Plant and Soil

, Volume 391, Issue 1–2, pp 293–305 | Cite as

Is phosphorus limiting in a mature Eucalyptus woodland? Phosphorus fertilisation stimulates stem growth

  • K. Y. Crous
  • A. Ósvaldsson
  • D. S. Ellsworth
Regular Article



Few direct tests of phosphorus (P) limitation on highly-weathered soils have been conducted, especially in mature, native Eucalyptus stands. We tested whether growth in a mature >80-year old stand of Eucalyptus tereticornis in Cumberland Plain Woodland was limited by P, and whether this P-limitation affected leaf photosynthetic capacity.


P was added to trees at the native woodland site at 50 kg ha-1 year-1 in each of 3 years, and stem and leaf responses were measured.


Leaf P concentrations before fertilisation were < 1 mg g-1 and N:P ratios ranged between 16 and 23. Addition of 50 kg ha-1 year-1 of P increased leaf P concentration significantly (+50 %) compared to non-fertilised trees, for two but not for the 3 years. Despite higher leaf P in fertilised trees, photosynthetic capacity was unaffected. However, there was a 54 % increase in tree stem basal area growth during the first and second years of P fertilisation, statistically significant in the second year of the experiment.


Our evidence shows that E. tereticornis is P-limited on Cumberland Plain soils. This has implications for forest responses to rising atmospheric [CO2], because photosynthesis in elevated [CO2] may become further constrained by required phosphate pools within the photosynthetic apparatus.


EucFACE Basal area increment Eucalyptus tereticornis Leaf N:P ratio Nutrients Photosynthesis Stem growth 



The research was supported by the Australian Research Council (ARC Discovery grant DP110105102). EucFACE is supported by the Australian government through the Education Investment Fund administrated by the Dept. of Industry and Science. Burhan Amiji and Marine Guerret are thanked for assistance in the field. Paul Milham and Cassie Mosdal are gratefully acknowledged for help in developing and implementing our method to obtain leaf P concentrations at the Hawkesbury Institute for the Environment. We thank the reviewers of the initial manuscript for providing thoughtful comments that improved the paper.

Supplementary material

11104_2015_2426_MOESM1_ESM.docx (25 kb)
ESM 1 (DOCX 25 kb)


