Plant and Soil

, Volume 443, Issue 1–2, pp 353–368 | Cite as

Field-scale variability in site conditions explain phenotypic plasticity in response to nitrogen source in Pinus radiata D. Don

  • Marta GallartEmail author
  • Jonathan Love
  • Dean F. Meason
  • Graham Coker
  • Peter W. Clinton
  • Jianming Xue
  • Paula E. Jameson
  • Jaroslav Klápště
  • Matthew H. Turnbull
Regular Article



Productivity of forest ecosystems is constrained by site resource availability and utilisation at an individual tree level. A better understanding of nitrogen (N) nutrition addition to forest ecosystems is critical for maintaining optimal plantation productivity, given the influence of an environment gradient, genetics, and their interactions.


We studied the aboveground growth response in a plantation setting of ten commercial P. radiata genotypes to N-fertilisation using three different N sources, and also assessed the effect of on-site environmental factors on this response. We compared, on equimolar basis, the effect of N-fertilisation with inorganic N (NH4NO3), organic N (L-arginine), and the two N sources combined (L-arginine:NO3) to that of unfertilised trees on tree height, diameter, descriptors of microsite variability, and climate and seasonal information. After 2.5 years of fertilisation, genotype-specific variation in aboveground growth response to N sources were measured, and these were significantly influenced by field-scale heterogeneity.


Across P. radiata genotypes, trees treated with inorganic N forms showed suppressed growth compared to unfertilised trees, while trees fertilised with organic N (either alone or in combination with inorganic N) were not significantly different than the untreated controls. We provide evidence of significant interactions between N source and genotype, N source and cover as well as genotype and microsite variability affecting temporal trends in tree volume.


We conclude that the comprehension of field-scale variability in soil properties and associated environmental variables is essential for understanding genotype performance as they are crucial determinants of intraspecific variation in response to N-fertilisation.


Phenotypic plasticity Pinus radiata Forest ecosystems G x E Genotype-by-environment interaction Genotype Organic N N source Microsite variation Apparent electrical conductivity Understory vegetation ECa Field-scale variability Temporal variation 



This research was supported by the Growing Confidence in Forestry’s Future programme, which is jointly funded by the New Zealand Ministry of Business, Innovation and Employment (contract No C04X1306) and the Forest Growers Levy Trust (Wellington, New Zealand). The author was supported by scholarships from the New Zealand Forest Research Institute (Scion, Rotorua, New Zealand) and the University of Canterbury. We thank Alan Leckie, Dave Conder, Marie Heaphy, Mike Carson, Juan Rodríguez-Gamir, Mariona Roigé and Torgny Näsholm for their kind advice and valuable technical skills.

Supplementary material

11104_2019_4237_MOESM1_ESM.doc (82 kb)
ESM 1 (DOC 81 kb)


