Plant and Soil

, Volume 334, Issue 1–2, pp 11–31 | Cite as

Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies

  • Hans Lambers
  • Mark C. Brundrett
  • John A. Raven
  • Stephen D. Hopper
Marschner Review

Abstract

Ancient landscapes, which have not been glaciated in recent times or disturbed by other major catastrophic events such as volcanic eruptions, are dominated by nutrient-impoverished soils. If these parts of the world have had a relatively stable climate, due to buffering by oceans, their floras tend to be very biodiverse. This review compares the functional ecophysiological plant traits that dominate in old, climatically buffered, infertile landscapes (OCBILS) with those commonly found in young, frequently disturbed, fertile landscapes (YODFELs). We show that, within the OCBILs of Western Australia, non-mycorrhizal species with specialised root clusters predominantly occur on the most phosphate-impoverished soils, where they co-occur with mycorrhizal species without such specialised root clusters. In global comparisons, we show that plants in OCBILs, especially in Western Australia, are characterised by very low leaf phosphorus (P) concentrations, very high N:P ratios, and very high LMA values (LMA = leaf mass per unit leaf area). In addition, we show that species in OCBILs are far more likely to show P-toxicity symptoms when exposed to slightly elevated soil P levels when compared with plants in YODFELs. In addition, some species in OCBILs exhibit a remarkable P-resorption proficiency, with some plants in Western Australia achieving leaf P concentrations in recently shed leaves that are lower than ever reported before. We discuss how this knowledge on functional traits can guide us towards sustainable management of ancient landscapes.

Keywords

Ancient landscapes Biodiversity Cluster roots LMA Mycorrhiza Nitrogen OCBIL Phosphorus Sclerophyllous YODFEL 

References

  1. Acharya K, Kyle M, Elser JJ (2004) Biological stoichiometry of Daphnia growth: an ecophysiological test of the growth rate hypothesis. Limnol Oceanogr 49:656–665CrossRefGoogle Scholar
  2. Adam P, Stricker P, Anderson DJ (1989) Species-richness and soil phosphorus in plant communities in coastal New South Wales. Austral Ecol 14:189–198CrossRefGoogle Scholar
  3. Adams F, Conrad JP (1953) Transition of phosphite to phosphate in soils. Soil Sci 75:361CrossRefGoogle Scholar
  4. Adiku S, Narh S, Jones J, Laryea K, Dowuona G (2008) Short-term effects of crop rotation, residue management, and soil water on carbon mineralization in a tropical cropping system. Plant Soil 311:29–38CrossRefGoogle Scholar
  5. Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608CrossRefGoogle Scholar
  6. Allsop N, Stock WD (1993) Mycorrhizal status of plants growing in the Cape Floristic Region, South Africa. Bothalia 23:91–104Google Scholar
  7. Andersson MX, Stridh MH, Larsson KE, Liljenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537:128–132PubMedCrossRefGoogle Scholar
  8. Anonymous (2003) A biodiversity audit of Western Australia’s biogeographical subregions in 2002. Department of Conservation and Land Management, Western AustraliaGoogle Scholar
  9. Anonymous (2006) Guidance Statement No. 6. Rehabilitation of Terrestrial Ecosystems. Environmental Protection Authority, Western AustraliaGoogle Scholar
  10. Anonymous (2007) Advice on areas of the highest conservation value in the proposed extensions to Mount Manning Nature Reserve. Bulletin 1256. Environmental Protection Authority, Western AustraliaGoogle Scholar
  11. Barrow NJ (1977) Phosphorus uptake and utilization by tree seedlings. Aust J Bot 25:571–584CrossRefGoogle Scholar
  12. Beadle NCW (1953) The edaphic factor in plant ecology with a special note on soil phosphates. Ecology 34:426–428CrossRefGoogle Scholar
  13. Beadle NCW (1954) Soil phosphate and the delimitation of plant communities in eastern Australia. Ecology 35:370–375CrossRefGoogle Scholar
