Abstract
Soil resource heterogeneity has clear effects on plant root development and overall plant performance. Here we test whether contrasting vegetation types have similar or different responses to soil patches of differing resource availability. We examined the fine root responses of grassland and forest vegetation at the northern edge of the Great Plains to transplanted patches of resource-poor and resource-rich soils, using rhizotron imaging. Every aspect of measured root behavior, including root length, production, mortality, turnover, variability and size distribution, varied significantly between patch types, and most aspects also varied between vegetation types. Most importantly, differential responses to patches between grassland and forest were shown by significant interactions between patch type and vegetation for two response variables. First, root length variability was significantly lower in resource-rich compared to resource-poor patches in forest but not grassland. Second, the proportion of very fine roots was significantly greater in resource-rich than resource-poor patches in forests but not grassland. Thus, compared to grassland, forest more fully occupied resource-rich patches relative to resource-poor patches by allocating more growth to very fine roots. We report the first example of significant differences between vegetation types (grassland and forest) in root responses to soil resource heterogeneity measured in a field experiment. The relatively high ability of forest roots to more fully occupy resource-rich patches is consistent with the global expansion of woody vegetation and associated increases in soil heterogeneity.
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References
Anderson TM, Starmer WT, Thorne M (2007) Bimodal root diameter distributions in Serengeti grasses exhibit plasticity in response to defoliation and soil texture: implications for nitrogen uptake. Funct Ecol 21:50–60
Archibold OW, Ripley EA, Bretell DL (1996) Comparison of the microclimates of a small aspen grove and adjacent prairie in Saskatchewan. Am Midl Nat 136:248–261
Belsky AJ, Canham CD (1994) Gaps, patches, and isolated trees: a comparison of the patch dynamics of forest gaps and savanna trees. Bioscience 44:77–84
Brassard BW, Chen HYH, Bergeron Y, Paré D (2011) Differences in fine root productivity between mixed- and single-species stands. Funct Ecol 25:238–246
Cahill JF, McNickle GG, Haag JJ, Lamb EG, Nyanumba SM, St Clair CC (2010) Plants integrate information about nutrients and neighbors. Science 328:1657
Comas LH, Eissenstat DM (2009) Patterns in root trait variation among 25 co-existing North American forest species. New Phytol 182:919–928
Curiel Yuste J, Baldocchi DD, Gershenson A, Mission L, Wong S (2007) Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture. Glob Change Biol 13:1–8
Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecol Lett 14:709–722
Fiala K, Tůma I, Holub P (2009) Effect of manipulated rainfall on root production and plant belowground dry mass of different grassland ecosystems. Ecosystems 12:906–914
Garcia-Palacios P, Maestre FT, Bardgett RD, de Kroon H (2012) Plant responses to soil heterogeneity and global environmental change. J Ecol 100:1303–1314
Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31
He WM, Alpert P, Yu FH, Zhang LL, Dong M (2011) Reciprocal and coincident patchiness of multiple resources differentially affect benefits of clonal integration in two perennial plants. J Ecol 99:1202–1210
Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends Ecol Evol 7:336–339
Hodge A (2003) Plant nitrogen capture from organic matter as affected by spatial dispersion, interspecific competition and mycorrhizal colonization. New Phytol 157:303–314
Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant, Cell Environ 22:811–820
Huntly N, Inouye R (1988) Pocket gophers in ecosystems: patterns and mechanisms. Bioscience 38:786–793
