Abstract
In forest succession, the ecological strategies of the dominant species that are based on functional traits are important in the determination of both the mechanisms and the potential directions of succession. Thirty-one plots were established in the Loess Plateau region of northern Shaanxi in China. Fifteen leaf traits were measured for the 31 dominant species that represented the six stages of succession, and the traits included four that were related to morphology, seven to stoichiometry and four to physiological ecology. The species from the different successional stages had different patterns of distribution of the traits, and different key traits predicted the turnover of the species during succession. The ash and the cellulose contents were key regulatory factors of species turnover in the early successional communities, and the trait niche forces in sugar and leaf dry mass content might become more important with the progression of succession. When only the three herb stages were considered, a progressive replacement of the ruderal by the competitive–ruderal species occurred in the intermediate stages of succession, which was followed by the stress-tolerant–competitive or the competitive-stress tolerant-ruderal strategists late in the succession. Thus, the different species that occurred in the different stages of succession shared different trait-based ecological strategies. Additionally, these differences occurred concomitantly with a shift toward competitive-stress tolerant-ruderal strategies.
Similar content being viewed by others
References
Ackerly DD, Cornwell WK (2007) A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecol Lett 10:135–145
Al Haj Khaled R, Duru M, Theau JP, Plantureux S, Cruz P (2005) Variation in leaf traits through seasons and N-availability levels and its consequences for ranking grassland species. J Veg Sci 16:391–398
Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S (2010) A multi-trait approach reveals the structure and the relative importance of intra-vs. interspecific variability in plant traits. Funct Ecol 24:1192–1201
An H, Shangguan ZP (2010) Leaf stoichiometric trait and specific leaf area of dominant species in the secondary succession of the Loess Plateau. Pol J Ecol 58:103–113
An H, Shangguan ZP (2012) Generality of leaf traits relationships of dominant species along the secondary succession in the Loess Plateau of China. Afr J Biotechnol 11:1624–1631
Anten NPR, Hirose T (2003) Shoot structure, leaf physiology, and daily carbon gain of plant species in a tallgrass meadow. Ecology 84:955–968
Bazzaz FA (1979) The physiological ecology of plant succession. Annu Rev Ecol Syst 10:351–371
Bhaskar R, Dawson TE, Balvanera P (2014) Community assembly and functional diversity along succession post-management. Funct Ecol 28:1256–1265
Bloor JM, Grubb PJ (2003) Growth and mortality in high and low light: trends among 15 shade-tolerant tropical rain forest tree species. J Ecol 91:77–85
Boege K, Dirzo R (2004) Intraspecific variation in growth, defense and herbivory in Dialium guianense (Caesalpiniaceae) mediated by edaphic heterogeneity. Plant Ecol 175:59–69
Böhnke M, Kröber W, Welk E, Wirth C, Bruelheide H (2013) Maintenance of constant functional diversity during secondary succession of a subtropical forest in China. J Veg Sci. doi:10.1111/jvs.12114
Booth RE, Grime JP (2003) Effects of genetic impoverishment on plant community diversity. J Ecol 91:721–730
Bowman R (1988) A rapid method to determine total phosphorus in soils. Soil Sci Soc Am J 52:1301
Brym ZT, Lake JK, Allen D, Ostling A (2011) Plant functional traits suggest novel ecological strategy for an invasive shrub in an understorey woody plant community. J Appl Ecol 48:1098–1106
Caccianiga M, Luzzaro A, Pierce S, Ceriani RM, Cerabolini B (2006) The functional basis of a primary succession resolved by CSR classification. Oikos 112:10–20
Catorci A, Vitanzi A, Tardella FM (2011) Variations in CSR strategies along stress gradients in the herb layer of submediterranean forests (central Italy). Plant Ecol Evol 144:299–306
Cavender-Bares J, Kitajima K, Bazzaz FA (2004) Multiple trait associations in relation to habitat differentiation among 17 Floridian oak species. Ecol Monogr 74:635–662
Chai YF, Liu X, Yue M, Guo JC, Wang M, Wan PC, Zhang XF, Zhang CG (2015) Leaf traits in dominant species from different secondary successional stages of deciduous forest on the Loess Plateau of northern China. Appl Veg Sci 18:50–63
Cornelissen JHC, Lavorel S, Garnier E, Diaz 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 standardized and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380