  14. Beadle NCW (1962) Soil phosphate and the delimitation of plant communities in eastern Australia, II. Ecology 43:281–288CrossRefGoogle Scholar
  15. Beadle NCW (1966) Soil phosphate and its role in molding segments of the Australian flora and vegetation, with special reference to xeromorphy and sclerophylly. Ecology 47:992–1007CrossRefGoogle Scholar
  16. Beard JS (1990) Plant life of Western Australia. Kangaroo, KenhurstGoogle Scholar
  17. Bowden WS (1986) Gaseous nitrogen emissions from undisturbed ecosystems: an assessment of their impacts on local and global nitrogen budgets. Biogeochemistry 2:249–279CrossRefGoogle Scholar
  18. Bowden WB, Bormann FH (1986) Transport and loss of nitrous oxide in soil water after forest clear-cutting. Science 233:867–869PubMedCrossRefGoogle Scholar
  19. Bowler JM, Wyrwoll K-H, Lu Y (2001) Variations of the northwest Australian summer monsoon over the last 300, 000 years: the paleohydrological record of the Gregory (Mulan) Lakes System. Quatern Int 83–85:63–80CrossRefGoogle Scholar
  20. Brundrett M (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  21. Calderon-Vazquez C, Ibarra-Laclette E, Caballero-Perez J, Herrera-Estrella L (2008) Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels. J Exp Bot 59:2479–2497PubMedCrossRefGoogle Scholar
  22. Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO (1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–497CrossRefGoogle Scholar
  23. Chapin FS, Bieleski RL (1982) Mild phosphorus stress in barley and a related low-phosphorus-adapted barleygrass: phosphorus fractions and phosphate absorption in relation to growth. Physiol Plant 54:309–317CrossRefGoogle Scholar
  24. Chiou T-J (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332PubMedCrossRefGoogle Scholar
  25. Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Global Environ Change 19:292–305CrossRefGoogle Scholar
  26. Crews TE, Kitayama K, Fownes JH, Riley RH, Herbert DA, Mueller-Dombois D, Vitousek PM (1995) Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:1407–1424CrossRefGoogle Scholar
  27. Crisp MD, Cook L, Steane D (2004) Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Phil Trans R Soc Lond B 359:551–1571CrossRefGoogle Scholar
  28. Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103:6765–6770PubMedCrossRefGoogle Scholar
  29. De Groot CC, Van den Boogaard R, Marcelis LFM, Harbinson J, Lambers H (2003) Contrasting effects of N and P deprivation on the regulation of photosynthesis in tomato plants in relation to feedback limitation. J Exp Bot 54:1957–1967PubMedCrossRefGoogle Scholar
  30. Denton M, Veneklaas E, Freimoser F, Lambers H (2007a) Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus. Plant Cell Environ 30:1557–1565PubMedCrossRefGoogle Scholar
  31. Denton MD, Veneklaas EJ, Lambers H (2007b) Does phenotypic plasticity in carboxylate exudation differ among rare and widespread Banksia species (Proteaceae)? New Phytol 173:592–599PubMedCrossRefGoogle Scholar
  32. Doerner P (2008) Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Curr Opin Plant Biol 11:536–540PubMedCrossRefGoogle Scholar
  33. Duff SMG, Moorhead GBG, Lefebvre DD, Plaxton WC (1989) Phosphate starvation inducible ‘bypasses’ of adenylate and phosphate dependent glycolytic enzymes in Brassica nigra suspension cells. Plant Physiol 90:1275–1278PubMedCrossRefGoogle Scholar
  34. Elser JJ, Dobberfuhl D, MacKay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry: towards a unified view of cellular and ecosystem processes. Bioscience 46:674CrossRefGoogle Scholar
  35. Fairbanks MM, Hardy GESJ, McComb JA (2000) Comparisons of phosphite concentrations in Corymbia (Eucalyptus) calophylla tissues after spray, mist or soil drench applications with the fungicide phosphite. Australas Plant Pathol 29:96–101CrossRefGoogle Scholar
