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

Plant and Soil

Volumn 391, Issue 1-2, 2015, Pages 293-305

  Crous, K Y ^a   Osvaldsson A ^a,b   Ellsworth, D S ^a  

^a WESTERN SYDNEY UNIVERSITY   (Australia)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

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

Indexed keywords

BASAL AREA; CARBON DIOXIDE; CONCENTRATION (COMPOSITION); EVERGREEN TREE; FERTILIZER APPLICATION; GROWTH RATE; MATURATION; NATIVE SPECIES; NITROGEN; NUTRIENT LIMITATION; PHOSPHATE; PHOSPHORUS; PHOTOSYNTHESIS; STAND STRUCTURE; STEM; WOODLAND;

AUSTRALIA; CUMBERLAND PLAIN; NEW SOUTH WALES;

EUCALYPTUS; EUCALYPTUS TERETICORNIS;

EID: 84938216319     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-015-2426-4     Document Type: Article

References (73)

1. Ågren GI (2004) The C: N: P stoichiometry of autotrophs - theory and observations. Ecol Lett 7:185–191
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 94:1540–1551
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 37:70–81
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 47:992–1007
5. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol Plant Mol Biol 24:225–252
6. Brady NC, Weil RR (2007) The nature and properties of soils. Prentice Hall, Upper Saddle River
7. Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260
8. Chapin FS, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37:49–57
9. Chiera J, Thomas J, Rufty T (2002) Leaf initiation and development in soybean under phosphorus stress. J Exp Bot 53:473–481
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 14:939–947
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 259:85–95
12. Conroy JP, Milham PJ, Reed ML, Barlow EW (1990) Increases in phosphorus requirements for CO2-enriched pine species. Plant Physiol 92:977–982
13. Craine JM, Morrow C, Stock WD (2008) Nutrient concentration ratios and co-limitation in South African grasslands. New Phytol 179:829–836
14. Cromer RN, Wheeler AM, Barr NJ (1984) Mineral nutrition and growth of Eucalyptus seedlings. N Z J For Sci 14:229–239
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 28:607–614
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 117:1741–1751
17. Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800
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
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 10:1135–1142
20. Epstein E, Bloom AJ (eds) (2005) Mineral nutrition of plants: principles and perspectives. Sinauer Associates, Sunderland, p 380
21. Farquhar GD, Caemmerer SV, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 plants. Planta 149:78–90
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 23:201–235
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 9:3547–3569
24. Gusewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266
25. Haase DL, Rose R (1995) Vector analysis and its use for interpreting plant nutrient shifts in response to silvicultural treatments. For Sci 41:54–66
26. Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109
27. Handreck KA (1997) Phosphorus requirements of Australian native plants. Aust J Soil Res 35:241–289
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 27:169–178
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 14:852–862
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 10:851–869
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 Alto
32. Isbell RF (2002) The Australian soil classification (Revised Edition). CSIRO Publishing, Collingwood
33. Johnson AH, Frizano J, Vann DR (2003) Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487–499
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, Collingwood
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 196:81–99
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 19:55–66
37. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450
38. Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17
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 334:11–31
40. Lambert MJ, Turner J (1987) Suburban development and change in vegetation nutrient status. Aust J Bot 12:193–196
41. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379
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 180:114–123
43. McColl JG (1969) Soil-plant relationships in a Eucalyptus forest on south coast of New South Wales. Ecology 50:354–362
44. McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide: Implications of terrestrial redfield-type ratios. Ecology 85:2390–2401
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 66:959–968
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 40:136–143
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 83:339–355
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 101:11001–11006
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 440:922–925
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 200:227–240
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 14:33–47
53. Schönau APG, Herbert MA (1989) Fertilizing eucalypts at plantation establishment. For Ecol Manag 29:221–244
54. Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Rev 51:53–105
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 95:668–681
56. Theodorou ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101:339–344
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 223:267–274
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 52:141–147
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 42:125–130
60. Tozer M (2003) The native vegetation of the Cumberland Plain, western Sydney: systematic classification and field identification of communities. Cunninghamia
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 77:1357–1369
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 195:306–320
63. Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75
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 7:737–750
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 304:1665–1669
66. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15
67. Walker TW, Syers JK (1976) Fate of phosphorus during pedogenesis. Geoderma 15:1–19
68. Wang YP, Law RM, Pak B (2010) A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere. Biogeosciences 7:2261–2282
69. Wild A (1985) The phosphate content of Australian Soils. Aust J Agric Res 9:193–204
70. Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol 17:10–19
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 92:1616–1625
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 161:89–100
73. Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8:2907–2916