Jackson RB, Caldwell MM (1989) The timing and degree of root proliferation in fertile-soil microsites of three cold-desert perennials. Oecologia 81:149–153
Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411
Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Nat Acad Sci USA 94:7362–7366
James JJ, Mangold JM, Sheley RL, Svejcar T (2009) Root plasticity of native and invasive Great Basin species in response to soil nitrogen heterogeneity. Plant Ecol 202:211–220
Jansen C, Van de Steeg HM, De Kroon H (2005) Investigating a trade-off in root morphological responses to a heterogeneous nutrient supply and to flooding. Funct Ecol 19:952–960
Jobbagy EG, Jackson RB (2004) The uplift of soil nutrients by plants: biogeochemical consequences across scales. Ecology 85:2380–2389
Johnson MS, Lehmann J (2006) Double-funneling of trees: stemflow and root-induced preferential flow. Ecoscience 13:324–333
Kembel SW, Cahill JF (2005) Plant phenotypic plasticity belowground: a phylogenetic perspective on root foraging trade-offs. Am Nat 166:216–230
Kleb HR, Wilson SD (1997) Vegetation effects on soil resource heterogeneity in prairie and forest. Am Nat 150:283–298
Knapp AK, Smith MD (2001) Variation among biomes in temporal dynamics of aboveground primary productivity. Science 291:481–484
Knapp AK, Briggs JM, Collins SL, Archer SR, Bret-Harte MS, Ewers BE, Peters DP, Young DR, Shaver GR, Pendall E, Cleary MB (2008) Shrub encroachment in North American grasslands: shifts in growth form dominance rapidly alters control of ecosystem carbon inputs. Glob Change Biol 14:615–623
Köchy M, Wilson SD (2001) Nitrogen deposition and forest expansion in the northern Great Plains. J Ecol 89:807–817
Kosola KR, Eissenstat DM, Graham JH (1995) Root demography of mature citrus trees: the influence of Phytophthora nicotianae. Plant Soil 171:283–288
Leffler AJ, Peek MS, Ryel RJ, Ivans CY, Caldwell MM (2005) Hydraulic redistribution through the root systems of senesced plants. Ecology 86:633–642
Lunt ID, Winsemius LM, McDonald SP, Morgan JW, Dehaan RL (2010) How widespread is woody plant encroachment in temperate Australia? Changes in woody vegetation cover in lowland woodland and coastal ecosystems in Victoria from 1989 to 2005. J Biogeogr 37:722–732
MacDougall AS, Wilson SD (2011) The invasive grass Agropyron cristatum doubles belowground productivity but not soil carbon. Ecology 92:657–664
Månsson K, Bengtson P, Falkengren-Grerup U, Bengtsson G (2009) Plant-microbial competition for nitrogen uncoupled from soil C:N ratios. Oikos 118:1908–1916
Moar SEL, Wilson SD (2006) Root responses to nutrient patches in forest and grassland. Plant Ecol 184:157–162
Mokany K, Raison RJ, Prokushkin AS (2006) Critical analysis of root: shoot ratios in terrestrial biomes. Glob Change Biol 12:84–96
Mommer L, Visser EJ, Wvan 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
Pärtel M, Helm A (2007) Invasion of woody species into temperate grasslands: relationship with abiotic and biotic soil resource heterogeneity. J Veg Sci 18:63–70
Pärtel M, Wilson SD (2001) Root and leaf production, mortality and longevity in response to soil heterogeneity. Funct Ecol 15:748–753
Pärtel M, Wilson SD (2002) Root dynamics and spatial pattern in prairie and forest. Ecology 83:1199–1203
Pärtel M, Laanisto L, Wilson SD (2008) Soil nitrogen and carbon heterogeneity in woodlands and grasslands: contrasts between temperate and tropical regions. Glob Ecol Biogeogr 17:18–24
Pinno BD, Wilson SD (2011) Ecosystem carbon changes with woody encroachment of grassland in the northern Great Plains. Ecoscience 18:157–163
Pregitzer KS, Zak DR, Talhelm AF, Burton AJ, Eikenberry JR (2011) Nitrogen turnover in the leaf litter and fine roots of sugar maple. Ecology 91:3456–3462
Qian P, Schoenau JJ (2002) Practical applications of ion exchange resins in agriculture and environmental soil research. Can J Soil Sci 82:9–21
