Skip to main content
SpringerLink
Log in

Nitrogen form and concentration interact to affect the performance of two ecologically distinct Mediterranean forest trees

  • Original Paper
  • Published:
European Journal of Forest Research Aims and scope Submit manuscript

Abstract

Most studies examining inorganic N form effects on growth and nutrition of forest trees have been conducted on single species from boreal or temperate environments, while comparative studies with species from other biomes are scarce. We evaluated the response of two Mediterranean trees of contrasting ecology, Quercus ilex L. and Pinus halepensis Mill., to cultivation with distinct inorganic N forms. Seedlings were fertilized with different NH4 +/NO3 − proportion at either 1 or 10 mM N. In both species, N forms had small effects at low N concentration, but at high N concentration they markedly affected the plant performance. A greater proportion of NH4 + in the fertilizer at high N caused toxicity as it reduced growth and caused seedling death, with the effect being greater in Q. ilex than in P. halepensis. An increase in the proportion of NO3 − at high N strongly enhanced growth relative to low N plants in P. halepensis but had minor effects in Q. ilex. Relatively more NH4 + in the fertilizer enhanced plant P concentration but reduced K concentration in both species, while the opposite effect occurred with NO3 −, and these effects were enhanced under high N concentration. We conclude that species responses to inorganic N forms were related to their ecology. P. halepensis, a pioneer tree, had improved performance with NO3 − at high N concentration and showed strong plasticity to changes in N supply. Q. ilex, a late successional tree, had low responsiveness to N form or concentration.

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

Similar content being viewed by others

References

  • Allison LE, Brown JW, Hayward HE, Richards LA, Bernstein L, Fireman M, Pearson GA, Wilcox LV, Bower CA, Hatcher JT, Reeve RC (1962) Determination of the properties of saline and alkali soils In: Richards LA (ed) Diagnosis and improvement of saline and alkali soils, agriculture handbook nº 60. United States Department of Agriculture, Maryland

  • Andivia E, Fernández M, Vázquez-Piqué J (2011) Autumn fertilization of Quercus ilex ssp. ballota (Desf.) Samp. nursery seedlings: effects on morpho-physiology and field performance. Ann For Sci 68:543–553

    Article  Google Scholar 

  • Arduini I, Kettner C, Godbold DL, Onnis A, Stefani A (1998) pH influence on root growth and nutrient uptake of Pinus pinaster seedlings. Chemosphere 36:733–738

    Article  CAS  Google Scholar 

  • Atkin OK, Cummins WR (1994) The effect of nitrogen source on growth, nitrogen economy and respiration of two high arctic plant species differing in relative growth rate. Func Ecol 8:389–399

    Article  Google Scholar 

  • Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environ Exp Bot 32:85–100

    Article  CAS  Google Scholar 

  • Bonilla D, Rodá F (1992) Soil nitrogen dynamics in a holm oak forest. Vegetatio 99–100:247–257

    Google Scholar 

  • Bown H, Watt M, Clinton P, Mason E (2010) Influence of ammonium and nitrate supply on growth, dry matter partitioning, N uptake and photosynthetic capacity of Pinus radiata seedlings. Trees 24:1097–1107

    Article  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

    Article  CAS  Google Scholar 

  • Cruz C, Lips SH, Martins-Loução MA (1993) Interactions between nitrate and ammonium during uptake by carob seedlings and the effect of the form of earlier nitrogen nutrition. Physiol Plant 89:544–551

    Article  CAS  Google Scholar 

  • Cruz C, Lips SH, Martins-Louçao MA (1997) Changes in the morphology of roots and leaves of carob seedlings induced by nitrogen source and atmospheric carbon dioxide. Ann Bot 80:817–823

    Article  Google Scholar 

  • Cubera E, Moreno G, Solla A (2009) Quercus ilex root growth in response to heterogeneous density and soil NH4–N content. Soil Tillage Res 103:16–22

    Article  Google Scholar 

  • Falkengren-Grerup U (1995) Interspecies differences in the preference of ammonium and nitrate in vascular plants. Oecologia 102:305–311

    Article  Google Scholar 

  • Fernández M, Martín RT (2005) Influencia de la intensidad luminosa sobre la tasa fotosintética de plantas de una savia de pinos españoles. In: Silva-Pando FJ, Sampedro L (eds) Actas de la I Reunión sobre Ecología, Ecología y Suelos Forestales. Cuad Soc Esp Cienc For 20:73–78

