C, Zhang C, Zhao X (2019) Understanding and protecting forest biodiversity in relation to species and local contributions to beta diversity. Eur J Forest Res. https://doi.org/10.1007/s10342-019-01220-3
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. https://doi.org/10.1126/science.277.5330.1300
Tobner CM, Paquette P, Gravel D, Reich PB, Williams LJ, Messier C (2016) Functional identity and complementarity drive overyielding in young tree communities. Ecol Lett 19:638–647. https://doi.org/10.1111/ele.12600
van der Plas F (2019) Biodiversity and ecosystem functioning in naturally assembled communities. Biol Rev. https://doi.org/10.1111/brv.12499
van der Sande MT, Arets EJ, Peña-Claros M, Hoosbeek MR, Cáceres-Siani Y, van der Hout P, Poorter L (2018) Soil fertility and species traits, but not diversity, drive productivity and biomass stocks in a Guyanese tropical rainforest. Funct Ecol 32:461–474. https://doi.org/10.1111/1365-2435.12968
Vilà M, Carrillo-Gavilán A, Vayreda J, Bugmann H, Fridman J, Grodzki W, Trasobares A (2013) Disentangling biodiversity and climatic determinants of wood production. PLoS ONE 8:e53530. https://doi.org/10.1371/journal.pone.0053530
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301. https://doi.org/10.1890/07-1206.1
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. https://doi.org/10.1111/j.0030-1299.2007.15559.x
Williamson GB, Wiemann MC (2010) Measuring wood specific gravitycorrectly. Am J Bot 97:519–524. https://doi.org/10.3732/ajb.0900243
Yamakura T, Kanzaki M, Itoh A, Ohkubo T, Ogino K, Chai EOK, Ashton PS (1995) Topography of a large-scale research plot established within a tropical rain forest at lambir, sarawak. Tropics 5:41–56. https://doi.org/10.3759/tropics.5.41
Zhang C, Zhao Y, Zhao X, Gadow KV (2012) Species-habitat associations in a northern temperate forest in China. Silva Fennica 46:501–519. https://doi.org/10.14214/sf.907
Acknowledgements
This research is supported by the Program of National Natural Science Foundation of China (31670643; 31800362), the Key Project of National Key Research and Development Plan (2017YFC0504104), Beijing Forestry University Outstanding Young Talent Cultivation Project (2019JQ03001), and the Short-term International Student Program for Postgraduates of Forestry First-Class Discipline (2019XKJS0501).
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MH and CM conceived the ideas and wrote the manuscript. MH and YG analyzed the data. CZ and XZ created the database of forest plots and performed project coordination. KVG provided comments and other technical support. All authors contributed critically to the drafts and gave final approval for publication.
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Hao, M., Messier, C., Geng, Y. et al. Functional traits influence biomass and productivity through multiple mechanisms in a temperate secondary forest. Eur J Forest Res 139, 959–968 (2020). https://doi.org/10.1007/s10342-020-01298-0
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DOI: https://doi.org/10.1007/s10342-020-01298-0