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Mineral Nutrition of Plants in Australia’s Arid Zone

  • Honghua He
  • David J. Eldridge
  • Hans Lambers
Chapter

Abstract

Australia’s arid-zone soils are highly leached and resorted (Winkworth 1967; Pillans 2018) and characterised by low levels of available water and nutrients (Orians and Milewski 2007). These soils are particularly low in total phosphorus (P) and nitrogen (N) (Islam et al. 2000; Bennett and Adams 2001; Grigg et al. 2008a). The distribution of these and other nutrients is typically heterogeneous, due to the development of ‘islands of fertility’ and tight nutrient cycling beneath the canopies of long-lived perennial plants (Tongway and Ludwig 1994; He et al. 2011). Nutrient cycling and decomposition of leaf litter are largely restricted to periods after rain, when bacteria (Skopp et al. 1990; Ford et al. 2007) and cyanobacteria, either free-living or as components of biological soil crusts (biocrusts), are active (Austin et al. 2004). Termites also play an important role in litter decomposition and nutrient cycling and contribute to the patchy distribution of nutrients (Tongway et al. 1989; Park et al. 1994).

References

  1. Almeida JPF, Hartwig UA, Frehner M, Nosberger J, Luscher A (2000) Evidence that P deficiency induces N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.). J Exp Bot 51:1289–1297PubMedGoogle Scholar
  2. Anderson CWN, Brooks RR, Stewart RB, Simcock R (1998) Harvesting a crop of gold in plants. Nature 395:553–554CrossRefGoogle Scholar
  3. Anderson CWN, Brooks RR, Chiarucci A, LaCoste CJ, Leblanc M, Robinson BH, Simcock R, Stewart RB (1999) Phytomining for nickel, thallium and gold. J Geochem Explor 67:407–415CrossRefGoogle Scholar
  4. Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235CrossRefGoogle Scholar
  5. Baird IRC (2014) A novel observation of putative aerial hemiparasitism in Exocarpus aphyllus. Queensland Nat 52:48–52Google Scholar
  6. Baran R, Brodie EL, Mayberry-Lewis J, Hummel E, Da Rocha UN, Chakraborty R, Bowen BP, Karaoz U, Cadillo-Quiroz H, Garcia-Pichel F, Northen TR (2015) Exometabolite niche partitioning among sympatric soil bacteria. Nat Commun 6:8289CrossRefPubMedPubMedCentralGoogle Scholar
  7. Barger N, Weber B, Garcia-Pichel F, Zaady E, Belnap J (2016) Patterns and controls on nitrogen cycling of biological soil crusts. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organising principle in drylands, Ecological series 226. Springer, Dordrecht, pp 257–285CrossRefGoogle Scholar
  8. Barnes CJ, Jacobson G, Smith GD (1992) The origin of high-nitrate ground waters in the Australian arid zone. J Hydrol 137:181–197CrossRefGoogle Scholar
  9. Bennett LT, Adams MA (2001) Response of a perennial grassland to nitrogen and phosphorus additions in sub-tropical, semi-arid Australia. J Arid Environ 48:289–308CrossRefGoogle Scholar
  10. Bidwell SD (2001) Hyperaccumulation of metals in Australian native plants. PhD thesis, The University of Melbourne, AustraliaGoogle Scholar
  11. Bidwell SD, Woodrow IE, Batianoff GN, Sommer-Knudsen J (2002) Hyperaccumulation of manganese in the rainforest tree Austromyrtus bidwillii (Myrtaceae) from Queensland, Australia. Funct Plant Biol 29:899–905CrossRefGoogle Scholar
  12. Bidwell SD, Crawford SA, Woodrow IE, Sommer-Knudsen J, Marshall AT (2004) Sub-cellular localization of Ni in the hyperaccumulator, Hybanthus floribundus (Lindley) F. Muell. Plant Cell Environ 27:705–716CrossRefGoogle Scholar
  13. Bodine MC, Ueckert DN (1975) Effect of desert termites on herbage and litter in a shortgrass ecosystem in west Texas. Rangel Ecol Manag/J Range Manag Arch 28:353–358Google Scholar
  14. Bowker MA, Belnap J, Davidson DW, Phillips SL (2005) Evidence for micronutrient limitation of biological soil crusts: importance to arid-lands restoration. Ecol Appl 15:1941–1951CrossRefGoogle Scholar