  36. Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of plant form and function. Ed.. Cambridge University Press, London, pp 25–55Google Scholar
  37. Fisher J, Veneklaas E, Lambers H, Loneragan W (2006) Enhanced soil and leaf nutrient status of a Western Australian Banksia woodland community invaded by Ehrharta calycina and Pelargonium capitatum. Plant Soil 284:253–264CrossRefGoogle Scholar
  38. Fisher JL, Loneragan WA, Dixon K, Delaney J, Veneklaas EJ (2009) Altered vegetation structure and composition linked to fire frequency and plant invasion in a biodiverse woodland. Biol Conserv 142:2270–2281CrossRefGoogle Scholar
  39. Flynn K, Raven J, Rees T, Finkel Z, Quigg A, Beardall J (2010) Is the growth rate hypthesis applicable to microalgae? J Phycol 46:1–12CrossRefGoogle Scholar
  40. Fricke W, Leigh RA, Tomos AD (1996) The intercellular distribution of vacuolar solutes in the epidermis and mesophyll of barley leaves changes in response to NaCl. J Exp Bot 47:1413–1426CrossRefGoogle Scholar
  41. Funk V, Hollowell T, Berry TP, Kelloff CL, Alexander SN (2007) Checklist of the plants of the Guiana Shield. Contr US Natl Herb 55:1–584Google Scholar
  42. Gaude N, Nakamura Y, Scheible W-R, Ohta H, Dörmann P (2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J 56:28–39PubMedCrossRefGoogle Scholar
  43. Gibson N, Keighery GJ, Lyons MN, Webb A (2004) Terrestrial flora and vegetation of the Western Australian wheatbelt. Records of the Western Australian Museum Supplement No 67:139–189Google Scholar
  44. Gniazdowska A, Rychter AM (2000) Nitrate uptake by bean (Phaseolus vulgaris L.) roots under phosphate deficiency. Plant Soil 226:79–85CrossRefGoogle Scholar
  45. Goldblatt P, Manning J (2000) Cape plants. A conspectus of the Cape flora of South Africa. Strelitzia 9Google Scholar
  46. Grigg AM, Veneklaas EJ, Lambers H (2008a) Water relations and mineral nutrition of closely related woody plant species on desert dunes and interdunes. Aust J Bot 56:27–43CrossRefGoogle Scholar
  47. Grigg AM, Veneklaas EJ, Lambers H (2008b) Water relations and mineral nutrition of Triodia grasses on desert dunes and interdunes. Aust J Bot 56:408–421CrossRefGoogle Scholar
  48. Groom PK, Lamont BB (2010) Phosphorus accumulation in Proteaceae seeds: a synthesis. Pland and Soil in pressGoogle Scholar
  49. Grundon NJ (1972) Mineral nutrition of some Queensland heath plants. J Ecol 60:171–181CrossRefGoogle Scholar
  50. Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266CrossRefGoogle Scholar
  51. Han WX, Fang JY, Guo DL, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385PubMedCrossRefGoogle Scholar
  52. Handreck K (1991a) Interactions between iron and phosphorus in the nutrition of Banksia ericifolia L.f var ericifolia (Proteaceae) in soil-less potting media. Aust J Bot 39:373–384CrossRefGoogle Scholar
  53. Handreck K (1991b) Phosphorus and iron effects on the early growth of some Australian native plants. In Proceedings of the International Plant Propagators Society. pp 56–59Google Scholar
  54. Harrison MT, Edwards EJ, Farquhar GD, Nicotra AB, Evans JR (2009) Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use efficiency. Plant Cell Environ 32:259–270PubMedCrossRefGoogle Scholar
  55. Härtel H, Dörmann P, Benning C (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97:10649–10654PubMedCrossRefGoogle Scholar
  56. Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009a) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. J Exp Bot 60:2303–2314PubMedCrossRefGoogle Scholar
  57. Hassiotou F, Evans JR, Ludwig M, Veneklaas EJ (2009b) Stomatal crypts may facilitate diffusion of CO2 to adaxial mesophyll cells in thick sclerophylls. Plant Cell Environ 32:1596–1611CrossRefGoogle Scholar
  58. Hawkins H-J, Hettasch H, Mesjasz-Przybylowicz J, Przybylowicz W, Cramer MD (2008) Phosphorus toxicity in the Proteaceae: a problem in post-agricultural lands. Sci Hort 117:357–365CrossRefGoogle Scholar