  1. Beamish D (2011) Low induction number, ground conductivity meters: A correction procedure in the absence of magnetic effects. J Appl Geophys 75:244–253. CrossRefGoogle Scholar
  2. Boczulak SA, Hawkins BJ, Roy R (2014) Temperature effects on nitrogen form uptake by seedling roots of three contrasting conifers. Tree Physiol 34:513–523. CrossRefPubMedGoogle Scholar
  3. Bongarten BC, Cregg BM, Dougherty PM, Hennessey TC (1987) Physiology and genetics of tree growth response to moisture and temperature stress: an examination of the characteristics of loblolly pine (Pinus taeda L.). Tree Physiol 61:41–61.
  4. Brackin R, Näsholm T, Robinson N et al (2015) Nitrogen fluxes at the root-soil interface show a mismatch of nitrogen fertilizer supply and sugarcane root uptake capacity. Sci Rep 5:15727. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155.
  6. Bradshaw AD (2006) Unravelling phenotypic plasticity - why should we bother? New Phytol 170:644–648. CrossRefPubMedGoogle Scholar
  7. Brevik EC, Fenton TE, Lazari A (2006) Soil electrical conductivity as a function of soil water content and implications for soil mapping. Precis Agric 7:393–404. CrossRefGoogle Scholar
  8. Britto DT, Kronzucker HJ (2013) Ecological significance and complexity of N-source preference in plants. Ann Bot 112:957–963. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Burdon R (1976) Foliar macronutrient concentrations and foliage retention in radiata pine clones on four sites. New Zeal J For Sci 5:250–259Google Scholar
  10. Burdon R, Shelbourne C (1971) Breeding populations for recurrent selection: conflicts and possible solutions. New Zeal J For Sci 1:174–193Google Scholar
  11. Burdon RD, Britton RAJ, Walford GB (2001) Wood stiffness and bending strength in relation to density in four native provenances of Pinus radiata. New Zeal J For Sci 31:130–146Google Scholar
  12. Burdon R, Carson M, Shelbourne C (2008) Achievements in forest tree genetic improvement in Australia and New Zealand 10: Pinus radiata in New Zealand. Aust For 71:263–279CrossRefGoogle Scholar
  13. Burger JA (2009) Management effects on growth, production and sustainability of managed forest ecosystems: Past trends and future directions. For Ecol Manage 258:2335–2346. CrossRefGoogle Scholar
  14. Butler DG, Cullis BR, Gilmour AR, Gogel BJ (2009) ASReml-R reference manual. Release 3.0. AustraliaGoogle Scholar
  15. Cambui CA, Svennerstam H, Gruffman L et al (2011) Patterns of plant biomass partitioning depend on nitrogen source. PLoS One 6:e19211. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Cook PG, Walker GR, Jolly ID (1989) Spatial variability of groundwater recharge in a semiarid region. J Hydrol 111:195–212. CrossRefGoogle Scholar
  17. Corcuera L, Gil-Pelegrin E, Notivol E (2010) Phenotypic plasticity in Pinus pinaster δ13C: environment modulates genetic variation. Ann For Sci 67:812–812. CrossRefGoogle Scholar
  18. Corwin DL, Lesch SM (2005) Apparent soil electrical conductivity measurements in agriculture. Comput Electron Agric 46:11–43. CrossRefGoogle Scholar
  19. Crawford DT, Lockaby BG, Somers GL (1991) Genotype-nutrition interactions in field-planted loblolly pine. Can J For Res 21:1523–1532CrossRefGoogle Scholar
  20. Cregg BM, Zhang JW (2001) Physiology and morphology of Pinus sylvestris seedlings from diverse sources under cyclic drought stress. For Ecol Manage 154:131–139. CrossRefGoogle Scholar
  21. Doolittle JA, Brevik EC (2014) The use of electromagnetic induction techniques in soils studies. Geoderma 223–225:33–45. CrossRefGoogle Scholar
  22. Fife DN, Nambiar EKS (1997) Changes in the canopy and growth of Pinus radiata in response to nitrogen supply. For Ecol Manage 93:137–152. CrossRefGoogle Scholar
  23. Forest Owners Association (2016) Facts and Figs. 2015/16: New Zealand plantation forestry industry.Google Scholar
  24. Franklin O, Cambui CA, Gruffman L et al (2017) The carbon bonus of organic nitrogen enhances nitrogen use efficiency of plants. Plant Cell Environ 40:25–35. CrossRefPubMedGoogle Scholar
  25. Gallart M, Adair KL, Love J et al (2018a) Host genotype and nitrogen form shape the root microbiome of Pinus radiata. Microb Ecol 75:419–433. CrossRefPubMedGoogle Scholar
  26. Gallart M, Adair KL, Love J et al (2018b) Genotypic variation in Pinus radiata responses to nitrogen source are related to changes in the root microbiome. FEMS Microbiol Ecol 94.