  15. Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Functions of nutrients: micronutrients. In: Marschner P (ed) Mineral nutrition of higher plants. Academic Press, London, pp 191–248CrossRefGoogle Scholar
  16. Brooks RR, Lee J, Reeves RD, Jaffre T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57CrossRefGoogle Scholar
  17. Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362CrossRefGoogle Scholar
  18. Cernusak LA, Pate JS, Farquhar GD (2004) Oxygen and carbon isotope composition of parasitic plants and their hosts in southwestern Australia. Oecologia 139:199–213CrossRefPubMedGoogle Scholar
  19. Coventry R, Holt J, Sinclair D (1988) Nutrient cycling by mound building termites in low fertility soils of semi-arid tropical Australia. Soil Res 26:375–390CrossRefGoogle Scholar
  20. Curtis AD, Waller DA (1998) Seasonal patterns of nitrogen fixation in termites. Funct Ecol 12:803–807CrossRefGoogle Scholar
  21. Davies AB, Eggleton P, van Rensburg BJ, Parr CL (2015) Seasonal activity patterns of African savanna termites vary across a rainfall gradient. Insect Soc 62:157–165CrossRefGoogle Scholar
  22. de Bruyn LAL, Conacher AJ (1990) The role of termites and ants in soil modification – a review. Soil Res 28:55–93Google Scholar
  23. de Bruyn LAL, Conacher AJ (1995) Soil modification by termites in the central wheatbelt of Australia. Aust J Soil Res 33:179–193CrossRefGoogle Scholar
  24. de Campos MCR, Pearse SJ, Oliveira RS, Lambers H (2013) Downregulation of net phosphorus-uptake capacity is inversely related to leaf phosphorus-resorption proficiency in four species from a phosphorus-impoverished environment. Ann Bot 111:445–454CrossRefPubMedPubMedCentralGoogle Scholar
  25. Delgado M, Suriyagoda L, Zúñiga-Feest A, Borie F, Lambers H (2014) Divergent functioning of Proteaceae species: the South American Embothrium coccineum displays a combination of adaptive traits to survive in high-phosphorus soils. Funct Ecol 28:1356–1366CrossRefGoogle Scholar
  26. Delgado M, Zuniga-Feest A, Almonacid L, Lambers H, Borie F (2015) Cluster roots of Embothrium coccineum (Proteaceae) affect enzyme activities and phosphorus lability in rhizosphere soil. Plant Soil 395:189–200CrossRefGoogle Scholar
  27. Denton MD, Veneklaas EJ, Freimoser FM, 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 30:1557–1565CrossRefPubMedGoogle Scholar
  28. Denton MD, Veneklaas EJ, Lambers H (2007b) Does phenotypic plasticity in carboxylate exudation differ among rare and widespread Banksia species (Proteaceae)? New Phytol 173:592–599CrossRefPubMedGoogle Scholar
  29. Desai MS, Brune A (2012) Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry-wood termites. ISME J 6:1302–1313CrossRefPubMedGoogle Scholar
  30. Dojani S, Lakatos M, Rascher U, Wanek W, Luettge U, Buedel B (2007) Nitrogen input by cyanobacterial biofilms of an inselberg into a tropical rainforest in French Guiana. Flora 202:521–529CrossRefGoogle Scholar
  31. Ehleringer JR, Schulze ED, Ziegler H, Lange OL, Farquhar GD, Cowar IR (1985) Xylem-tapping mistletoes: water or nutrient parasites? Science (New York, NY) 227:1479–1481CrossRefGoogle Scholar
  32. Elbert W, Weber B, Burrows S, Steinkamp J, Budel B, Andreae MO, Poschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462CrossRefGoogle Scholar
  33. Eldridge DJ (1996) Distribution and floristics of terricolous lichens in soil crusts in arid and semi-arid New South Wales, Australia. Aust J Bot 44:581–599CrossRefGoogle Scholar
  34. Eldridge DJ (2003) Biological soil crusts of Australia. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 119–132Google Scholar
  35. Eldridge DJ, Beecham G (2016) The impact of climate variability on land use and livelihoods in Australia’s rangelands. In: Gaur MK, Squires VR (eds) Climate variability impacts on land use and livelihoods in drylands. Springer, Dordrecht, pp 293–318Google Scholar