  1. Ågren GI (2004) The C : N : P stoichiometry of autotrophs - theory and observations. Ecol Lett 7:185–191CrossRefGoogle Scholar
  2. Alvarez-Clare S, Mack MC, Brooks M (2013) A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. Ecology 94:1540–1551CrossRefPubMedGoogle Scholar
  3. Battie-Laclau P, Laclau JP, Beri C, Mietton L, Muniz MRA, Arenque BC, Piccolo MDC, Jordan-Meille L, Bouillet JP, Nouvellon Y (2014) Photosynthetic and anatomical responses of Eucalyptus grandis leaves to potassium and sodium supply in a field experiment. Plant Cell Environ 37:70–81CrossRefPubMedGoogle Scholar
  4. Beadle NCW (1966) Soil phosphate and its role in molding segments of Australian flor and vegetation with special reference to xeromorphy and sclerophylly. Ecology 47:992–1007CrossRefGoogle Scholar
  5. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol Plant Mol Biol 24:225–252CrossRefGoogle Scholar
  6. Brady NC, Weil RR (2007) The nature and properties of soils. Prentice Hall, Upper Saddle RiverGoogle Scholar
  7. Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  8. Chapin FS, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37:49–57CrossRefGoogle Scholar
  9. Chiera J, Thomas J, Rufty T (2002) Leaf initiation and development in soybean under phosphorus stress. J Exp Bot 53:473–481CrossRefPubMedGoogle Scholar
  10. Cleveland CC, Townsend AR, Taylor P, Alvarez-Clare S, Bustamante MMC, Chuyong G, Dobrowski SZ, Grierson P, Harms KE, Houlton BZ, Marklein A, Parton W, Porder S, Reed SC, Sierra CA, Silver WL, Tanner EVJ, Wieder WR (2011) Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14:939–947CrossRefPubMedGoogle Scholar
  11. Close DC, Beadle CL (2004) Total, and chemical fractions, of nitrogen and phosphorus in Eucalyptus seedling leaves: Effects of species, nursery fertiliser management and transplanting. Plant Soil 259:85–95CrossRefGoogle Scholar
  12. Conroy JP, Milham PJ, Reed ML, Barlow EW (1990) Increases in phosphorus requirements for CO2-enriched pine species. Plant Physiol 92:977–982CrossRefPubMedCentralPubMedGoogle Scholar
  13. Craine JM, Morrow C, Stock WD (2008) Nutrient concentration ratios and co-limitation in South African grasslands. New Phytol 179:829–836CrossRefPubMedGoogle Scholar
  14. Cromer RN, Wheeler AM, Barr NJ (1984) Mineral nutrition and growth of Eucalyptus seedlings. N Z J For Sci 14:229–239Google Scholar
  15. Crous KY, Walters MB, Ellsworth DS (2008) Elevated CO2 concentration affects leaf photosynthesis-nitrogen relationships in Pinus taeda over nine years in FACE. Tree Physiol 28:607–614CrossRefPubMedGoogle Scholar
  16. Danger M, Daufresne T, Lucas F, Pissard S, Lacroix G (2008) Does Liebig’s law of the minimum scale up from species to communities? Oikos 117:1741–1751CrossRefGoogle Scholar
  17. Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800CrossRefGoogle Scholar
  18. Ellsworth DS, Crous KY, Lambers H, Cooke J (2015) Phosphorus recycling in photorespiration maintains high photosynthetic capacity in woody species. Plant Cell Environ. doi: 10.1111/pce.12468 PubMedGoogle Scholar
  19. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142CrossRefPubMedGoogle Scholar
  20. Epstein E, Bloom AJ (eds) (2005) Mineral nutrition of plants: principles and perspectives. Sinauer Associates, Sunderland, p 380Google Scholar
  21. Farquhar GD, Caemmerer SV, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 plants. Planta 149:78–90CrossRefPubMedGoogle Scholar
  22. Field CB, Chapin FS, Matson PA, Mooney HA (1992) Responses of terrestrial ecosystems to the changing atmosphere: a resource-based approach. Annu Rev Ecol Syst 23:201–235CrossRefGoogle Scholar
  23. Goll DS, Brovkin V, Parida BR, Reick CH, Kattge J, Reich PB, van Bodegom PM, Niinemets U (2012) Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling. Biogeosciences 9:3547–3569CrossRefGoogle Scholar
  24. Gusewell S (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266CrossRefGoogle Scholar
  25. Haase DL, Rose R (1995) Vector analysis and its use for interpreting plant nutrient shifts in response to silvicultural treatments. For Sci 41:54–66Google Scholar
  26. Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109CrossRefPubMedGoogle Scholar
  27. Handreck KA (1997) Phosphorus requirements of Australian native plants. Aust J Soil Res 35:241–289CrossRefGoogle Scholar
  28. Harley PC, Sharkey TD (1991) An improved model of C3 photosynthesis at high CO2 - reverse O2 sensitivity explained by lack of glycerate re-entry into the chloroplast. Photosynth Res 27:169–178PubMedGoogle Scholar
  29. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862CrossRefPubMedGoogle Scholar
  30. Haverd V, Raupach MR, Briggs PR, Canadell JG, Davis SJ, Law RM, Meyer CP, Peters GP, Pickett-Heaps C, Sherman B (2013) The Australian terrestrial carbon budget. Biogeosciences 10:851–869CrossRefGoogle Scholar
  31. Hedin LO, Brookshire ENJ, Menge DNL, Barron AR (2009) The nitrogen paradox in tropical forest ecosystems. Annual review of ecology evolution and systematics. Annual Reviews, Palo AltoGoogle Scholar
  32. Isbell RF (2002) The Australian soil classification (Revised Edition). CSIRO Publishing, CollingwoodGoogle Scholar
  33. Johnson AH, Frizano J, Vann DR (2003) Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487–499CrossRefPubMedGoogle Scholar
  34. Judd TS, Attiwill PM, Adams MA (1996) Nutrient concentrations in Eucalyptus: a synthesis in relation to differences between taxa, sites and components. In: Attiwill PM, Adams MA (eds) Nutrition of eucalypts. CSIRO Press, CollingwoodGoogle Scholar
  35. Keith H, Raison RJ, Jacobsen KL (1997) Allocation of carbon in a mature eucalypt forest and some effects of soil phosphorus availability. Plant Soil 196:81–99CrossRefGoogle Scholar
  36. Kirschbaum MUF, Bellingham DW, Cromer RN (1992) Growth analysis of the effects of phosphorus nutrition on seedlings of Eucalyptus grandis. Aust J Plant Physiol 19:55–66CrossRefGoogle Scholar