Cornwell WK, Ackerly DD (2010) A link between plant traits and abundance: evidence from coastal California woody plants. J Ecol 98:814–821
Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Diaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071
Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534
Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Diaz S, Lavorel S, De Bello F, Quetier F, Grigulis K, Robson M (2007) Incorporating plant functional diversity effects in ecosystem service assessments. Proc Natl Acad Sci USA 104:20684–20689
Erschbamer B, Kneringer E, Niederfriniger Schlag R (2001) Seed rain, soil seed bank, seedling recruitment, and survival of seedlings on a glacier foreland in the Central Alps. Flora Morphol Geobot Ecophysiol 196:304–312
Fischer C, Höll W (1991) Food reserves of Scots pine (Pinus sylvestris L.). I. Seasonal changes in the carbohydrate and fat reserves of pine needles. Trees 5:187–195
Fortunel C, Paine CE, Fine PV, Kraft NJ, Baraloto C (2014) Environmental factors predict community functional composition in Amazonian forests. J Ecol 102:145–155
Garnier E, Laurent G, Bellmann A, Debain S, Berthelier P, Ducout B, Roumet C, Navas ML (2001) Consistency of species ranking based on functional leaf traits. New Phytol 152:69–83
Garnier E, Cortez J, Bills G, Navas ML, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellmann A (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637
Grime JP (1987) Dominant and subordinate components of plant communities: implications for succession, stability and diversity. In: Symposium of the British Ecological Society
Grime JP (2001) Plant strategies, vegetation processes and ecosystem properties. Wiley, London
Grime JP, Hodgson JG, Hunt R (2007) Comparative plant ecology a functional approach to common British species. Castlepoint Press, Dalbeattie
Grotkopp E, Rejmanek M (2007) High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. Am J Bot 94:526–532
Hodgson J, Wilson P, Hunt R, Grime J, Thompson K (1999) Allocating CSR plant functional types: a soft approach to a hard problem. Oikos 85:283
Hunt R, Hodgson JG, Thompson K, Bungener P, Dunnett NP, Askew AP (2004) A new practical tool for deriving a functional signature for herbaceous vegetation. Appl Veg Sci 7:163–170
Kahmen S, Poschlod P (2004) Plant functional trait responses to grassland succession over 25 years. J Veg Sci 15:21–32
Kazakou E, Garnier E, Navas M, Roumet C, Collin C, Laurent G (2007) Components of nutrient residence time and the leaf economics spectrum in species from Mediterranean old-fields differing in successional status. Funct Ecol 21:235–245
Kikuzawa K, Ackerly D (1999) Significance of leaf longevity in plants. Plant Species Biol 14:39–45
Kröber W, Böhnke M, Welk E, Wirth C, Bruelheide H (2012) Leaf trait-environment relationships in a subtropical broadleaved forest in south-east China. PLoS One 7:e35742
Lake JK, Ostling A (2009) Comment on “Functional traits and niche-based tree community assembly in an Amazonian forest”. Science 324:1015c
Lecerf A, Chauvet E (2008) Intraspecific variability in leaf traits strongly affects alder leaf decomposition in a stream. Basic Appl Ecol 9:598–605
Leps J, De Bello F, Lavorel S, Berman S (2006) Quantifying and interpreting functional diversity of natural communities: practical considerations matter. Preslia 78:481–501
Lloyd KM, Pollock ML, Mason NWH, Lee WG (2010) Leaf trait-palatability relationships differ between ungulate species: evidence from cafeteria experiments using naive tussock grasses. N Z J Ecol 34:219–226
Mason NW, Carswell FE, Richardson SJ, Burrows LE (2011) Leaf palatability and decomposability increase during a 200-year-old post-cultural woody succession in New Zealand. J Veg Sci 22:6–17
Matthews JA (1992) The ecology of recently deglaciated terrain: a geoecological approach to glacier forelands. Cambridge University Press, Cambridge
McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059
McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185
Miller-Rushing AJ, Primack RB (2008) Global warming and flowering times in Thoreau’s Concord: a community perspective. Ecology 89:332–341
Monti A, Di Virgilio N, Venturi G (2008) Mineral composition and ash content of six major energy crops. Biomass Bioenerg 32:216–223
Mouillot D, Stubbs W, Faure M, Dumay O, Tomasini JA, Wilson J, Chi TD (2005) Niche overlap estimates based on quantitative functional traits: a new family of non-parametric indices. Oecologia 145:345–353
Nafziger ED, Koller HR (1976) Influence of leaf starch concentration on CO2 assimilation in soybean. Plant Physiol 57:560–563
Navas ML, Ducout B, Roumet C, Richarte J, Garnier J, Garnier E (2003) Leaf life span, dynamics and construction cost of species from Mediterranean old fields differing in successional status. New Phytol 159:213–228
