Skip to main content
SpringerLink
Log in

Root nutrient concentration and biomass allocation are more plastic than morphological traits in response to nutrient limitation

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Understanding the magnitude of phenotypic plasticity within a species is important, particularly when comparing species from diverse habitats or when using traits from global databases. Our objective was to quantify the magnitude of intraspecific variability of fine root, stem, and leaf traits in response to nutrient availability.

Methods

We measured growth rates and traits from fine roots, stems, and leaves on replicate seedlings of four species grown in two treatments: low and high soil nutrient availability. We used ANOVA to test for effects of fertilizer, species, and their interaction on trait expression, and ranked intraspecific trait variation using the coefficient of variation.

Results

Root nutrient concentration, relative growth rate, and biomass allocation exhibited the most plastic responses to nutrient availability. Specific root length, specific leaf area, root diameter, and wood density were the least variable traits within species. Nutrient limitation only induced greater root branching in the non-mycorrhizal Proteaceae species that produced more cluster roots.

Conclusions

Woody plants respond to nutrient limitation by increasing root mass fraction, rather than by adjusting root morphology or structure. We urge caution when using root tissue chemistry traits obtained from global databases in local studies, as this is one of the most plastic traits in response to nutrient availability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

RGR:

Relative growth rate

SLA:

Specific leaf area

SRL:

Specific root length

References

  • Aerts R, Chapin FS (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    Article  Google Scholar 

  • Aerts R, De Caluwe H, Konings H (1992) Seasonal allocation of biomass and nitrogen in four Carex species from mesotrophic and eutrophic fens as affected by nitrogen supply. J Ecol 80:653–664

    Article  Google Scholar 

  • Aikio S, Mari Markkola A (2002) Optimality and phenotypic plasticity of shoot-to-root ratio under variable light and nutrient availabilities. Evol Ecol 16:67–76. doi:10.1023/A:1016096309637

    Article  Google Scholar 

  • Albornoz FE, Burgess TI, Lambers H, Etchells H, Laliberté E (2016) Native soilborne pathogens equalize differences in competitive ability between plants of contrasting nutrient-acquisition strategies. J Ecol 105:549–557

    Article  Google Scholar 

  • Ames GM, Anderson SM, Wright JP (2016) Multiple environmental drivers structure plant traits at the community level in a pyrogenic ecosystem. Funct Ecol 30:789–798. doi:10.1111/1365-2435.12536

    Article  Google Scholar 

  • Atkin OK, Bloomfield KJ, Reich PB, Tjoelker MG, Asner GP, Bonal D, Bönisch G, Bradford MG, Cernusak LA, Cosio EG (2015) Global variability in leaf respiration in relation to climate, plant functional types and leaf traits. New Phytol. 206:614–636

    Article  CAS  PubMed  Google Scholar 

  • Baltzer JL, Thomas SC (2007) Determinants of whole-plant light requirements in Bornean rain forest tree saplings. J Ecol 95:1208–1221. doi:10.1111/j.1365-2745.2007.01286.x

    Article  Google Scholar 

  • Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699. doi:10.1016/j.tree.2014.10.006

    Article  PubMed  Google Scholar 

  • Berta G, Trotta A, Fusconi A, Hooker JE, Munro M, Atkinson D, Giovannetti M, Morini S, Fortuna P, Tisserant B (1995) Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. Tree Physiol 15:281–293

    Article  CAS  PubMed  Google Scholar 

  • Boot RA, Mensink M (1990) Size and morphology of root systems of perennial grasses from contrasting habitats as affected by nitrogen supply. Plant Soil 129:291–299. doi:10.1007/BF00032425

    Article  CAS  Google Scholar 

  • Borken W, Kossmann G, Matzner E (2007) Biomass, morphology and nutrient contents of fine roots in four Norway spruce stands. Plant Soil 292:79–93

    Article  CAS  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155

    Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260. doi:10.2307/2096908

    Article  CAS  Google Scholar 

  • Chen W, Zeng H, Eissenstat DM, Guo D (2013) Variation of first-order root traits across climatic gradients and evolutionary trends in geological time. Glob Ecol Biogeogr 22:846–856. doi:10.1111/geb.12048

    Article  Google Scholar 

  • Clemensson-Lindell A, Asp H (1995) Fine-root morphology and uptake of 32P and 35S in a Norway spruce (Picea abies (L.) karst.) stand subjected to various nutrient and water supplies. Plant Soil 173:147–155