Questad EJ, Foster BL (2008) Coexistence through spatio-temporal heterogeneity and species sorting in grassland plant communities. Ecol Lett 11:717–726
Rajaniemi TK (2011) Competition for patchy soil resources reduces community evenness. Oecologia 165:169–174
Rajaniemi TK, Reynolds HL (2004) Root foraging for patchy resources in eight herbaceous plant species. Oecologia 141:519–525
Robinson D (1994) The responses of plant and their roots to non-uniform supplies of nutrients. New Phytol 127:635–674
Robinson D, Hodge A, Griffiths BS, Fitter AH (1999) Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proc R Soc London B 266:431–435
Sala OE, Parton WJ, Joyce LA, Lauenroth WK (1988) Primary production of the central grassland region of the United States. Ecology 69:40–45
Schlesinger WH, Reynolds JF, Cunningham GL, Huenneke LF, Jarrell WM, Virginia RA, Whitford WG (1990) Biological feedbacks in global desertification. Science 247:1043–1048
Šmilauerová M, Šmilauer P (2006) Co-occurring graminoid and forb species do not differ in their root morphological response to soil heterogeneity. Folia Geobot 41:121–135
Šmilauerová M, Šmilauer P (2010) First come, first served: grasses have a head start on forbs with prompt nutrient patch occupation. Plant Soil 328:327–336
Soil Classification Working Group (1998) The Canadian system of soil classification, 3rd edn. Agriculture and Agri-Food Canada, NRC Research Press, Ottawa. Publication 1646
Steinaker DF, Wilson SD (2005) Belowground litter contributions to nitrogen cycling at a northern grassland-forest boundary. Ecology 86:2825–2833
Steinaker DF, Wilson SD (2008a) Phenology of fine roots and leaves in forest and grassland. J Ecol 96:1222–1229
Steinaker DF, Wilson SD (2008b) Scale and density dependent relationships among roots, mycorrhizal fungi and collembolan in grassland and forest. Oikos 117:703–710
Strand AE, Pritchard SG, McCormack ML, Davis MA, Oren R (2008) Irreconcilable differences: fine-root life spans and soil carbon persistence. Science 319:456–458
Taub DR, Goldberg D (1996) Root system topology of plants from habitats differing in soil resource availability. Funct Ecol 10:258–264
Tilman D (1987) Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol Monogr 57:189–214
Umbanhowar CE (1992) Abundance, vegetation, and environment of four patch types in a northern mixed prairie. Can J Bot 70:277–284
van der Waal C, de Kroon H, Heitkonig IMA, Skidmore AK, van Langevelde F, de Boer WF, Slotow R, Grant RC, Peel MPS, Kohi EM, de Knegt HJ, Prins HHT (2011) Scale of nutrient patchiness mediates resource partitioning between trees and grasses in a semi-arid savanna. J Ecol 99:1124–1133
Van Rees KCJ, Comerford NB (1986) Vertical root distribution and strontium uptake of a slash pine stand on a Florida spodosol. Soil Sci Soc Am J 50:1042–1046
Webster R, Oliver MA (1990) Statistical methods in soil and land resource survey. Oxford University Press, New York
Wilson SD (2000) Heterogeneity, diversity, and scale in plant communities. In: Hutchings MJ, John EA, Stewart AJ (eds) Ecological consequences of habitat heterogeneity. Blackwell Science, Oxford, pp 53–69
Zobel M, Moora M, Herben T (2010) Clonal mobility and its implications for spatio-temporal patterns of plant communities: what do we need to know next? Oikos 119:802–806
Acknowledgments
We thank M. Jakubowski and K. Tollefson for field assistance, V. Balogianni, B. Kishchuk, B. Brassard and D. Steinaker for helpful comments, and the Natural Sciences and Engineering Research Council of Canada and the Faculty of Science of the University of Regina for support.
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Pinno, B.D., Wilson, S.D. Fine root response to soil resource heterogeneity differs between grassland and forest. Plant Ecol 214, 821–829 (2013). https://doi.org/10.1007/s11258-013-0210-1
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DOI: https://doi.org/10.1007/s11258-013-0210-1