  36. Eldridge DJ, Greene RSB (1994) Microbiotic soil crusts: a review of their roles in soil and ecological process in the rangelands of Australia. Aust J Soil Res 32:389–415CrossRefGoogle Scholar
  37. Eldridge DJ, Leys JF (2003) Exploring some relationships between biological soil crusts, soil aggregation and wind erosion. J Arid Environ 53:457–466CrossRefGoogle Scholar
  38. Eldridge DJ, Bowker MA, Maestre FT, Alonso P, Mau RL, Papadopoulos J, Escudero A (2010) Interactive effects of three ecosystem engineers on infiltration in a semi-arid mediterranean grassland. Ecosystems 13:499–510CrossRefGoogle Scholar
  39. Ernst WHO (1998) Sulfur metabolism in higher plants: potential for phytoremediation. Biodegradation 9:311–318CrossRefPubMedGoogle Scholar
  40. Erskine PD, Stewart GR, Schmidt S, Turnbull MH, Unkovich M, Pate JS (1996) Water availability – a physiological constraint on nitrate utilization in plants of Australian semi-arid mulga woodlands. Plant Cell Environ 19:1149–1159CrossRefGoogle Scholar
  41. Fernando DR, Guymer G, Reeves RD, Woodrow IE, Baker AJ, Batianoff GN (2009) Foliar Mn accumulation in eastern Australian herbarium specimens: prospecting for ‘new’ Mn hyperaccumulators and potential applications in taxonomy. Ann Bot 103:931–939CrossRefPubMedPubMedCentralGoogle Scholar
  42. Fernando DR, Woodrow IE, Baker AJM, Marshall AT (2012) Plant homeostasis of foliar manganese sinks: specific variation in hyperaccumulators. Planta 236:1459–1470CrossRefPubMedGoogle Scholar
  43. Ford DJ, Cookson WR, Adams MA, Grierson PF (2007) Role of soil drying in nitrogen mineralization and microbial community function in semi-arid grasslands of north-west Australia. Soil Biol Biochem 39:1557–1569CrossRefGoogle Scholar
  44. Getzin S, Yizhaq H, Bell B, Erickson TE, Postle AC, Katra I, Tzuk O, Zelnik YR, Wiegand K, Wiegand T, Meron E (2016) Discovery of fairy circles in Australia supports self-organization theory. Proc Natl Acad Sci U S A 113:3551–3556CrossRefPubMedPubMedCentralGoogle Scholar
  45. Goldie X, Gillman L, Crisp M, Wright S (2010) Evolutionary speed limited by water in arid Australia. Proc R Soc B Biol Sci 277:2645–2653CrossRefGoogle Scholar
  46. Gonzalez-Orozco CE, Laffan SW, Miller JT (2011) Spatial distribution of species richness and endemism of the genus Acacia in Australia. Aust J Bot 59:600–608CrossRefGoogle Scholar
  47. Greenwood DJ, Karpinets TV, Zhang K, Bosh-Serra A, Boldrini A, Karawulova L (2008) A unifying concept for the dependence of whole-crop N:P ratio on biomass: theory and experiment. Ann Bot 102:967–977CrossRefPubMedPubMedCentralGoogle Scholar
  48. Grigg A (2009) An ecophysiological approach to determine problems associated with mine-site rehabilitation: a case study in the Great Sandy Desert, north-western Australia. PhD Thesis, The University of Western AustraliaGoogle Scholar
  49. 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
  50. 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
  51. Groom PK, Lamont BB (2010) Phosphorus accumulation in Proteaceae seeds: a synthesis. Plant Soil 334:61–72CrossRefGoogle Scholar
  52. Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266CrossRefGoogle Scholar
  53. 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 Hortic 117:357–365CrossRefGoogle Scholar
  54. Hayes P, Turner BL, Lambers H, Laliberte E (2014) Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102:396–410CrossRefGoogle Scholar
  55. Hayes PE, Clode PL, Oliveira RS, Lambers H (2018) Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: an adaptation improving phosphorus-use efficiency. Plant Cell Environ 41:605–619Google Scholar
  56. He H, Bleby TM, Veneklaas EJ, Lambers H (2011) Dinitrogen-fixing Acacia species from phosphorus-impoverished soils resorb leaf phosphorus efficiently. Plant Cell Environ 34:2060–2070CrossRefPubMedGoogle Scholar