  59. Herppich M, Herppich WB, Von Willert DJ (2002) Leaf nitrogen content and photosynthetic activity mountain fynbos plants (South Africa). Basic Appl Ecol 3:329–337CrossRefGoogle Scholar
  60. Hesse PP, Magee JW, Van der Kaars S (2004) Late Quaternary climates of the Australian arid zone: a review. Quatern Int 118–119:87–102CrossRefGoogle Scholar
  61. Hidaka A, Kitayama K (2009) Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen-use efficiency of tree leaves along nutrient-availability gradients. J Ecol 97:984–991CrossRefGoogle Scholar
  62. Hooker JD (1860) The Botany Of The Antarctic Voyage of H. M. Discovery Ships Erebus and Terror in the years 1839–1843. Part III. Flora Tasmaniae Vol. I Dicotyledones. Lovell Reeve, LondonGoogle Scholar
  63. Hopper SD (2003) South-western Australia - Cinderella of the world’s temperate floristic regions. 1. Curt Bot Mag 20:101–126CrossRefGoogle Scholar
  64. Hopper SD (2004) South-western Australia - Cinderella of the world’s temperate floristic regions. 2. Curt Bot Mag 21:132–180CrossRefGoogle Scholar
  65. Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322:49–86CrossRefGoogle Scholar
  66. Hopper SD (2010) Nuytsia floribunda. Curt Bot Mag 26:333–368CrossRefGoogle Scholar
  67. Hopper SD, Gioia P (2004) The southwest Australian floristic region: evolution and conservation of global hotspot of biodiversity. Annu Rev Ecol Evol Systemat 35:623–650CrossRefGoogle Scholar
  68. Hopper SD, Lambers H (2009) Darwin as a plant scientist: a Southern Hemisphere perspective. Trends Plant Sci 14:421–435PubMedCrossRefGoogle Scholar
  69. Hopper SD, Smith RJ, Fay MF, Manning JC, Chase MW (2009) Molecular phylogenetics of Haemodoraceae in the Greater Cape and Southwest Australian Floristic Regions. Mol Phylogenet Evol 51:19–30PubMedCrossRefGoogle Scholar
  70. Huston M (1980) Soil nutrients and tree species richness in Costa Rican forests. J Biogeogr 7:147–157CrossRefGoogle Scholar
  71. Jemo M, Abaidoo R, Nolte C, Tchienkoua M, Sanginga N, Horst W (2006) Phosphorus benefits from grain-legume crops to subsequent maize grown on acid soils of southern Cameroon. Plant Soil 284:385–397CrossRefGoogle Scholar
  72. Kamh M, Horst WJ, Amer F, Mostafa H, Maier P (1999) Mobilization of soil and fertilizer phosphate by cover crops. Plant Soil 211:19–27CrossRefGoogle Scholar
  73. Karley AJ, Leigh RA, Sanders D (2000) Differential ion accumulation and ion fluxes in the mesophyll and epidermis of barley. Plant Physiol 122:835–844PubMedCrossRefGoogle Scholar
  74. Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727CrossRefGoogle Scholar
  75. Kuo J, Hocking PJ, Pate JS (1982) Nutrient reserves in seeds of selected Proteaceous species from south-western Australia. Aust J Bot 30:231–249CrossRefGoogle Scholar
  76. Kustka A, Sañudo-Wilhelmy S, Carpenter EJ, Capone DG, Raven JA (2003a) A revised estimate of the Fe use efficiency of nitrogen fixation, with special reference to the N2 fixing cyanobacterium Trichodesmium (Cyanophyta). J Phycol 39:12–25CrossRefGoogle Scholar
  77. Kustka AB, Sanudo-Wilhelmy SA, Carpenter EJ, Capone D, Burns J, Sunda WG (2003b) Iron requirements for dinitrogen- and ammonium-supported growth in cultures of Trichodesmium (IMS 101): comparison with nitrogen fixation rates and iron: carbon ratios of field populations. Limnol Oceanogr 48:1869–1884CrossRefGoogle Scholar
  78. Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 22:187–261CrossRefGoogle Scholar
  79. Lambers H, Juniper D, Cawthray GR, Veneklaas EJ, Martínez-Ferri E (2002) The pattern of carboxylate exudation in Banksia grandis (Proteaceae) is affected by the form of phosphate added to the soil. Plant Soil 238:111–122CrossRefGoogle Scholar
  80. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713PubMedCrossRefGoogle Scholar
  81. Lambers H, Chapin FS, Pons TL (2008a) Plant physiological ecology, 2nd edn. Springer, New YorkGoogle Scholar