Navas ML, Roumet C, Bellmann A, Laurent G, Garnier E (2010) Suites of plant traits in species from different stages of a Mediterranean secondary succession. Plant Biol 12:183–196
Ovington JD, Heitkamp D (1960) The accumulation of energy in forest plantations in Britain. J Ecol 48:639–646
Patton AR (1943) Seasonal changes in the lignin and cellulose content of some Montana grasses. II. J Anim Sci 2:59–62
Penning DVF, Brunsting AH, van Laar HH (1974) Products, requirements and efficiency of biosynthesis: a quantitative approach. J Theor Biol 45:339–377
Pierce S, Brusa G, Vagge I, Cerabolini BE (2013) Allocating CSR plant functional types: the use of leaf economics and size traits to classify woody and herbaceous vascular plants. Funct Ecol 27:1002–1010
Prach K, Walker LR (2011) Four opportunities for studies of ecological succession. Trends Ecol Evol 26:119–123
Raevel V, Violle C, Munoz F (2012) Mechanisms of ecological succession: insights from plant functional strategies. Oikos 121:1761–1770
Raunkiaer C (1934) The life forms of plants and statistical plant geography; being the collected papers of C. Raunkiaer. Clarendon Press, Oxford
Roche P, Diaz-Burlinson N, Gachet S (2004) Congruency analysis of species ranking based on leaf traits: which traits are the more reliable? Plant Ecol 174:37–48
Schneider ED, Kay JJ (1994) Life as a manifestation of the second law of thermodynamics. Math Comput Model 19:25–48
Shipley B, Vu TT (2002) Dry matter content as a measure of dry matter concentration in plants and their parts. New Phytol 153:359–364
Suding KN, Lavorel S, Chapin FS, Cornelissen JHC, Diaz 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. Glob Change Biol 14:1125–1140
Toussaint O, Schneider ED (1998) The thermodynamics and evolution of complexity in biological systems. Comp Biochem Physiol 120:3–9
Vile D, Shipley B, Garnier E (2006) A structural equation model to integrate changes in functional strategies during old-field succession. Ecology 87:504–517
Villar R, Merino J (2001) Comparison of leaf construction costs in woody species with differing leaf life-spans in contrasting ecosystems. New Phytol 151:213–226
Violle C, Jiang L (2009) Towards a trait-based quantification of species niche. J Plant Ecol 2:87–93
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
Williams K, Percival F, Merino J, Mooney H (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant Cell Environ 10:725–734
Wilson JB (1999) Assembly rules in plant communities. In: Weiher E, Keddy PA (eds) Ecological assembly rules: perspectives, advances, retreats. Cambridge University Press, Cambridge, pp 130–164
Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Funct Ecol 15:423–434
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin FS, 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 Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The world-wide leaf economics spectrum. Nature 428:821–827
Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N (2005) Assessing the generality of global leaf trait relationships. New Phytol 166:485–496
Yamamoto SI (2000) Forest gap and tree regeneration. J For Res 5:223–229
Yan ER, Wang XH, Huang JJ (2006) Shifts in plant nutrient use strategies under secondary forest succession. Plant Soil 289:187–197
Zhu ZC (1993) Recovering succession of vegetation in forest region of north Shaanxi Loess Plateau. J Northwest For Coll 8:87–94 (in Chinese with English summary)
Acknowledgments
We thank Ren Jianyi and Cheng Yu for help during the fieldwork, and Li Qian and Zhang Ruichang for critical discussion. The study was financially supported by the S&T Basic Work Program of the Ministry of Science and Technology, China (2011FY110300), Forerunner Projects of the Chinese Academy of Sciences (XDA05050301-4) and the National Science Foundation of China (41571500). The experiments comply with the current laws of China in which the experiments were performed.
Author contribution statement
Y. F. C. and M. Y. designed the study, conducted the analyses and wrote the paper. X. L. and M. W. helped completing the major fieldwork. J. S. X. prepared Fig. 5. R. C. Z. and P. C. W. provided help in the data analyses.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Yu-Long Feng.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chai, Y., Yue, M., Wang, M. et al. Plant functional traits suggest a change in novel ecological strategies for dominant species in the stages of forest succession. Oecologia 180, 771–783 (2016). https://doi.org/10.1007/s00442-015-3483-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-015-3483-3