    Article  CAS  Google Scholar 

  • Comas LH, Eissenstat DM (2009) Patterns in root trait variation among 25 co-existing North American forest species. New Phytol. 182:919–928. doi:10.1111/j.1469-8137.2009.02799.x

    Article  CAS  PubMed  Google Scholar 

  • Comas LH, Callahan HS, Midford PE (2014) Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies. Ecology and evolution 4:2979–2990. doi:10.1002/ece3.1147

    Article  PubMed  PubMed Central  Google Scholar 

  • Coomes DA, Allen RB, Bentley WA, Burrows LE, Canham CD, Fagan L, Forsyth DM, Gaxiola-Alcantar A, Parfitt RL, Ruscoe WA (2005) The hare, the tortoise and the crocodile: the ecology of angiosperm dominance, conifer persistence and fern filtering. J Ecol 93:918–935

    Article  Google Scholar 

  • Craine JM (2009) Resource strategies of wild plants. Princeton University Press, Princeton

    Book  Google Scholar 

  • Cromer R, Jarvis P (1990) Growth and biomass partitioning in Eucalyptus grandis seedlings in response to nitrogen supply. Funct Plant Biol 17:503–515

    CAS  Google Scholar 

  • Drew M (1975) Comparison of the effects of a localised supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol. 75:479–490

    Article  CAS  Google Scholar 

  • Drew M, Saker L, Ashley T (1973) Nutrient supply and the growth of the seminal root system in barley I. The effect of nitrate concentration on the growth of axes and laterals Journal of Experimental Botany 24:1189–1202

    CAS  Google Scholar 

  • Dyer AR, Goldberg DE, Turkington R, Sayre C (2001) Effects of growing conditions and source habitat on plant traits and functional group definition. Funct Ecol 15:85–95

    Article  Google Scholar 

  • Ecroyd C (1982) Biological flora of New Zealand 8. Agathis australis (D. Don) Lindl.(Araucariaceae) kauri. N Z J Bot 20:17–36

    Article  Google Scholar 

  • Eissenstat DM, Kucharski JM, Zadworny M, Adams TS, Koide RT (2015) Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest. New Phytol. 208:114–124

    Article  PubMed  Google Scholar 

  • Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives. Sinauer Associates, Inc., Sunderland

    Google Scholar 

  • Freschet GT, Bellingham PJ, Lyver POB, Bonner KI, Wardle DA (2013) Plasticity in above-and belowground resource acquisition traits in response to single and multiple environmental factors in three tree species. Ecology and evolution 3:1065–1078

    Article  PubMed  PubMed Central  Google Scholar 

  • Freschet GT, Swart EM, Cornelissen JH (2015) Integrated plant phenotypic responses to contrasting above-and below-ground resources: key roles of specific leaf area and root mass fraction. New Phytol. 206:1247–1260

    Article  CAS  PubMed  Google Scholar 

  • Grassein F, Till-Bottraud I, Lavorel S (2010) Plant resource-use strategies: the importance of phenotypic plasticity in response to a productivity gradient for two subalpine species. Ann Bot 106:637–645

    Article  PubMed  PubMed Central  Google Scholar 

  • Gratani L, Covone F, Larcher W (2006) Leaf plasticity in response to light of three evergreen species of the Mediterranean maquis. Trees 20:549–558. doi:10.1007/s00468-006-0070-6

    Article  Google Scholar 

  • Grime JP, Pierce S (2012) The evolutionary strategies that shape ecosystems. John Wiley & Sons, West Sussex

    Book  Google Scholar 

  • Gross K, Peters A, Pregitzer K (1993) Fine root growth and demographic responses to nutrient patches in four old-field plant species. Oecologia 95:61–64. doi:10.1007/BF00649507

    Article  PubMed  Google Scholar 

  • Hetrick B, Wilson G, Leslie J (1991) Root architecture of warm-and cool-season grasses: relationship to mycorrhizal dependence. Can. J. Bot. 69:112–118

    Article  Google Scholar 

  • Hill J, Simpson R, Moore A, Chapman D (2006) Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition. Plant Soil 286:7–19

