Abstract
Aims
The stress-dominance hypothesis (SDH) predicts the dominance of environmental filtering under harsh conditions and the dominance of competition in favourable habitats. Here, we aimed to assess the generality of the SDH using both leaf and absorptive root traits and phylogenetic diversity at a large scale.
Methods
We examined the changes in the trait and phylogenetic diversity of six leaf and absorptive root traits along a soil fertility gradient from tropical to boreal forests. Trait and phylogenetic convergence and divergence were tested by the null model approach.
Results
Leaf economic traits (i.e. specific leaf area and leaf nitrogen concentration) and root tissue density (RTD) exhibited a coordinated response to soil fertility gradient, shifting from convergence toward species with conservative leaf traits and low RTD under infertile condition to high trait divergence under fertile soil. Similarly, community phylogenetic structure varied from convergence to divergence along the soil fertility gradient. However, variation in other traits was not consistent with the SDH prediction.
Conclusions
The SDH depends on the trait’s ecological role, and RTD is the most consistent root trait with leaf economic traits that reflect community assembly along soil fertility gradient. These results offer a new perspective for understanding complex integration of above- and belowground assembly processes, and emphasize the importance of incorporating belowground traits and phylogenetic information into community ecology.
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Abbreviations
- SLA:
-
Specific leaf area
- LDMC:
-
Leaf dry matter content
- LN:
-
Leaf nitrogen concentration
- SRL:
-
Specific root length
- RTD:
-
Root tissue density
- RN:
-
Root nitrogen concentration
- SDH:
-
Stress-dominance hypothesis
- CWM:
-
Community-weighted mean
- SES:
-
Standardized effect size
- MPD:
-
Mean pairwise distance
- MNTD:
-
Mean nearest taxon distance
References
Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699
Bernard-Verdier M, Navas ML, Vellend M, Violle C, Fayolle A, Garnier E (2012) Community assembly along a soil depth gradient: contrasting patterns of plant trait convergence and divergence in a Mediterranean rangeland. J Ecol 100:1422–1433
Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745
Butterfield BJ, Bradford JB, Munson S, Gremer J (2017) Aridity increases below-ground niche breadth in grass communities. Plant Ecol 218:385–394
Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. P Natl Acad Sci USA 105:17012–17017
Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715
Chen WL, Zeng H, Eissenstat DM, Guo DL (2013) Variation of first-order root traits across climatic gradients and evolutionary trends in geological time. Glob Ecol Biogeogr 22:846–856
Chen W, Koide RT, Adams TS, DeForest JL, Cheng L, Eissenstat DM (2016) Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. P Natl Acad Sci USA 113:8741–8746
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366
Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, Steege H, Morgan HD, MGA H, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380
Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–126
Costa DS, Gerschlauer F, Pabst H, Kuhnel A, Huwe B, Kiese R, Kuzyakov Y, Kleyer M (2017) Community-weighted means and functional dispersion of plant functional traits along environmental gradients on Mount Kilimanjaro. J Veg Sci 28:684–695
Coyle JR, Halliday FW, Lopez BE, Palmquist KA, Wilfahrt PA, Hurlbert AH (2014) Using trait and phylogenetic diversity to evaluate the generality of the stress-dominance hypothesis in eastern north American tree communities. Ecography 37:814–826
de la Riva EG, Tosto A, Perez-Ramos IM, Navarro-Fernandez CM, Olmo M, Anten NPR, Maranon T, Villar R (2016) A plant economics spectrum in Mediterranean forests along environmental gradients: is there coordination among leaf, stem and root traits? J Veg Sci 27:187–199
Diaz S, Lavorel S, de Bello F, Quetier F, Grigulis K, Robson M (2007) Incorporating plant functional diversity effects in ecosystem service assessments. P Natl Acad Sci USA 104:20684–20689
Domínguez MT, Aponte C, Perez-Ramos IM, Garcia LV, Villar R, Maranon T (2012) Relationships between leaf morphological traits, nutrient concentrations and isotopic signatures for Mediterranean woody plant species and communities. Plant Soil 357:407–424
Garnier E, Cortez J, Billes G, Navas ML, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellmann A, Neill C, Toussaint JP (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637
Grime JP (2006) Trait convergence and trait divergence in herbaceous plant communities: mechanisms and consequences. J Veg Sci 17:255–260
Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011) Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. J Ecol 99:954–963
Kong DL, Wang JJ, Kardol P, Wu HF, Zeng H, Deng XB, Deng Y (2016) Economic strategies of plant absorptive roots vary with root diameter. Biogeosciences 13:415–424
