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

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Abstract

Aims

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.

Methods

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.

Results

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.

Conclusions

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.

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References

  • Ågren GI (2004) The C : N : P stoichiometry of autotrophs - theory and observations. Ecol Lett 7:185–191

    Article  Google Scholar 

  • 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 94:1540–1551

    Article  CAS  PubMed  Google Scholar 

  • 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 37:70–81

    Article  CAS  PubMed  Google Scholar 

  • Beadle NCW (1966) Soil phosphate and its role in molding segments of Australian flor and vegetation with special reference to xeromorphy and sclerophylly. Ecology 47:992–1007

    Article  Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol Plant Mol Biol 24:225–252

    Article  CAS  Google Scholar 

  • Brady NC, Weil RR (2007) The nature and properties of soils. Prentice Hall, Upper Saddle River

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chapin FS, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37:49–57

    Article  Google Scholar 

  • Chiera J, Thomas J, Rufty T (2002) Leaf initiation and development in soybean under phosphorus stress. J Exp Bot 53:473–481

    Article  CAS  PubMed  Google Scholar 

  • 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 14:939–947

    Article  PubMed  Google Scholar 

  • 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 259:85–95

    Article  CAS  Google Scholar 

  • Conroy JP, Milham PJ, Reed ML, Barlow EW (1990) Increases in phosphorus requirements for CO2-enriched pine species. Plant Physiol 92:977–982

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Craine JM, Morrow C, Stock WD (2008) Nutrient concentration ratios and co-limitation in South African grasslands. New Phytol 179:829–836

    Article  CAS  PubMed  Google Scholar 

  • Cromer RN, Wheeler AM, Barr NJ (1984) Mineral nutrition and growth of Eucalyptus seedlings. N Z J For Sci 14:229–239

    Google Scholar 

  • 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 28:607–614

    Article  CAS  PubMed  Google Scholar 

  • 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 117:1741–1751

    Article  Google Scholar 

  • Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800

    Article  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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 10:1135–1142

    Article  PubMed  Google Scholar 

  • Epstein E, Bloom AJ (eds) (2005) Mineral nutrition of plants: principles and perspectives. Sinauer Associates, Sunderland, p 380

    Google Scholar 

  • Farquhar GD, Caemmerer SV, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 plants. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • 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 23:201–235

    Article  Google Scholar 

  • 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 9:3547–3569

    Article  CAS  Google Scholar 

  • Gusewell S (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  Google Scholar 

  • Haase DL, Rose R (1995) Vector analysis and its use for interpreting plant nutrient shifts in response to silvicultural treatments. For Sci 41:54–66

    Google Scholar 

  • Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109

    Article  CAS  PubMed  Google Scholar 

  • Handreck KA (1997) Phosphorus requirements of Australian native plants. Aust J Soil Res 35:241–289

    Article  Google Scholar 

  • 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 27:169–178

    CAS  PubMed  Google Scholar 

  • 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 14:852–862

    Article  PubMed  Google Scholar 

  • 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 10:851–869

    Article  Google Scholar 

  • 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 Alto

    Google Scholar 

  • Isbell RF (2002) The Australian soil classification (Revised Edition). CSIRO Publishing, Collingwood

    Google Scholar 

  • Johnson AH, Frizano J, Vann DR (2003) Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487–499

    Article  PubMed  Google Scholar 

  • 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, Collingwood

    Google Scholar 

  • Keith H, Raison RJ, Jacobsen KL (1997) Allocation of carbon in a mature eucalypt forest and some effects of soil phosphorus availability. Plant Soil 196:81–99

    Article  CAS  Google Scholar 

  • Kirschbaum MUF, Bellingham DW, Cromer RN (1992) Growth analysis of the effects of phosphorus nutrition on seedlings of Eucalyptus grandis. Aust J Plant Physiol 19:55–66

    Article  CAS  Google Scholar 

  • Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450

    Article  Google Scholar 

  • Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17

    Article  Google Scholar 

  • 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 334:11–31

    Article  CAS  Google Scholar 

  • Lambert MJ, Turner J (1987) Suburban development and change in vegetation nutrient status. Aust J Bot 12:193–196

    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 

  • Mäkelä A, Valentine HT, Helmisaari H-S (2008) Optimal co-allocation of carbon and nitrogen in a forest stand at steady state. New Phytol 180:114–123

    Article  PubMed  Google Scholar 

  • McColl JG (1969) Soil-plant relationships in a Eucalyptus forest on south coast of New South Wales. Ecology 50:354–362

    Article  CAS  Google Scholar 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide: Implications of terrestrial redfield-type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • 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 66:959–968

    Article  CAS  Google Scholar 

  • 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

  • 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 40:136–143

    Article  Google Scholar 

  • 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 83:339–355

    Google Scholar 

  • 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 101:11001–11006

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 440:922–925

    Article  CAS  PubMed  Google Scholar 

  • 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 200:227–240

    Article  CAS  Google Scholar 

  • 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 14:33–47

    Article  Google Scholar 

  • Schönau APG, Herbert MA (1989) Fertilizing eucalypts at plantation establishment. For Ecol Manag 29:221–244

    Article  Google Scholar 

  • Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Rev 51:53–105

    Article  Google Scholar 

  • 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 95:668–681

    Article  PubMed  Google Scholar 

  • Theodorou ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101:339–344

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 223:267–274

    Article  Google Scholar 

  • 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 52:141–147

    Article  Google Scholar 

  • Timmer VR, Stone EL (1978) Comparative foliar analysis of young balsam fir fertilized with nitrogen, phosphorus, potassium, and lime. Soil Sci Soc Am J 42:125–130

    Article  CAS  Google Scholar 

  • Tozer M (2003) The native vegetation of the Cumberland Plain, western Sydney: systematic classification and field identification of communities. Cunninghamia

  • 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 77:1357–1369

    Article  CAS  Google Scholar 

  • 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 195:306–320

    Article  CAS  PubMed  Google Scholar 

  • Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75

    Article  CAS  Google Scholar 

  • 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 7:737–750

    Google Scholar 

  • 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 304:1665–1669

    Article  CAS  PubMed  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15

    Article  PubMed  Google Scholar 

  • Walker TW, Syers JK (1976) Fate of phosphorus during pedogenesis. Geoderma 15:1–19

    Article  CAS  Google Scholar 

  • Wang YP, Law RM, Pak B (2010) A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere. Biogeosciences 7:2261–2282

    Article  CAS  Google Scholar 

  • Wild A (1985) The phosphate content of Australian Soils. Aust J Agric Res 9:193–204

    Article  Google Scholar 

  • Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol 17:10–19

    Article  Google Scholar 

  • 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 92:1616–1625

    Article  PubMed  Google Scholar 

  • 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 161:89–100

    Article  Google Scholar 

  • Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8:2907–2916

    Article  CAS  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. Hawkesbury Institute for the Environment, University of Western Sydney, Penrith, NSW 2751, Australia

    K. Y. Crous, A. Ósvaldsson & D. S. Ellsworth

  2. Department of Biology, Case Western Reserve University, Cleveland, OH, 44106-7080, USA

    A. Ósvaldsson

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  1. K. Y. Crous
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  2. A. Ósvaldsson
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Correspondence to K. Y. Crous.

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Crous, K.Y., Ósvaldsson, A. & Ellsworth, D.S. Is phosphorus limiting in a mature Eucalyptus woodland? Phosphorus fertilisation stimulates stem growth. Plant Soil 391, 293–305 (2015). https://doi.org/10.1007/s11104-015-2426-4

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