  37. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450CrossRefGoogle Scholar
  38. Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17CrossRefGoogle Scholar
  39. Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31CrossRefGoogle Scholar
  40. Lambert MJ, Turner J (1987) Suburban development and change in vegetation nutrient status. Aust J Bot 12:193–196Google Scholar
  41. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379CrossRefPubMedGoogle Scholar
  42. Mäkelä A, Valentine HT, Helmisaari H-S (2008) Optimal co-allocation of carbon and nitrogen in a forest stand at steady state. New Phytol 180:114–123CrossRefPubMedGoogle Scholar
  43. McColl JG (1969) Soil-plant relationships in a Eucalyptus forest on south coast of New South Wales. Ecology 50:354–362CrossRefGoogle Scholar
  44. McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide: Implications of terrestrial redfield-type ratios. Ecology 85:2390–2401CrossRefGoogle Scholar
  45. Mendham DS, Smethurst PJ, Holz GK, Menary RC, Grove TS, Weston C, Baker T (2002) Soil analyses as indicators of phosphorus response in young eucalypt plantations. Soil Sci Soc Am J 66:959–968CrossRefGoogle Scholar
  46. Nielsen U, Prior S, Delroy B, Walker JKM, Ellsworth DS, Powell JR (2015) Response of belowground communities to short-term phosphorus addition in a phosphorus-limited Woodland. Plant Soil doi: 10.1007/s11104-015-2432-6
  47. O’Connell AM, Mendham DS (2004) Impact of N and P fertilizer application on nutrient cycling in jarrah (Eucalyptus marginata) forests of southwestern Australia. Biol Fertil Soils 40:136–143CrossRefGoogle Scholar
  48. Ollinger SV, Smith ML, Martin ME, Hallett RA, Goodale CL, Aber JD (2002) Regional variation in foliar chemistry and N cycling among forests of diverse history and composition. Ecology 83:339–355Google Scholar
  49. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci U S A 101:11001–11006CrossRefPubMedCentralPubMedGoogle Scholar
  50. Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925CrossRefPubMedGoogle Scholar
  51. Rodriguez D, Keltjens WG, Goudriaan J (1998) Plant leaf area expansion and assimilate production in wheat (Triticum aestivum L.) growing under low phosphorus conditions. Plant Soil 200:227–240CrossRefGoogle Scholar
  52. Sardans J, Rivas-Ubach A, Penuelas J (2012) The C:N:P stoichiometry of organisms and ecosystems in a changing world: A review and perspectives. Perspect Plant Ecol Evol Syst 14:33–47CrossRefGoogle Scholar
  53. Schönau APG, Herbert MA (1989) Fertilizing eucalypts at plantation establishment. For Ecol Manag 29:221–244CrossRefGoogle Scholar
  54. Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Rev 51:53–105CrossRefGoogle Scholar
  55. Sullivan BW, Alvarez-Clare S, Castle SC, Porder S, Reed SC, Schreeg L, Townsend AR, Cleveland CC (2014) Assessing nutrient limitation in complex forested ecosystems: alternatives to large-scale fertilization experiments. Ecology 95:668–681CrossRefPubMedGoogle Scholar
  56. Theodorou ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101:339–344PubMedCentralPubMedGoogle Scholar
  57. Thomas DS, Montagu KD, Conroy JP (2006) Leaf inorganic phosphorus as a potential indicator of phosphorus status, photosynthesis and growth of Eucalyptus grandis seedlings. For Ecol Manag 223:267–274CrossRefGoogle Scholar
  58. Thomson VP, Leishman MR (2004) Survival of native plants of Hawkesbury Sandstone communities with additional nutrients: effect of plant age and habitat. Aust J Bot 52:141–147CrossRefGoogle Scholar
  59. Timmer VR, Stone EL (1978) Comparative foliar analysis of young balsam fir fertilized with nitrogen, phosphorus, potassium, and lime. Soil Sci Soc Am J 42:125–130CrossRefGoogle Scholar
  60. Tozer M (2003) The native vegetation of the Cumberland Plain, western Sydney: systematic classification and field identification of communities. CunninghamiaGoogle Scholar
  61. Turner BL, Yavitt JB, Harms KE, Garcia MN, Romero TE, Wright SJ (2013) Seasonal changes and treatment effects on soil inorganic nutrients following a decade of fertilizer addition in a lowland tropical forest. Soil Sci Soc Am J 77:1357–1369CrossRefGoogle Scholar
  62. Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320CrossRefPubMedGoogle Scholar
  63. Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75CrossRefGoogle Scholar
  64. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750Google Scholar
  65. Vitousek PM, Ladefoged TN, Kirch PV, Hartshorn AS, Graves MW, Hotchkiss SC, Tuljapurkar S, Chadwick OA (2004) Soils, agriculture, and society in precontact Hawai. Science 304:1665–1669CrossRefPubMedGoogle Scholar
  66. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15CrossRefPubMedGoogle Scholar
  67. Walker TW, Syers JK (1976) Fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  68. Wang YP, Law RM, Pak B (2010) A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere. Biogeosciences 7:2261–2282CrossRefGoogle Scholar
  69. Wild A (1985) The phosphate content of Australian Soils. Aust J Agric Res 9:193–204CrossRefGoogle Scholar
  70. Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol 17:10–19CrossRefGoogle Scholar
  71. Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625CrossRefPubMedGoogle Scholar
  72. Xu D, Dell B, Malajczuk N, Gong M (2002) Effects of P fertilisation on productivity and nutrient accumulation in a Eucalyptus grandis x E. urophylla plantation in southern China. For Ecol Manag 161:89–100CrossRefGoogle Scholar
  73. Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8:2907–2916CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • K. Y. Crous
    • 1
  • A. Ósvaldsson
    • 1
    • 2
  • D. S. Ellsworth
    • 1
  1. 1.Hawkesbury Institute for the EnvironmentUniversity of Western SydneyPenrithAustralia
  2. 2.Department of BiologyCase Western Reserve UniversityClevelandUSA

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