  27. Garcia Villacorta AM, Martin TA, Jokela EJ et al (2015) Variation in biomass distribution and nutrient content in loblolly pine (Pinus taeda L.) clones having contrasting crown architecture and growth efficiency. For Ecol Manage 342:84–92. CrossRefGoogle Scholar
  28. Gruffman L, Ishida T, Nordin A, Näsholm T (2012) Cultivation of Norway spruce and Scots pine on organic nitrogen improves seedling morphology and field performance. For Ecol Manage 276:118–124. CrossRefGoogle Scholar
  29. Hangs RD, Knight JD, Van Rees KC (2003) Nitrogen uptake characteristics for roots of conifer seedlings and common boreal forest competitor species. Can J For Res 33:156–163. CrossRefGoogle Scholar
  30. Harrison KA, Bol R, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–999. CrossRefPubMedGoogle Scholar
  31. Harrison KA, Bol R, Bardgett RD (2008) Do plant species with different growth strategies vary in their ability to compete with soil microbes for chemical forms of nitrogen? Soil Biol Biochem 40:228–237. CrossRefGoogle Scholar
  32. Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss After eutrophication. Science 324(80):636–638. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hawkins BJ, Xue J, Bown HE, Clinton PW (2010) Relating nutritional and physiological characteristics to growth of Pinus radiata clones planted on a range of sites in New Zealand. Tree Physiol 30:1174–1191. CrossRefPubMedGoogle Scholar
  34. Hewitt AE (1993) New Zealand soil classification. Manaaki Whenua - Landcare Research New Zealand.Google Scholar
  35. Hossain MB, Lamb DW, Lockwood PV, Frazier P (2010) EM38 for volumetric soil water content estimation in the root-zone of deep vertosol soils. Comput Electron Agric 74:100–109. CrossRefGoogle Scholar
  36. Irvine J, Perks MP, Magnani F, Grace J (1998) The response of Pinus sylvestris to drought: stomatal control of transpiration and hydraulic conductance. Tree Physiol 18:393–402. CrossRefPubMedGoogle Scholar
  37. Jones DL, Kielland K (2002) Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biol Biochem 34:209–219. CrossRefGoogle Scholar
  38. Khakural BR, Robert PC, Hugins DR (1998) Use of non-contacting electromagnetic inductive method for estimating soil moisture across a landscape. Commun Soil Sci Plant Anal 29:2055–2065. CrossRefGoogle Scholar
  39. Kronzucker HJ, Siddiqi MY, Glass ADM (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385:59–61. CrossRefGoogle Scholar
  40. Lim H, Oren R, Palmroth S et al (2015) Inter-annual variability of precipitation constrains the production response of boreal Pinus sylvestris to nitrogen fertilization. For Ecol Manage 348:31–45. CrossRefGoogle Scholar
  41. Lu C, Zhou Z, Zhu Q et al (2017) Using residual analysis in electromagnetic induction data interpretation to improve the prediction of soil properties. CATENA 149:176–184. CrossRefGoogle Scholar
  42. Manzoni S, Schimel JP, Porporato A et al (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938. CrossRefPubMedGoogle Scholar
  43. McDonald PM, Laacke RJ (1990) Pinus radiata D. Don. Monterey Pine. In: Burns R, Honkala B (eds) Silvics of North America. Volume 1, Conifers. Agriculture Handbook 654. United States Department of Agriculture, Forest Service, Washington, DC, pp 433–441Google Scholar
  44. McLaren RG, Cameron KC (1990) Soil Science: An introduction to the properties and management of New Zealand soils. Oxford University Press, Auckland, New ZealandGoogle Scholar
  45. Mead DJ (2013) Sustainable management of Pinus radiata plantations. Food and agriculture organization of the United nations (FAO), Roma.Google Scholar
  46. Mead D, Draper D, Madgwick H (1984) Dry matter production of a young stand of Pinus radiata: some effects of nitrogen fertiliser and thinning. New Zeal J For Sci 14:97–108Google Scholar
  47. Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36CrossRefGoogle Scholar
  48. Ministry for Primary Industries of New Zealand (2013) National exotic forest description. As at 1 april 2013.Google Scholar
  49. Miyazawa K, Lechowicz MJ (2004) Comparative seedling ecology of eight North American spruce (Picea) species in relation to their geographic ranges. Ann Bot 94:635–644. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Nadler A, Frenkel H (1980) Determination of soil solution electrical conductivity from bulk soil electrical conductivity measurements by the four-electrode method. Soil Sci Soc Am J 44:1216. CrossRefGoogle Scholar
  51. Näsholm T, Persson J (2001) Plant acquisition of organic nitrogen in boreal forests. Physiol Plant 111:419–426. CrossRefPubMedGoogle Scholar
  52. Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48. CrossRefPubMedGoogle Scholar