  82. Lambers H, Raven JA, Shaver GR, Smith SE (2008b) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103PubMedCrossRefGoogle Scholar
  83. Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115CrossRefGoogle Scholar
  84. Lauer MJ, Blevins DG, Sierzputowska-Gracz H (1989) 31P-Nuclear Magnetic Resonance determination of phosphate compartmentation in leaves of reproductive soybeans (Glycine max L.) as affected by phosphate nutrition. Plant Physiol 89:1331–1336PubMedCrossRefGoogle Scholar
  85. Lee RB, Ratcliffe RG (1993) Subcellular distribution of inorganic phosphate, and levels of nucleoside triphosphate, in mature maize roots at low external phosphate concentrations: measurements with 31P-NMR. J Exp Bot 44:587–598CrossRefGoogle Scholar
  86. Lee RB, Ratcliffe RG, Southon TE (1990) 31P NMR measurements of the cytoplasmic and vacuolar Pi content of mature maize roots: relationships with phosphorus status and phosphate fluxes. J Exp Bot 41:1063–1078CrossRefGoogle Scholar
  87. Lee T-M, Tsai P-F, Shyu Y-T, Sheu F (2005) The effects of phosphite on phosphate starvation responses of Ulva lactuca (Ulvales, Chlorophyta). J Phycol 41:975–982CrossRefGoogle Scholar
  88. Linder HP (2008) Plant species radiations: where, when, why? Phil Trans Roy Soc Series B: Biol Sci 363:3097–3105CrossRefGoogle Scholar
  89. Loughman BC, Ratcliffe RG, Southon TE (1989) Observations on the cytoplasmic and vacuolar orthophosphate pools in leaf tissues using in vivo 31P-NMR spectroscopy. FEBS Lett 242:279–284CrossRefGoogle Scholar
  90. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  91. Mason B (1958) Principles of geochemistry. Wiley, New YorkGoogle Scholar
  92. Mast AR, Jones EH, Havery SP (2005) An assessment of old and new DNA sequence evidence for the paraphyly of Banksia with respect to Dryandra (Proteaceae). Aust Syst Bot 18:75–88CrossRefGoogle Scholar
  93. Matzek V, Vitousek PM (2009) N:P stoichiometry and protein:RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecol Lett 12:765–771PubMedCrossRefGoogle Scholar
  94. McArthur WM (1991) Reference soils of south-western Australia. Department of Agriculture Western Australia, South PerthGoogle Scholar
  95. McBirney AR (1993) Igneous petrology, 2nd edn. Jone and Bartlett, BostonGoogle Scholar
  96. Milberg P, Lamont BB (1997) Seed/cotyledon size and nutrient content play a major role in early performance of species on nutrient-poor soils. New Phytol 137:665–672CrossRefGoogle Scholar
  97. Mitchell PJ, Veneklaas EJ, Lambers H, Burgess SSO (2008a) Leaf water relations during summer water deficit: differential responses in turgor maintenance and variation in leaf structure among different plant communities in south-western Australia. Plant Cell Environ 31:1791–1802PubMedCrossRefGoogle Scholar
  98. Mitchell PJ, Veneklaas EJ, Lambers H, Burgess SSO (2008b) Using multiple trait associations to define hydraulic functional types in plant communities of south-western Australia. Oecologia 158:385–397PubMedCrossRefGoogle Scholar
  99. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedCrossRefGoogle Scholar
  100. Orians GH, Milewski AV (2007) Ecology of Australia: the effects of nutrient-poor soils and intense fires. Biol Rev 82:393–423PubMedCrossRefGoogle Scholar
  101. Pang J, Tibbett M, Denton M, Lambers H, Siddique K, Bolland M, Revell C, Ryan M (2010) Variation in seedling growth of 11 perennial legumes in response to phosphorus supply. Plant Soil 328:133–143CrossRefGoogle Scholar
  102. Parfitt RL, Ross DJ, Coomes DA, Richardson SJ, Smale MC, Dahlgren RA (2005) N and P in New Zealand soil chronosequences and relationships with foliar N and P. Biogeochemistry 75:305–328CrossRefGoogle Scholar
  103. Parks SE, Haigh AM, Cresswell GC (2000) Stem tissue phosphorus as an index of the phosphorus status of Banksia ericifolia L. f. Plant Soil 227:59–65CrossRefGoogle Scholar