  • Field C, Mooney H (1983) The photosynthesis-nitrogen relationship in wild plants. In: Givnish T (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 25–50

    Google Scholar 

  • Gigon A, Rorison IH (1972) The response of some ecologically distinct plant species to nitrate- and to ammonium-nitrogen. J Ecol 60:93–102

    Article  CAS  Google Scholar 

  • Gimeno-García E, Andreu V, Rubio JL (2001) Influence of Mediterranean shrub species on soil chemical properties in typical Mediterranean environment. Comm Soil Sci Plant Anal 32:1885–1898

    Article  Google Scholar 

  • Grossnickle SC (2012) Why seedlings survive: influence of plant attributes. New For 43(5–6):711–738

    Article  Google Scholar 

  • Guo S, Brück H, Sattelmacher B (2002) Effects of supplied nitrogen form on growth and water uptake of French bean (Phaseolus vulgaris L.) plants nitrogen form and water uptake. Plant Soil 239:267–275

    Article  CAS  Google Scholar 

  • Hawkins BJ, Henry G, Kiiskila SBR (1999) Biomass and nutrient allocation in Douglas-fir and amabilis fir seedlings: influence of growth rate and nutrition. Tree Physiol 19:59–63

    Article  PubMed  Google Scholar 

  • Hawkins BJ, Burgess D, Mitchell AK (2005) Growth and nutrient dynamics of western hemlock with conventional or exponential greenhouse fertilization and planting in different fertility conditions. Can J For Res 35:1002–1016

    Article  CAS  Google Scholar 

  • Horchani F, Hajri R, Aschi-smiti S (2010) Effect of ammonium or nitrate nutrition on photosynthesis, growth, and nitrogen assimilation in tomato plants. J Plant Nutr Soil Sci 173:610–617

    Article  CAS  Google Scholar 

  • Ingestad T (1979) Mineral nutrient requirements of Pinus silvestris and Picea abies seedlings. Physiol Plant 45:373–380

    Article  CAS  Google Scholar 

  • Islam MA, Apostol KG, Jacobs DF, Dumroese RK (2009) Fall fertilization of Pinus resinosa seedlings: nutrient uptake, cold hardiness, and morphological development. Ann For Sci 66:704

    Article  Google Scholar 

  • Jacobs DF, Timmer VR (2005) Fertilizer-induced changes in rhizosphere electrical conductivity: relation to forest tree seedling root system growth and function. New For 30:147–166

    Article  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM, Britto DT (2003) Root ammonium transport efficiency as a determinant in forest colonization patterns: an hypothesis. Physiol Plant 117:164–170

    Article  CAS  Google Scholar 

  • Landis T, Tinus R, McDonald AJS, Barnett JP (1989) Mineral nutrients and fertilization. In: Landis TD, Tinus RW, McDonald SE, Barnett JP (eds) The container tree nursery manual. Vol. 4. Seedling nutrition and irrigation. U.S. Department of Agriculture, Forest Service, Washington, DC, pp 1–67

    Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    Article  PubMed  Google Scholar 

  • Loreto F, Ciccioli P, Cecinato A, Brancaleoni E, Frattoni M, Tricoli D (1996) Influence of environmental factors and air composition on the emission of [alpha]-Pinene from Quercus ilex leaves. Plant Physiol 110:267–275

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press, San Diego

    Google Scholar 

  • Metcalfe RJ, Nault J, Hawkins BJ (2011) Adaptations to nitrogen form: comparing inorganic nitrogen and amino acid availability and uptake by four temperate forest plants. Can J For Res 1637:1626–1637

    Article  Google Scholar 

  • Ministry of Forestry and Range (2007) ANOVA: factorial designs with a separate control. Biometrics Information Pamphlets #14., www.for.gov.bc.ca/hre/biopamph

  • Miyamoto S, Martinez I, Padilla M, Portillo A, Ornelas D (2004) Landscape plant lists for salt tolerance assessment. Agricultural Research and Extension Center of El Paso, Texas Agricultural Experimentation Station, El Paso

    Google Scholar 

  • Mulvaney R (1996) Nitrogen-inorganic forms. In: Sparks DL (ed) Methods of soil analysis. Part 2. Chemical properties. American Society of Agronomy, Madison. Soil Sci Soc Am 1123–1184

