Abstract
To understand impacts of post-disturbance assembly mechanisms on the functional diversity (FD) of plant communities, it is necessary to determine how the environment drives their functional trait composition. In the boreal forest, post-fire abiotic filters may control community assembly by selecting plants with specific traits. Ericaceous heaths are characterized by low FD and are thought to be subject to such filters. We hypothesized that soil parameters select for a specific suite of traits and act as a secondary abiotic filter in post-fire ericaceous heath and contribute to the observed reduction of FD. We measured six soil parameters, five functional traits, and plant species abundances in eight post-fire heath and four regenerating forest sites in Eastern Canada. We conducted a combined analysis of RLQ (R-table Linked to Q-table) and fourth-corner methods to examine the links between plant traits and plot-level soil parameters, mediated by species abundances. Only below ground traits were significantly linked to soil variables. Specific root length and ericoid mycorrhizal associations were negatively linked to total soil nitrogen, available ammonium, and pH. Post-fire heath soils favour a specific suite of species traits. Only a portion of the regional species pool possesses the above-mentioned traits, and when they are favoured by habitat conditions, they assemble into a community with low FD. The novelty of our study is here we show how the relationship between traits and soil chemistry can act as a secondary filter and exert community-level trait changes responsible for the low functional diversity observed in heaths.
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References
Adamczyk S, Kiikkila O, Kitunen V, Smolander A (2013) Potential response of soil processes to diterpenes, triterpenes and tannins: nitrification, growth of microorganisms and precipitation of proteins. Appl Soil Ecol 67:47–52. https://doi.org/10.1016/j.apsoil.2013.02.009
Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573. https://doi.org/10.2307/2960528
Bloom RG, Mallik AU (2006) Relationships between ericaceous vegetation and soil nutrient status in a post-fire Kalmia angustifolia-black spruce chronosequence. Plant Soil 289:211–226. https://doi.org/10.1007/s11104-006-9130-3
Bonner FT, Karrfalt RP (eds) 2008 The woody plant seed manual. USDA Forest Service, Agriculture Handbook 727, USA
Brais S, David P, Ouimet R (2000) Impacts of wild fire severity and salvage harvesting on the nutrient balance of jack pine and black spruce boreal stands. For Ecol Manag 137:231–243. https://doi.org/10.1016/S0378-1127(99)00331-X
Canadensys (2015) Vascan: database of vascular plants in Canada. Accessed 10 Dec 2015. http://data.canadensys.net/vascan/search?lang=en
Caplan JS, Stone BWG, Faillace CA, Lafond JJ, Baumgarten JM, Mozdzer TJ, Dighton J, Meiners SJ, Grabosky JC, Erenfeld JG (2017) Nutrient foraging strategies are associated with productivity and population growth in forest shrubs. Ann Bot 119:977–988. https://doi.org/10.1093/aob/mcw271
Caplan JS, Meiners SJ, Flores-Moreno H, McCormack ML (2019) Fine-root traits are linked to species dynamics in a successional plant community. Ecology 100:e02588. https://doi.org/10.1002/ecy.2588
Carbognani M, Petraglia A, Tomaselli M (2014) Warming effects and plant trait control on the early decomposition in alpine snowbeds. Plant Soil 376:277–290. https://doi.org/10.1007/s11104-013-1982-8
Cornelissen J, Aerts R, Cerabolini B, Werger M, van der Heijden MGA (2001) Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129:611–619. https://doi.org/10.1007/s004420100752
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. Aust J Bot 51:335. https://doi.org/10.1071/BT02124
Damman AWH (1983) An ecological subdivision of the island of Newfoundland. In: South R (ed) Biogeography and ecology of the Island of Newfoundland. Junk Publishers, The Netherlands, pp 163–206
Dolédec S, Chessel D, ter Braak CJF, Champely S (1996) Matching species traits to environmental variables: a new three-table ordination method. Environ Ecol Stat 3:143–166. https://doi.org/10.1007/BF02427859
Dray S, Choler P, Dolédec S, Peres-Neto PR, Thuiller W, Pavoine S, ter Braak CJF (2014) Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation. Ecology 95:14–21. https://doi.org/10.1890/13-0196.1
Eichenberg D, Trogisch S, Huang Y, He J-S, Bruelheide H (2015) Shifts in community leaf functional traits are related to litter decomposition along a secondary forest succession series in subtropical China. J Plant Ecol 8:401–410. https://doi.org/10.1093/jpe/rtu021
Environment Canada (2017) Canadian climate normals, Gambo, NL, 1981–2010. http://climate.weather.gc.ca/