    Article  CAS  Google Scholar 

  • Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol. 162:9–24

    Article  Google Scholar 

  • 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. doi:10.1111/j.1365-2745.2011.01821.x

    Article  Google Scholar 

  • Hutchings M, de Kroon H (1994) Foraging in plants: the role of morphological plasticity in resource acquisition. Adv Ecol Res 25:159–238

    Article  Google Scholar 

  • Jager MM, Richardson SJ, Bellingham PJ, Clearwater MJ, Laughlin DC (2015) Soil fertility induces coordinated responses of multiple independent functional traits. J Ecol 103:374–385. doi:10.1111/1365-2745.12366

    Article  Google Scholar 

  • Kalliokoski T, Pennanen T, Nygren P, Sievänen R, Helmisaari H-S (2010) Belowground interspecific competition in mixed boreal forests: fine root and ectomycorrhiza characteristics along stand developmental stage and soil fertility gradients. Plant Soil 330:73–89

    Article  CAS  Google Scholar 

  • Kattge J, Diaz S, Lavorel S, Prentice I, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright I (2011) TRY–a global database of plant traits. Glob Chang Biol 17:2905–2935

    Article  PubMed Central  Google Scholar 

  • Keenan TF, Niinemets Ü (2016) Global leaf trait estimates biased due to plasticity in the shade. Nature Plants 3:16201

    Article  PubMed  Google Scholar 

  • Kembel SW, Cahill JF Jr (2011) Independent evolution of leaf and root traits within and among temperate grassland plant communities. PLoS One 6:e19992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein T, Siegwolf RT, Körner C (2016) Belowground carbon trade among tall trees in a temperate forest. Science 352:342–344

    Article  CAS  PubMed  Google Scholar 

  • Knops JM, Reinhart K (2000) Specific leaf area along a nitrogen fertilization gradient. Am Midl Nat 144:265–272

    Article  Google Scholar 

  • Kong D, Ma C, Zhang Q, Li L, Chen X, Zeng H, Guo D (2014) Leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytol. 203:863–872. doi:10.1111/nph.12842

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • de Kroon H, Hutchings MJ (1995) Morphological plasticity in clonal plants: the foraging concept reconsidered. J Ecol 83:143–152. doi:10.2307/2261158

    Article  Google Scholar 

  • Larigauderie A, Richards J (1994) Root proliferation characteristics of seven perennial arid-land grasses in nutrient-enriched microsites. Oecologia 99:102–111

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Li H, Zhu B, Koide RT, Eissenstat DM, Guo D (2015) Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytol. 208:125–136. doi:10.1111/nph.13434

    Article  PubMed  Google Scholar 

  • Louw-Gaume A, Rao I, Gaume A, Frossard E (2010) A comparative study on plant growth and root plasticity responses of two Brachiaria forage grasses grown in nutrient solution at low and high phosphorus supply. Plant Soil 328:155–164. doi:10.1007/s11104-009-0093-z

    Article  CAS  Google Scholar 

  • Lusk CH, Reich PB, Montgomery RA, Ackerly DD, Cavender-Bares J (2008) Why are evergreen leaves so contrary about shade? Trends Ecol Evol 23:299–303

    Article  PubMed  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol. 207:505–518

    Article  PubMed  Google Scholar 

  • Meziane D, Shipley B (1999) Interacting components of interspecific relative growth rate: constancy and change under differing conditions of light and nutrient supply. Funct Ecol 13:611–622

    Article  Google Scholar 

  • Meziane D, Shipley B (2001) Direct and indirect relationships between specific leaf area, leaf nitrogen and leaf gas exchange. Effects of irradiance and nutrient supply Annals of Botany 88:915–927

    Google Scholar 

  • Mokany K, Ash J (2008) Are traits measured on pot grown plants representative of those in natural communities? J Veg Sci 19:119–126

    Article  Google Scholar 

  • Navas M-L, Garnier E (2002) Plasticity of whole plant and leaf traits in Rubia peregrina in response to light, nutrient and water availability. Acta Oecol 23:375–383

    Article  Google Scholar 

  • Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234

    Article  Google Scholar 

  • Poorter H, Niinemets Ü, 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

    Article  PubMed  Google Scholar 

  • Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol. 193:30–50

    Article  CAS  PubMed  Google Scholar 

  • Poorter H, Fiorani F, Pieruschka R, Wojciechowski T, van der Putten WH, Kleyer M, Schurr U, Postma J (2016) Pampered inside, pestered outside? Differences and similarities between plants growing in controlled conditions and in the field. New Phytol. 212:838–855. doi:10.1111/nph.14243