  57. He H, Bleby TM, Veneklaas EJ, Lambers H (2012a) Arid-zone Acacia species can access poorly soluble iron phosphate but show limited growth response. Plant Soil 358:119–130CrossRefGoogle Scholar
  58. He H, Bleby TM, Veneklaas EJ, Lambers H, Kuo J (2012b) Morphologies and elemental compositions of calcium crystals in phyllodes and branchlets of Acacia robeorum (Leguminosae: Mimosoideae). Ann Bot 109:887–896CrossRefPubMedPubMedCentralGoogle Scholar
  59. He H, Veneklaas EJ, Kuo J, Lambers H (2014) Physiological and ecological significance of biomineralization in plants. Trends Plant Sci 19:166–174Google Scholar
  60. Hellmuth EO (1971) Eco-physiological studies on plants in arid and semi-arid regions in Western Australia: IV. Comparison of the field physiology of the host, Acacia gasbyi and its hemiparasite, Amyema nestor under optimal and stress conditions. J Ecol 59:351–363CrossRefGoogle Scholar
  61. Hingston F, Malajczuk N, Grove T (1982) Acetylene reduction (N2-fixation) by jarrah forest legumes following fire and phosphate application. J Appl Ecol 19:631–645CrossRefGoogle Scholar
  62. Hinsinger P, Plassard C, Tang CX, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59CrossRefGoogle Scholar
  63. Hocking P (1986) Mineral nutrient composition of leaves and fruits of selected species of Grevillea from southwestern Australia, with special reference to Grevillea leucopteris Meissn. Aust J Bot 34:155–164CrossRefGoogle Scholar
  64. Islam M, Turner DW, Adams MA (2000) Regeneration of the legumes Acacia ancistrocarpa and Senna notabilis in the Pilbara region of Western Australia: mineral nutrition and carbon fractions. Aust J Bot 48:435–444CrossRefGoogle Scholar
  65. Ji R, Brune A (2006) Nitrogen mineralization, ammonia accumulation, and emission of gaseous NH3 by soil-feeding termites. Biogeochemistry 78:267–283CrossRefGoogle Scholar
  66. Kachenko AG, Singh B, Bhatia NP, Siegele R (2008) Quantitative elemental localisation in leaves and stems of nickel hyperaccumulating shrub Hybanthus floribundus subsp floribundus using micro-PIXE spectroscopy. Nucl Instrum Methods Phys Res Sect B Beam Interact Mater Atoms 266:667–676CrossRefGoogle Scholar
  67. Kersten WJ, Brooks RR, Reeves RD, Jaffré A (1980) Nature of nickel complexes in Psychotria douarrei and other nickel-accumulating plants. Phytochemistry 19:1963–1965CrossRefGoogle Scholar
  68. Kirkby E (2012) Introduction, definition and classification of nutrients. In: Marschner P (ed) Mineral nutrition of higher plants. Academic Press, London, pp 3–5CrossRefGoogle Scholar
  69. Kleiner EF, Harper KT (1972) Environment and communiy organization in grasslands of Canyonlands National Park. Ecology 53:299–309CrossRefGoogle Scholar
  70. 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
  71. Kouas S, Louche J, Debez A, Plassard C, Drevon JJ, Abdelly C (2009) Effect of phosphorus deficiency on acid phosphatase and phytase activities in common bean (Phaseolus vulgaris L.) under symbiotic nitrogen fixation. Symbiosis 47:141–149CrossRefGoogle Scholar
  72. Kuo J (1982) Nutrient reserves in seeds of selected Proteaceous species from south-western Australia. Aust J Bot 30:231–249CrossRefGoogle Scholar
  73. Lambers H, Teste FP (2013) Interactions between arbuscular mycorrhizal and non-mycorrhizal plants: do non-mycorrhizal species at both extremes of nutrient availability play the same game? Plant Cell Environ 36:1911–1915PubMedGoogle Scholar
  74. 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 98:693–713CrossRefPubMedPubMedCentralGoogle Scholar
  75. Lambers H, Thijs LP, Chapin FS (2008) Plant physiological ecology. Springer, New YorkCrossRefGoogle Scholar
  76. 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
  77. Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberte E, Pearse SJ, Scheible W-R, Stitt M, Teste F, Turner BL (2012) Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytol 196:1098–1108CrossRefPubMedGoogle Scholar