  104. Pate J, Bell T (1999) Application of the ecosystem mimic concept to the species-rich Banksia woodlands of Western Australia. Agrofor Syst 45:303–341CrossRefGoogle Scholar
  105. Pate J, Dawson T (1999) Assessing the performance of woody plants in uptake and utilisation of carbon, water and nutrients: Implications for designing agricultural mimic systems. Agrofor Syst 45:245–275CrossRefGoogle Scholar
  106. Pate JS, Dell B (1984) Economy of mineral nutrients in sandplain species. In: Pate JS, Beard JS (eds) Kwongan. Plant life of the sandplain. University of Western Australia Press, NedlandsGoogle Scholar
  107. Pate JS, Verboom WH (2009) Contemporary biogenic formation of clay pavements by eucalypts: further support for the phytotarium concept. Ann Bot 103:673–685PubMedCrossRefGoogle Scholar
  108. Pate JS, Verboom WH, Galloway PD (2001) Co-occurrence of Proteaceae. Laterite and related oligotrophic soils: coincidental associations or causative inter-relationships. Aust J Bot 49:529–560CrossRefGoogle Scholar
  109. Playford P (1998) Voyage of discovery to Terra Australis by Willem de Vlamingh in 1696–97. Western Australian Museum, PerthGoogle Scholar
  110. Playsted CWS, Johnstonargaret ME, Ramage CM, Edwards DG, Cawthray GR, Lambers H (2006) Functional significance of dauciform roots: exudation of carboxylates and acid phosphatase under phosphorus deficiency in Caustis blakei (Cyperaceae). New Phytol 170:491–500PubMedCrossRefGoogle Scholar
  111. Poorter H, Evans JR (1998) Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area. Oecologia 116:26–37CrossRefGoogle Scholar
  112. Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol 94:621–627PubMedCrossRefGoogle Scholar
  113. Poot P, Lambers H (2003) Are trade-offs in allocation pattern and root morphology related to species abundance? A congeneric comparison between rare and common species in the south-western Australian flora. J Ecol 91:58–67CrossRefGoogle Scholar
  114. Poot P, Lambers H (2008) Shallow-soil endemics: adaptive advantages and constraints of a specialized root-system morphology. New Phytol 178:371–381PubMedCrossRefGoogle Scholar
  115. Raven JA (2008) Phosphorus and the future. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions. Springer, Dordrecht, pp 271–283CrossRefGoogle Scholar
  116. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006PubMedCrossRefGoogle Scholar
  117. Richardson S, Peltzer D, Allen R, McGlone M, Parfitt R (2004) Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139:267–276PubMedCrossRefGoogle Scholar
  118. Roelofs RFR, Rengel Z, Cawthray GR, Dixon KW, Lambers H (2001) Exudation of carboxylates in Australian Proteaceae: chemical composition. Plant Cell Environ 24:891–904CrossRefGoogle Scholar
  119. Rokich DP, Dixon KW, Sivasithsamparam K, Meney KA (2000) Topsoil handling and storage effects on woodland restoration in Western Australia. Restor Ecol 8:196–208CrossRefGoogle Scholar
  120. Roth-Nebelsick A, Hassiotou F, Veneklaas EJ (2009) Stomatal crypts have small effects on transpiration: a numerical model analysis. Plant Physiol 151:2018–2027PubMedCrossRefGoogle Scholar
  121. Rufty TWJ, Israel DW, Volk RJ, Qiu J, Sa T (1993) Phosphate regulation of nitrate assimilation in soybean. J Exp Bot 44:879–891CrossRefGoogle Scholar
  122. Rundel PW, Specht RL, Hopkins AJM, Montenegro G, Margaris NS (1988) Vegetation, nutrition and climate - data-tables. (2) Foliar analyses. In: Specht RL (ed) Tasks for vegetation science, 19: Mediterranean-type ecosystems. A data source book. Kluwer Academic, Dordrecht, pp 63–80Google Scholar
  123. Ryan MH, Ehrenberg S, Bennett RG, Tibbett M (2009) Putting the P in Ptilotus: a phosphorus-accumulating herb native to Australia. Ann Bot 103:901–911PubMedCrossRefGoogle Scholar