    Article  CAS  PubMed  Google Scholar 

  • Porter JR, Lawlor DW (1991) Plant growth: interactions with nutrition and environment. Cambridge University Press, Cambridge

    Google Scholar 

  • Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine North American trees. Ecol Monogr 72:293–309

    Article  Google Scholar 

  • Roumet C, Urcelay C, Díaz S (2006) Suites of root traits differ between annual and perennial species growing in the field. New Phytol. 170:357–368

    Article  PubMed  Google Scholar 

  • Roumet C, Lafont F, Sari M, Warembourg F, Garnier E (2008) Root traits and taxonomic affiliation of nine herbaceous species grown in glasshouse conditions. Plant Soil 312:69–83

    Article  CAS  Google Scholar 

  • Rozendaal DMA, Hurtado VH, Poorter L (2006) Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature. Funct Ecol 20:207–216. doi:10.1111/j.1365-2435.2006.01105.x

    Article  Google Scholar 

  • Schlichting CD, Levin DA (1986) Phenotypic plasticity: an evolving plant character. Biol J Linn Soc 29:37–47

    Article  Google Scholar 

  • Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125. doi:10.1007/s11104-004-2725-7

    Article  CAS  Google Scholar 

  • Shipley B, De Bello F, Cornelissen JHC, Laliberté E, Laughlin DC, Reich PB (2016) Reinforcing loose foundation stones in trait-based plant ecology. Oecologia 180:923–931. doi:10.1007/s00442-016-3549-x

    Article  PubMed  Google Scholar 

  • Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci. 5:537–542

    Article  CAS  PubMed  Google Scholar 

  • Vaitkus MR, McLeod KW (1995) Photosynthesis and water-use efficiency of two sandhill oaks following additions of water and nutrients. Bulletin of the Torrey Botanical Club 122:30–39

    Article  Google Scholar 

  • Valladares F, Martinez-Ferri E, Balaguer L, Perez-Corona E, Manrique E (2000a) Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy? New Phytol. 148:79–91

    Article  CAS  Google Scholar 

  • Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000b) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecotoxicology 81:1925–1936

    Google Scholar 

  • Valverde-Barrantes OJ, Horning AL, Smemo KA, Blackwood CB (2016) Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms. Plant Soil 404:1–12

    Article  CAS  Google Scholar 

  • Violle C, Reich PB, Pacala SW, Enquist BJ, Kattge J (2014) The emergence and promise of functional biogeography. Proc. Natl. Acad. Sci. U. S. A. 111:13690–13696. doi:10.1073/pnas.1415442111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Visser EJ, Bögemann GM (2003) Measurement of porosity in very small samples of plant tissue. Plant Soil 253:81–90

    Article  CAS  Google Scholar 

  • Yuan C-M, Wu T, Geng Y-F, Chai Y, Hao J-B (2016) Phenotypic plasticity of lianas in response to altered light environment. Ecol Res 31:375–384

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by a grant (UOW1201) from the Royal Society of New Zealand Marsden Fund, and a University of Waikato Research Scholarship. We thank Toni Cornes, Lynne Baxter, Adam Purcell, and Angela Simpson for their assistance in this study.

Author information

Authors and Affiliations

  1. Environmental Research Institute and School of Science, University of Waikato, Private Bag 3105, Hamilton, 3240, New Zealand

    Kris R. Kramer-Walter & Daniel C. Laughlin

  2. Department of Botany, University of Wyoming, 1000 East University Ave, Laramie, WY, 82071, USA

    Daniel C. Laughlin

Authors
  1. Kris R. Kramer-Walter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel C. Laughlin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kris R. Kramer-Walter or Daniel C. Laughlin.

Additional information

Responsible Editor: Hans Lambers.

Electronic supplementary material

ESM 1

(DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kramer-Walter, K.R., Laughlin, D.C. Root nutrient concentration and biomass allocation are more plastic than morphological traits in response to nutrient limitation. Plant Soil 416, 539–550 (2017). https://doi.org/10.1007/s11104-017-3234-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3234-9

Keywords

Search

Navigation