  • Nicodemus MA, Salifu FK, Jacobs DF (2008) Growth, nutrition, and photosynthetic response of Black Walnut to varying nitrogen sources and rates. Plant Physiol 31:1917–1936

    CAS  Google Scholar 

  • Öhlund J, Näsholm T (2001) Growth of conifer seedlings on organic and inorganic nitrogen sources. Tree Physiol 21:1319–1326

    Article  PubMed  Google Scholar 

  • Oliet JA, Planelles R, Segura ML, Artero F, Jacobs DF (2004) Mineral nutrition and growth of containerized Pinus halepensis seedlings under controlled-release fertilizer. Sci Hortic 103:113–129

    Article  CAS  Google Scholar 

  • Oliet JA, Valdecantos A, Puértolas J, Trubat R (2006) Influencia del estado nutricional y el contenido en carbohidratos en el establecimiento de las plantaciones. In: Cortina J, Peñuelas JL, Puértolas J, Savé R, Vilagrosa A (eds) Calidad de planta forestal para la restauración en ambientes mediterráneos. Estado actual de conocimientos. OAPN–MMA (España), pp 89–117

  • Paungfoo-Lonhienne C, Lonhienne TGA, Rentsch D, Robinson N, Christie M, Webb RI, Gamage HK, Carroll BJ, Schenk PM, Schmidt S (2008) Plants can use protein as a nitrogen source without assistance from other organisms. PNAS 105:4524–4529

    Article  CAS  PubMed  Google Scholar 

  • Puértolas J, Oliet JA, Jacobs DF, Benito LF, Peñuelas JL (2010) Is light the key factor for success of tube shelters in forest restoration plantings under Mediterranean climates? For Ecol Manag 260:610–617

    Article  Google Scholar 

  • Raven JA, Wollenweber B, Handley LL (1992) A comparison of ammonium and nitrate as nitrogen sources for photolithotrophs. New Phytol 121:19–32

    Article  CAS  Google Scholar 

  • Roosta HR, Sajjadinia A, Rahimi A, Schjoerring JK (2009) Responses of cucumber plant to NH4 + and NO3 − nutrition: the relative addition rate technique vs. cultivation at constant nitrogen concentration. Sci Hortic 121:397–403

    Article  CAS  Google Scholar 

  • Rothstein DE, Cregg BM (2005) Effects of nitrogen form on nutrient uptake and physiology of Fraser fir (Abies fraseri). For Ecol Manag 219:69–80

    Article  Google Scholar 

  • Rygiewicz PT, Bledsoe CS, Zasoski RJ (1984a) Effects of ectomycorrhizae and solution pH on [15N]ammonium uptake by coniferous seedlings. Can J For Res 14:885–892

    Article  CAS  Google Scholar 

  • Rygiewicz PT, Bledsoe CS, Zasoski RJ (1984b) Effects of ectomycorrhizae and solution pH on [15N]nitrate uptake by coniferous seedlings. Can J For Res 14:893–899

    Article  CAS  Google Scholar 

  • Salifu KF, Jacobs DF (2006) Characterizing fertility targets and multi-element interactions in nursery culture of Quercus rubra seedlings. Ann For Sci 63:231–237

    Article  Google Scholar 

  • Salifu KF, Timmer VR (2003) Optimizing nitrogen loading of Picea mariana seedlings during nursery culture. Can J For Res 33:1287–1294

    Article  Google Scholar 

  • Sanz-Pérez V, Castro-Díez P, Valladares F (2007) Growth versus storage: responses of Mediterranean oak seedlings to changes in nutrient and water availabilities. Ann For Sci 64:201–210

    Article  Google Scholar 

  • Serrasoles I, Diego V, Bonilla D (1999) Soil nitrogen dynamics. In: Roda F, Retana J, Gracia CA, Bellot J (eds) Ecology of Mediterranean evergreen oak forests. Springer, Berlin, pp 223–235

    Chapter  Google Scholar 

  • Sotiropoulos TE, Mouhtaridou GN, Thomidis T, Tsirakoglou V, Dimassi KN, Therios IN (2005) Effects of different N-sources on growth, nutritional status, chlorophyll content, and photosynthetic parameters of shoots of the apple rootstock MM 106 cultured in vitro. Biol Plant 49:297–299