Francis R, Read DJ (1995) Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Can J Bot 73:1301–1309. https://doi.org/10.1139/b95-391
Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194. https://doi.org/10.1086/283244
Hill MO, Smith AJE (1976) Principal component analysis of taxonomic data with multi-state discrete characters. Taxon 25:249–255
Inderjit, Mallik AU (1996) The nature of interference potential of Kalmia angustifolia. Can J For Res 26:1899–1904. https://doi.org/10.1139/x26-214
Inderjit, Malik AU (1999) Nutrient status of black spruce (Picea mariana [Mill.] BSP) forest soils dominated by Kalmia angustifolia L. Acta Oecol 20:87–92
Inderjit, Mallik AU (2002) Can Kalmia angustifolia interference to black spruce (Picea mariana) be explained by allelopathy? For Ecol Manag 160:75–84. https://doi.org/10.1016/S0378-1127(01)00463-7
Inderjit, van der Putten WH (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25:512–519. https://doi.org/10.1016/j.tree.2010.06.006
Joanisse GD, Bradley RL, Preston CM, Bending GD (2009) Sequestration of soil nitrogen as tannin-protein complexes may improve the competitive ability of sheep laurel (Kalmia angustifolia) relative to black spruce (Picea mariana). New Phytol 181:187–198. https://doi.org/10.1111/j.1469-8137.2008.02622.x
Johnstone JF, Hollingsworth TN, Chapin FS, Mack MC (2010) Changes in fire regime break the legacy lock on successional trajectories in Alaskan boreal forest. Glob Chang Biol 16:1281–1295. https://doi.org/10.1111/j.1365-2486.2009.02051.x
Jung V, Violle C, Mondy C, Hoffman L, Muller S (2010) Intraspecific variability and trait-based community assembly: Intraspecific variability and community assembly. J Ecol 98:1134–1140. https://doi.org/10.1111/j.1365-2745.2010.01687.x
Keddy PA (1992) Assembly and response rules: two goals for predictive community ecology. J Veg Sci 3:157–164. https://doi.org/10.2307/3235676
Kraft NJB, Adler PB, Godoy O, James EC, Fuller S, Levine JM (2015) Community assembly, coexistence and the environmental filtering metaphor. Funct Ecol 29:592–599. https://doi.org/10.1111/1365-2435.12345
Lasky JR, Sun I-F, Su S-H, Chen Z-S, Keitt TH (2013) Trait-mediated effects of environmental filtering on tree community dynamics. J Ecol 101:722–733. https://doi.org/10.1111/1365-2745.12065
Legendre P, Galzin R, Harmelin-Vivien ML (1997) Relating behavior to habitat: solutions to the fourth-corner problem. Ecology 78:547–562. https://doi.org/10.1890/0012-9658(1997)078[0547:RBTHST]2.0.CO;2
Mallik AU (1987) Allelopathic potential of Kalmia angustifolia to black spruce. For Ecol Manag 20:43–51
Mallik AU (1993) Ecology of a forest weed of Newfoundland: vegetative regeneration strategy of Kalmia angustifolia. Can J Bot 71:161–166. https://doi.org/10.1139/b93-018
Mallik AU (1995) Conversion of temperate forests into heaths: role of ecosystem disturbance and ericaceous plants. Environ Manag 19:675–684. https://doi.org/10.1007/BF02471950
Mallik AU, Bloom RG, Whisenant SG (2010) Seedbed filter controls post-fire succession. Basic Appl Ecol 11:170–181. https://doi.org/10.1016/j.baae.2009.11.005
Mallik AU, Wang JR, Siegwart-Collier LS, Roberts BA (2012) Morphological and ecophysiological responses of sheep laurel (Kalmia angustifolia L.) to shade. Forestry 85:513–522. https://doi.org/10.1093/forestry/cps047
Mallik AU, Biswas SR, Collier LCS (2016) Belowground interactions between Kalmia angustifolia and Picea mariana: roles of competition, root exudates and ectomycorrhizal association. Plant Soil 403:471–483. https://doi.org/10.1007/s11104-016-2819-z
Miki T, Kondoh M (2002) Feedbacks between nutrient cycling and vegetation predict plant species coexistence and invasion. Ecol Lett 5:624–633. https://doi.org/10.1046/j.1461-0248.2002.00347.x
Miles J, Young WF (1980) The effects on heathland and moorland soils in Scotland and northern England following colonization by birch (Betula spp.). Bul d’Ecol 11:233–242
Mommer L, Visser EJW, van Ruijven J, de Caluwe H, Pierik R, de Kroon H (2011) Contrasting root behaviour in two grass species: a test of functionality in dynamic heterogeneous conditions. Plant Soil 344:347–360. https://doi.org/10.1007/s11104-011-0752-8
Nilsson M-C, Högberg P, Zackrisson O, Fengyou W (1993) Allelopathic effects by Empetrum hermaphroditum on development and nitrogen uptake by roots and mycorrhizae of Pinus silvestris. Can J Bot 71:620–628. https://doi.org/10.1139/b93-071
Pakeman RJ (2011) Functional diversity indices reveal the impacts of land use intensification on plant community assembly. J Ecol 99:1143–1151. https://doi.org/10.1111/j.1365-2745.2011.01853.x
Perkins LB, Nowak RS (2013) Native and non-native grasses generate common types of plant–soil feedbacks by altering soil nutrients and microbial communities. Oikos 122:199–208. https://doi.org/10.1111/j.1600-0706.2012.20592.x