  53. Näsholm T, Högberg P, Franklin O et al (2013) Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytol 198:214–221. CrossRefPubMedGoogle Scholar
  54. Öhlund J, Näsholm T (2002) Low nitrogen losses with a new source of nitrogen for cultivation of conifer seedlings. Environ Sci Technol 36:4854–4859. CrossRefPubMedGoogle Scholar
  55. Öhlund J, Näsholm T (2004) Regulation of organic and inorganic nitrogen uptake in Scots pine (Pinus sylvestris) seedlings. Tree Physiol 24:1397–1402.
  56. Owen AG, Jones DL (2001) Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biol Biochem 33:651–657. CrossRefGoogle Scholar
  57. Parfitt R, Scott N, Ross D et al (2003) Land-use change effects on soil C and N transformations in soils of high N status: comparisons under indigenous forest, pasture and pine plantation. Biogeochemistry 66:203–221CrossRefGoogle Scholar
  58. Prasolova NV, Xu ZH, Lundkvist K et al (2003) Genetic variation in foliar carbon isotope composition in relation to tree growth and foliar nitrogen concentration in clones of the F1 hybrid between slash pine and Caribbean pine. For Ecol Manage 172:145–160. CrossRefGoogle Scholar
  59. Richardson DM (1998) Ecology and biogeography of Pinus, 1st edn. Cambridge University Press, CambridgeGoogle Scholar
  60. Rodríguez-Gamir J, Xue J, Clearwater MJ et al (2018) Aquaporin regulation in roots controls plant hydraulic conductance, stomatal conductance, and leaf water potential in Pinus radiata under water stress. Plant Cell Environ.
  61. Scanlon BR, Langford RP, Goldsmith RS (1999) Relationship between geomorphic settings and unsaturated flow in an arid setting. Water Resour Res 35:983–999. CrossRefGoogle Scholar
  62. Schlichting CD, Levin DA (1984) Phenotypic plasticity of annual phlox: Tests of some hypotheses. Am J Bot 71:252–260. CrossRefGoogle Scholar
  63. Souza L, Stuble KL, Genung MA, Classen AT (2017) Plant genotypic variation and intraspecific diversity trump soil nutrient availability to shape old-field structure and function. Funct Ecol 31:965–974. CrossRefGoogle Scholar
  64. Stadler A, Rudolph S, Kupisch M et al (2015) Quantifying the effects of soil variability on crop growth using apparent soil electrical conductivity measurements. Eur J Agron 64:8–20. CrossRefGoogle Scholar
  65. Sudduth KA, Kitchen NR, Wiebold WJ, Batchelor WD, Bollero GA, Bullock DG, Clay DE, Palm HL, Pierce FJ, Schuler RT, Thelen KD (2005) Relating apparent electrical conductivity to soil properties across the north-central USA. Comput Electron Agric 46(1-3):263–283Google Scholar
  66. Thornley J (1972) A balanced quantitative model for root:shoot ratios in vegetative plants. Ann Bot 36:431–441. CrossRefGoogle Scholar
  67. Triantafilis J, Laslett GM, McBratney AB (2000) Calibrating an electromagnetic induction instrument to measure salinity in soil under irrigated cotton. Soil Sci Soc Am J 64:1009. CrossRefGoogle Scholar
  68. Valladares F, Wright SJ, Lasso E et al (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936.[1925:PPRTLO]2.0.CO;2 CrossRefGoogle Scholar
  69. van den Driessche R (1971) Response of conifer seedlings to nitrate and ammonium sources of nitrogen. Plant Soil 34:421–439. CrossRefGoogle Scholar
  70. Williams B, Baker G (1982) An electromagnetic induction technique for reconnaissance surveys of soil salinity hazards. Aust J Soil Res 20:107. CrossRefGoogle Scholar
  71. Wilson AR, Nzokou P, Güney D, Kulaç Ş (2013) Growth response and nitrogen use physiology of Fraser fir (Abies fraseri), red pine (Pinus resinosa), and hybrid poplar under amino acid nutrition. New For 44:281–295. CrossRefGoogle Scholar
  72. Xue J, Clinton PW, Davis MR et al (2013) Genotypic variation in foliar nutrient concentrations, delta13C, and chlorophyll fluorescence in relation to tree growth of radiata pine clones in a serpentine soil. J Plant Nutr Soil Sci 176:724–733Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Marta Gallart
    • 1
    • 2
    Email author
  • Jonathan Love
    • 1
    • 3
  • Dean F. Meason
    • 4
  • Graham Coker
    • 2
  • Peter W. Clinton
    • 2
  • Jianming Xue
    • 2
  • Paula E. Jameson
    • 1
  • Jaroslav Klápště
    • 4
  • Matthew H. Turnbull
    • 1
  1. 1.Centre for Integrative Ecology, School of Biological SciencesUniversity of CanterburyChristchurchNew Zealand
  2. 2.ScionChristchurchNew Zealand
  3. 3.Department of Forest Ecology and ManagementSwedish University of Agricultural SciencesUmeåSweden
  4. 4.ScionRotoruaNew Zealand

Personalised recommendations