    Article  Google Scholar 

  • Valladares F, Martínez-Ferri E, Balaguer L, Pérez-Corona E, Manrique E (2000) 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 

  • Vallejo VR, Smanis A, Chirino E, Fuentes D, Valdecantos A, Vilagrosa A (2012) Perspectives in dryland restoration: approaches for climate change adaptation. New For 43:561–579

    Article  Google Scholar 

  • van den Driessche R (1971) Response of conifer seedlings to nitrate and ammonium sources of nitrogen. Plant Soil 34:421–439

    Article  Google Scholar 

  • Villar-salvador P, Planelles R, Enríquez E, Peñuelas Rubira J (2004) Nursery cultivation regimes, plant functional attributes, and field performance relationships in the Mediterranean oak. For Ecol Manag 196:257–266

    Article  Google Scholar 

  • Villar-Salvador P, Heredia N, Millard P (2010) Remobilization of acorn nitrogen for seedling growth in holm oak (Quercus ilex), cultivated with contrasting nutrient availability. Tree Physiol 30:257–263

    Article  CAS  PubMed  Google Scholar 

  • Villar-Salvador P, Puértolas J, Cuesta B, Peñuelas JL, Uscola M, Heredia-Guerrero N, Rey Benayas JM (2012) Increase in size and nitrogen concentration enhances seedling survival in Mediterranean plantations. Insights from an ecophysiological conceptual model of plant survival. New For 43:755–770

    Article  Google Scholar 

  • Warren CR, Adams MA (2002) Possible causes of slow growth of nitrate-supplied Pinus pinaster. Can J For Res 32:569–580

    Article  Google Scholar 

  • Warren CR, Adams MA, Chen Z (2000) Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Aust J Plant Physiol 27:407–416

    CAS  Google Scholar 

  • Weigelt A, Bol R, Bardgett RD (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627–635

    Article  PubMed  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, total carotenoids using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Zavala MA, Espelta JM, Retana J (2000) Constraints and trade-offs in Mediterranean plant communities: the case of holm oak-Aleppo pine forests. Bot Rev 66:119–149

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to the Jardín Botánico Juan Carlos I of the Universidad de Alcalá and to Centro Nacional de Recursos Genéticos Forestales “El Serranillo” for their technical support. Agustín Rubio from the UPM is acknowledged for support in growing media analyses. This study was supported by a FPU-MEC grant to M. Uscola, and by projects AGL2006-12609-C02-01/FOR, AGL2011-24296 ECOLPIN (MICIIN), and the network REMEDINAL 2 (S2009/AMB/1783) of the Community of Madrid. We appreciate constructive reviews from anonymous referees and subject editor.

Author information

Author notes

  1. Eugenio Díaz-Pinés

    Present address: Division of Bio-Geo-Chemical Processes, Institute of Meteorology and Climate Research, Karlsruhe Institute of Technology, 82467, Garmisch-Partenkirchen, Germany

Authors and Affiliations

  1. Forest Ecology and Restoration Group, Departamento de Ciencias de la Vida, Universidad de Alcalá, Campus Universitario A.P. 20, 28805, Alcalá de Henares, Madrid, Spain

    Mercedes Uscola & Pedro Villar-Salvador

  2. Departamento de Silvopascicultura, Escuela de Ingeniería Forestal y del Medio Natural, Universidad Politécnica de Madrid, 28040, Madrid, Spain

    Juan A. Oliet & Eugenio Díaz-Pinés

  3. Department of Forestry and Natural Resources, Hardwood Tree Improvement and Regeneration Center, Purdue University, West Lafayette, IN, 47907-2061, USA

    Douglass F. Jacobs

Authors
  1. Mercedes Uscola
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan A. Oliet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pedro Villar-Salvador
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eugenio Díaz-Pinés
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Douglass F. Jacobs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mercedes Uscola.

Additional information

Communicated by Rainer Matyssek.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Uscola, M., Oliet, J.A., Villar-Salvador, P. et al. Nitrogen form and concentration interact to affect the performance of two ecologically distinct Mediterranean forest trees. Eur J Forest Res 133, 235–246 (2014). https://doi.org/10.1007/s10342-013-0749-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10342-013-0749-3

Keywords

Search

Navigation