  78. Lambers H, Ahmedi I, Berkowitz O, Dunne C, Finnegan PM, Hardy GESJ, Jost R, Laliberte E, Pearse SJ, Teste FP (2013) Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. Conserv Physiol 1:cot010CrossRefPubMedPubMedCentralGoogle Scholar
  79. Lambers H, Clode PL, Hawkins H-J, Laliberte E, Oliveira RS, Reddell P, Shane MW, Stitt M, Weston P (2015a) Metabolic adaptations of the non-mycotrophic Proteaceae to soil with a low phosphorus availability. In: Plaxton WC, Lambers H (eds) Phosphorus metabolism in plants. Wiley, Chichester, pp 289–335Google Scholar
  80. Lambers H, Hayes PE, Laliberte E, Oliveira RS, Turner BL (2015b) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20:83–90CrossRefGoogle Scholar
  81. Lilburn TC, Kim KS, Ostrom NE, Byzek KR, Leadbetter JR, Breznak JA (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292:2495–2498CrossRefPubMedGoogle Scholar
  82. Lintern MJ, Butt CRM, Scott KM (1997) Gold in vegetation and soil – three case studies from the goldfields of southern Western Australia. J Geochem Explor 58:1–14CrossRefGoogle Scholar
  83. Maestre FT, Escolar C, Ladron De Guevara M, Quero JL, Lazaro R, Delgado-Baquerizo M, Ochoa V, Berdugo M, Gozalo B, Gallardo A (2013) Changes in biocrust cover drive carbon cycle responses to climate change in drylands. Glob Chang Biol 19:3835–3847CrossRefPubMedPubMedCentralGoogle Scholar
  84. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  85. Marsudi NDS, Glenn AR, Dilworth MJ (1999) Identification and characterization of fast- and slow-growing root nodule bacteria from South-Western Australian soils able to nodulate Acacia saligna. Soil Biol Biochem 31:1229–1238CrossRefGoogle Scholar
  86. Melchiorre EB, Williams PA, Rose TP, Talyn BC (2006) Biogenic nitrogen from termite mounds and the origin of gerhardtite at the great Australia mine, Cloncurry, Queensland, Australia. Can Mineral 44:1447–1455CrossRefGoogle Scholar
  87. 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
  88. Morillas L, Gallardo A (2015) Biological soil crusts and wetting events: effects on soil N and C cycles. Appl Soil Ecol 94:1–6CrossRefGoogle Scholar
  89. Morton SR, Smith DMS, Dickman CR, Dunkerley DL, Friedel MH, McAllister RRJ, Reid JRW, Roshier DA, Smith MA, Walsh FJ, Wardle GM, Watson IW, Westoby M (2011) A fresh framework for the ecology of arid Australia. J Arid Environ 75:313–329CrossRefGoogle Scholar
  90. Ndiaye D, Lepage M, Sall CE, Brauman A (2004) Nitrogen transformations associated with termite biogenic structures in a dry savanna ecosystem. Plant Soil 265:189–196CrossRefGoogle Scholar
  91. Ngugi DK, Ji R, Brune A (2011) Nitrogen mineralization, denitrification, and nitrate ammonification by soil-feeding termites: a 15N-based approach. Biogeochemistry 103:355–369CrossRefGoogle Scholar
  92. Noble JC, Müller WJ, Whitford WG, Pfitzner GH (2009) The significance of termites as decomposers in contrasting grassland communities of semi-arid eastern Australia. J Arid Environ 73:113–119CrossRefGoogle Scholar
  93. Orians GH, Milewski AV (2007) Ecology of Australia: the effects of nutrient-poor soils and intense fires. Biol Rev 82:393–423CrossRefPubMedGoogle Scholar
  94. Palomo L, Claassenb N, Jones DL (2006) Differential mobilization of P in the maize rhizosphere by citric acid and potassium citrate. Soil Biol Biochem 38:683–692CrossRefGoogle Scholar
  95. Park HC, Majer JD, Hobbs RJ (1994) Contribution of the Western Australian wheatbelt termite, Drepanotermes tamminensis (Hill), to the soil nutrient budget. Ecol Res 9:351–356CrossRefGoogle Scholar
  96. Pate JS, Davidson NJ, Kuo J, Milburn JA (1990) Water relations of the root hemiparasite Olax phyllanthi (Labill) R.Br. (Olacaceae) and its multiple hosts. Oecologia 84:186–193CrossRefPubMedGoogle Scholar