Power R (2000) Vegetation management plan for Terra Nova National Park 2000–2004. Parks Canada, Terra Nova National Park
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Ravenek JM, Mommer L, Visser EJW, van Ruijven J, van der Paauw JW, Smit-Tiekstra A, de Caluwe H, de Kroon H (2016) Linking root traits and competitive success in grassland species. Plant Soil 407:39–53. https://doi.org/10.1007/s11104-016-2843-z
Read DJ (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot 77:365–374. https://doi.org/10.1006/anbo.1996.0044
Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can. J. Bot 82:1243–1263. https://doi.org/10.1139/b04-123
Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J of Ecol 102:275–301. https://doi.org/10.1111/1365-2745.12211
Revilla TA, Veen(Ciska)Eppinga GFMB, Weissing FJ (2013) Plant–soil feedbacks and the coexistence of competing plants. Theor Ecol 6:99–113. https://doi.org/10.1007/s12080-012-0163-3
Shenoy A, Johnstone JF, Kasischke ES, Kielland K (2011) Persistent effects of fire severity on early successional forests in interior Alaska. For Ecol Manag 261:381–390. https://doi.org/10.1016/j.foreco.2010.10.021
Siegwart Collier LC, Mallik AU (2010) Does post-fire abiotic habitat filtering create divergent plant communities in black spruce forests of eastern Canada? Oecologia 164:465–477. https://doi.org/10.1007/s00442-010-1642-0
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York, p 814
Smithwick EAH, Turner MG, Mack MC, Chapin FS (2005) Postfire soil N cycling in northern conifer forests affected by severe, stand-replacing wildfires. Ecosystems 8:163–181. https://doi.org/10.1007/s10021-004-0097-8
Soil Classification Working Group (1998) Canadian soil classification system, 3rd edn. Agriculture and Agri-Food Canada Publication 1646, NRC Press, Canada
St. Martin P, Mallik AU (2016) Growth release of stunted black spruce (Picea mariana) in Kalmia heath: the role of ectomycorrhizal fungi and near-ground microclimate. Can J For Res 46:666–673. https://doi.org/10.1139/cjfr-2015-0267
St. Martin P, Malik AU (2017) The status of non-vascular plants in trait-based ecosystem function studies. Perspect Plant Ecol Evol Syst 27:1–8. https://doi.org/10.1016/j.ppees.2017.04.002
St. Martin P, Mallik AU (2019) Alternate successional pathway yields alternate pattern of functional diversity. J Veg Sci 30:461–470. https://doi.org/10.1111/jvs.12740
Suding KN, Larson JR, Thorsos E, Stelzer H, Bowman WD (2004) Species effects on resource supply rates: do they influence competitive interactions? Plant Ecol 175:47–58
von Oheimb G, Power SA, Falk K, Friedrich U, Mohamed A, Krug A, Boschatzke N, Härdtle W (2010) N: P ratio and the nature of nutrient limitation in Calluna-dominated Heathlands. Ecosystems 13:317–327. https://doi.org/10.1007/s10021-010-9320-y
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 (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Wurzburger N, Hendrick RL (2009) Plant litter chemistry and mycorrhizal roots promote a nitrogen feedback in a temperate forest. J Ecol 97:528–536. https://doi.org/10.1111/j.1365-2745.2009.01487.x
Yamasaki SH, Fyles JW, Titus BD (2002) Interactions among Kalmia angustifolia, soil characteristics, and the growth and nutrition of black spruce seedlings in two boreal Newfoundland plantations of contrasting fertility. Can J For Res 32:2215–2224. https://doi.org/10.1139/x02-119
Zeng RS, Mallik AU (2006) Selected ectomycorrhizal fungi of black spruce (Picea mariana) can detoxify phenolic compounds of Kalmia angustifolia. J Chem Ecol 32:1473–1489. https://doi.org/10.1007/s10886-006-9063-6
Zhu H, Mallik AU (1994) Interactions between Kalmia and black spruce: isolation and identification of allelopathic compounds. J Chem Ecol 20:407–421. https://doi.org/10.1007/BF02064447
Acknowledgements
This work was supported by a National Sciences and Engineering Research Council Discovery Grant (NSERC DG) awarded to AUM (grant number 2014-06239). We would like to thank Colin St. James and Regina Lauffer for fieldwork assistance and the staff of Terra Nova National Park for logistical help.
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PSM and AUM conceived and designed the experiment. PSM collected the data and performed the analyses. PSM and AUM wrote and revised the manuscript.
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Communicated by Edith B. Allen.
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St. Martin, P., Mallik, A.U. Soil chemistry drives below ground traits in an alternate successional pathway from forest to heath. Oecologia 195, 469–478 (2021). https://doi.org/10.1007/s00442-021-04864-4
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DOI: https://doi.org/10.1007/s00442-021-04864-4