  124. Sañudo-Wilhelmy S, Kustka AB, Gobler CJ, Hutchins DA, Yang M, Lwiza K, Burns J, Capone DG, Raven JA, Carpenter EJ (2001) Phosphorus limitation of nitrogen fixation by Trichodesmium in the Central Atlantic Ocean. Nature 411:66–69PubMedCrossRefGoogle Scholar
  125. Sauquet H, Weston PH, Anderson CL, Barker NP, Cantrill DJ, Mast AR, Savolainen V (2009) Contrasted patterns of hyperdiversification in Mediterranean hotspots. Proc Natl Acad Sci USA 106:221–225PubMedCrossRefGoogle Scholar
  126. Schulze J, Temple GA, Temple SJ, Beschow H, Vance CP (2006) Nitrogen fixation by white lupin under phosphorus deficiency. Ann Bot 98:731–740PubMedCrossRefGoogle Scholar
  127. Selmants PC, Hart SC (2010) Phosphorus and soil development: does the Walker and Syers model apply to semiarid ecosystems? Ecology 91:474–484PubMedCrossRefGoogle Scholar
  128. Shane M, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125CrossRefGoogle Scholar
  129. Shane MW, Lambers H (2006) Systemic suppression of cluster-root formation and net P-uptake rates in Grevillea crithmifolia at elevated P supply: a proteacean with resistance for developing symptoms of ‘P toxicity’. J Exp Bot 57:413–423PubMedCrossRefGoogle Scholar
  130. Shane M, Szota C, Lambers H (2004a) A root trait accounting for the extreme phosphorus sensitivity of Hakea prostrata (Proteaceae). Plant Cell Environ 27:991–1004CrossRefGoogle Scholar
  131. Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004b) Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiol 135:549–560PubMedCrossRefGoogle Scholar
  132. Shane MW, McCully ME, Lambers H (2004c) Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). J Exp Bot 55:1033–1044PubMedCrossRefGoogle Scholar
  133. Shane M, Cawthray G, Cramer M, Kuo J, Lambers H (2006) Specialized ‘dauciform’ roots of Cyperaceae are structurally distinct, but functionally analogous with ‘cluster’ roots. Plant Cell Environ 29:1989–1999PubMedCrossRefGoogle Scholar
  134. Shane M, Lambers H, Cawthray G, Kuhn A, Schurr U (2008a) Impact of phosphorus mineral source (Al–P or Fe–P) and pH on cluster-root formation and carboxylate exudation in Lupinus albus L. Plant Soil 304:169–178CrossRefGoogle Scholar
  135. Shane MW, Cramer MD, Lambers H (2008b) Root of edaphically controlled Proteaceae turnover on the Agulhas Plain, South Africa: phosphate uptake regulation and growth. Plant Cell Environ 31:1825–1833PubMedCrossRefGoogle Scholar
  136. Shearer BL, Fairman RG (2007) Application of phosphite in a high-volume foliar spray delays and reduces the rate of mortality of four Banksia species infected with Phytophthora cinnamomi. Australas Plant Pathol 36:358–368CrossRefGoogle Scholar
  137. Shearer BL, Crane CE, Fairman RG, Dunne CP (2009) Ecosystem dynamics altered by pathogen-mediated changes following invasion of Banksia woodland and Eucalyptus marginata forest biomes of south-western Australia by Phytophthora cinnamomi. Australas Plant Pathol 38:417–436CrossRefGoogle Scholar
  138. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press and Elsevier, LondonGoogle Scholar
  139. Standish R, Hobbs R (2010) Restoration of OCBILs in south-western Australia: response to Hopper. Plant Soil 330:15–18CrossRefGoogle Scholar
  140. Sterner R, Elser JJ (2002) Ecological stoichiometry: the biiology of elements from molecules to the biosphere. Princetion University Press, PrincetonGoogle Scholar
  141. Stock WD, Allsopp N, Van der Heyden F, Witkowski ETF (1997) Plant form and function. In: Cowling RM, Richardson DM, Pierce SM (eds) Vegetation of Southern Africa. Cambridge University Press, Cambridge, pp 376–396Google Scholar
  142. Taylor LL, Leake JR, Quirk J, Hardy K, Banwart SA, Beerling DJ (2009) Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm. Geobiology 7:171–191PubMedCrossRefGoogle Scholar
  143. Theodorou ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101:339–344PubMedGoogle Scholar
  144. Ticconi CA, Delatorre CA, Abel S (2001) Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiol 127:963–972PubMedCrossRefGoogle Scholar