Kraft NJB, Cornwell WK, Webb CO, Ackerly DD (2007) Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170:271–283
Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104:1299–1310
Laliberte E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103
Lhotsky B, Kovacs B, Onodi G, Csecserits A, Redei T, Lengyel A, Kertesz M, Botta-Dukat Z (2016) Changes in assembly rules along a stress gradient from open dry grasslands to wetlands. J Ecol 104:507–517
Ma ZQ, Guo DL, Xu XL, Lu M, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO (2018) Evolutionary history resolves global organization of root functional traits. Nature 555:94–97
Maire V, Gross N, Börger L, Proulx R, Wirth C, Pontes LS, Soussana JF, Louault F (2012) Habitat filtering and niche differentiation jointly explain species relative abundance within grassland communities along fertility and disturbance gradients. New Phytol 196:497–509
de Martonne E (1926) L'indice d'aridité. Bulletin de l'Association de géographes français 3:3–5
Mason NW, de Bello F, Doležal J, Lepš J (2011) Niche overlap reveals the effects of competition, disturbance and contrasting assembly processes in experimental grassland communities. J Ecol 99:788–796
Mayfield MM, Levine JM (2010) Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Lett 13:1085–1093
McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185
Pavoine S, Gasc A, Bonsall MB, Mason NWH (2013) Correlations between phylogenetic and functional diversity: mathematical artefacts or true ecological and evolutionary processes? J Veg Sci 24:781–793
Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588
Prieto I, Roumet C, Cardinael R, Dupraz C, Jourdan C, Kim JH, Maeght JL, Mao Z, Pierret A, Portillo N, Roupsard O, Thammahacksa C, Stokes A (2015) Root functional parameters along a land-use gradient: evidence of a community-level economics spectrum. J Ecol 103:361–373
Qian H, Jin Y (2016) An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. J Plant Ecol 9:233–239
Reich PB (2014) The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301
Spasojevic MJ, Suding KN (2012) Inferring community assembly mechanisms from functional diversity patterns: the importance of multiple assembly processes. J Ecol 100:652–661
Swenson NG (2014) Functional and phylogenetic ecology in R. Springer, New York
Valencia E, Maestre FT, Le Bagousse-Pinguet Y, Quero JL, Tamme R, Borger L, Garcia-Gomez M, Gross N (2015) Functional diversity enhances the resistance of ecosystem multifunctionality to aridity in Mediterranean drylands. New Phytol 206:660–671
Valverde-Barrantes OJ, Freschet GT, Roumet C, Blackwood CB (2017) A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine-root tissues in seed plants. New Phytol 215:1562–1573
Wang R, Yu G, He N, Wang Q, Zhao N, Xu Z, Ge J (2015) Latitudinal variation of leaf stomatal traits from species to community level in forests: linkage with ecosystem productivity. Sci Rep 5:14454
Wang R, Wang Q, Zhao N, Yu G, He N (2017) Complex trait relationships between leaves and absorptive roots: coordination in tissue N concentration but divergence in morphology. Ecol Evol 7:2697–2705
Wang R, Wang Q, Zhao N, Xu Z, Zhu X, Jiao C, Yu G, He N (2018) Different phylogenetic and environmental controls of first-order root morphological and nutrient traits: evidence of multidimensional root traits. Funct Ecol 32:29–39
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505
Weemstra M, Mommer L, Visser EJW, van Ruijven J, Kuyper TW, Mohren GMJ, Sterck FJ (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169
Weiher E, Keddy PA (1995) Assembly rules, null models, and trait dispersion - new questions front old patterns. Oikos 74:159–164
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 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 worldwide leaf economics spectrum. Nature 428:821–827
Zadworny M, McCormack ML, Żytkowiak R, Karolewski P, Mucha J, Oleksyn J (2016) Patterns of structural and defense investments in fine roots of scots pine (Pinus sylvestris L.) across a strong temperature and latitudinal gradient in Europe. Glob Chang Biol 23:1218–1231
Zemunik G, Turner BL, Lambers H, Laliberte E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:1–4
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31700381), the National Key R&D Program of China (2016YFC0500202, 2017YFA0604803), China Postdoctoral Science Foundation (2017 M623252, 2018 T111101), and the Doctoral Start-up Fund of Northwest A&F University (2452016138). We thank “Functional Trait Database of Terrestrial Ecosystems in China (China_Trait)” for sharing data, further information for other materials should contact to N. He (henp@igsnrr.ac.cn). There are no conflicts of interest to declare.
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Wang, R., Wang, Q., Liu, C. et al. Changes in trait and phylogenetic diversity of leaves and absorptive roots from tropical to boreal forests. Plant Soil 432, 389–401 (2018). https://doi.org/10.1007/s11104-018-3816-1
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DOI: https://doi.org/10.1007/s11104-018-3816-1