  145. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37:801PubMedCrossRefGoogle Scholar
  146. Tjellström H, Andersson MX, Larsson KE, Sandelius AS (2008) Membrane phospholipids as a phosphate reserve: the dynamic nature of phospholipid-to-digalactosyl diacylglycerol exchange in higher plants. Plant Cell Environ 31:1388–1398PubMedCrossRefGoogle Scholar
  147. Van Mooy BAS, Rocap G, Fredricks HF, Evans CT, Devol AH (2006) Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc Natl Acad Sci USA 103:8607–8612PubMedCrossRefGoogle Scholar
  148. Van Mooy BAS, Fredricks HF, Pedler BE, Dyhrman ST, Karl DM, Koblizek M, Lomas MW, Mincer TJ, Moore LR, Moutin T, Rappe MS, Webb EA (2009) Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458:69–72PubMedCrossRefGoogle Scholar
  149. Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447CrossRefGoogle Scholar
  150. Varadarajan DK, Karthikeyan AS, Matilda PD, Raghothama KG (2002) Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol 129:1232–1240PubMedCrossRefGoogle Scholar
  151. Verboom WH, Pate JS (2003) Relationships between cluster root-bearing taxa and laterite across landscapes in southwest Western Australia: an approach using airborne radiometric and digital elevation models. Plant Soil 248:321–333CrossRefGoogle Scholar
  152. Verboom WH, Pate JS (2006) Bioengineering of soil profiles in semiarid ecosystems: the ‘phytotarium’ concept. A review. Plant Soil 289:71–102CrossRefGoogle Scholar
  153. Vinogradov AP (1962) Average content of chemical elements in the principal types of igneous rocks in the earth’s crust. Geochemistry 7:641–664Google Scholar
  154. Vitousek PM, Field CB (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46:179–202Google Scholar
  155. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15PubMedCrossRefGoogle Scholar
  156. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–9CrossRefGoogle Scholar
  157. Westman WE, Rogers RW (1977) Nutrient stocks in a sub-tropical eucalypt forest, North Stradbroke Island. Aust J Ecol 4:447–460Google Scholar
  158. White AK, Metcalf WW (2007) Microbial metabolism of reduced phosphorus compounds. Annu Rev Microbiol 61:379–400PubMedCrossRefGoogle Scholar
  159. Williams ML, Thomas BJ, Farrar JF, Pollock CJ (1993) Visualizing the distribution of elements within barley leaves by Energy Dispersive X-Ray Image Maps (EDX Maps). New Phytol 125:367–372CrossRefGoogle Scholar
  160. Witkowski ETF, Lamont BB (1996) Disproportionate allocation of mineral nutrients and carbon between vegetative and reproductive structures in Banksia hookeriana. Oecologia 105:38–42CrossRefGoogle Scholar
  161. Wright IJ, Cannon K (2001) Relationships between leaf lifespan and structural defences in a low-nutrient, sclerophyll flora. Funct Ecol 15:351–359CrossRefGoogle Scholar
  162. Wright IJ, Westoby M, Reich PB (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. J Ecol 90:534–543CrossRefGoogle Scholar
  163. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827PubMedCrossRefGoogle Scholar
  164. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005) Assessing the generality of global leaf trait relationships. New Phytol 166:485–496PubMedCrossRefGoogle Scholar
  165. Yamaryo Y, Dubots E, Albrieux C, Baldan B, Block MA (2008) Phosphate availability affects the tonoplast localization of PLD[zeta]2, an Arabidopsis thaliana phospholipase D. FEBS Lett 582:685–690PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Hans Lambers
    • 1
  • Mark C. Brundrett
    • 1
  • John A. Raven
    • 1
    • 2
  • Stephen D. Hopper
    • 1
    • 3
  1. 1.School of Plant BiologyThe University of Western AustraliaCrawleyAustralia
  2. 2.Division of Plant SciencesUniversity of Dundee at SCRI, Scottish Crop Research InstituteDundeeUK
  3. 3.Royal Botanic Gardens, KewRichmondUK

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