  97. Pate JS, Unkovich MJ, Erskine PD, Stewart GR (1998) Australian mulga ecosystems – 13C and 15N natural abundances of biota components and their ecophysiological significance. Plant Cell Environ 21:1231–1242CrossRefGoogle Scholar
  98. 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
  99. Piccinin RCR, Ebbs SD, Reichman SM, Kolev SD (2007) A screen of some native Australian flora and exotic agricultural species for their potential application in cyanide-induced phytoextraction of gold. Miner Eng 20:1327–1330CrossRefGoogle Scholar
  100. Pillans B (2018) Seeing red: some aspects of the geological and climatic history of the Australian arid zone. In: Lambers H (ed) On the ecology of Australia’s arid zone. Springer, DordrechtGoogle Scholar
  101. Prodhan MA, Jost R, Watanabe M, Hoefgen R, Lambers H, Finnegan PM (2016) Tight control of nitrate acquisition in a plant species that evolved in an extremely phosphorus-impoverished environment. Plant Cell Environ 39:2754–2761CrossRefPubMedGoogle Scholar
  102. Prodhan MA, Jost R, Watanabe M, Hoefgen R, Lambers H, Finnegan PM (2017) Tight control of sulfur assimilation: an adaptive mechanism for a plant from a severely phosphorus-impoverished habitat. New Phytol 215:1068–1079CrossRefPubMedGoogle Scholar
  103. Radomiljac AM, McComb JA, Pate JS (1999) Gas exchange and water relations of the root hemi-parasite Santalum album L. in association with legume and non-legume hosts. Ann Bot 83:215–224CrossRefGoogle Scholar
  104. Reid N, Lange RT (1988) Host specificity, dispersion and persistence through drought of two arid zone mistletoes. Aust J Bot 36:299–313CrossRefGoogle Scholar
  105. Reid N, Robson TC, Radcliffe B, Verrall M (2016) Excessive sulphur accumulation and ionic storage behaviour identified in species of Acacia (Leguminosae: Mimosoideae). Ann Bot 117:653–666CrossRefPubMedPubMedCentralGoogle Scholar
  106. Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156CrossRefGoogle Scholar
  107. Robson T, Stevens J, Dixon K, Reid N (2017a) Foliar gypsum formation and litter production in the desert shrub, Acacia bivenosa, influences sulfur and calcium biogeochemical cycling in arid habitats. Plant Soil 417:1–16CrossRefGoogle Scholar
  108. Robson T, Stevens J, Dixon K, Reid N (2017b) Sulfur accumulation in gypsum-forming thiophores has its roots firmly in calcium. Environ Exp Bot 137:208–219CrossRefGoogle Scholar
  109. Roelofs RFR, Rengel Z, Cawthray GR, Dixon KW, Lambers H (2001) Exudation of carboxylates in Australian Proteaceae: chemical composition. Plant Cell Environ 24:891–903CrossRefGoogle Scholar
  110. Rogers RW (1971) Distribution of the lichen Chondropsis semiviridis in relation to its heat and drought resistance. New Phytol 70:1069–1077CrossRefGoogle Scholar
  111. Schaefer DA, Whitford WG (1981) Nutrient cycling by the subterranean termite Gnathamitermes tubiformans in a Chihuahuan desert ecosystem. Oecologia 48:277–283CrossRefPubMedGoogle Scholar
  112. Schortemeyer M, Atkin OK, McFarlane N, Evans JR (2002) N2 fixation by Acacia species increases under elevated atmospheric CO2. Plant Cell Environ 25:567–579CrossRefGoogle Scholar
  113. Severne BC (1974) Nickel accumulation by Hybanthus floribundus. Nature 248:807–808CrossRefPubMedGoogle Scholar
  114. Severne BC, Brooks RR (1972) A nickel-accumulating plant from Western Australia. Planta 103:91–94CrossRefPubMedGoogle Scholar
  115. Shane MW, Lambers H (2005a) Cluster roots: a curiosity in context. Plant Soil 274:101–125CrossRefGoogle Scholar
  116. Shane MW, Lambers H (2005b) Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol Plant 124:441–450CrossRefGoogle Scholar
  117. 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 57:413–423CrossRefPubMedGoogle Scholar
  118. Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004a) Development physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiol 135:549–560CrossRefPubMedPubMedCentralGoogle Scholar
  119. Shane MW, McCully ME, Lambers H (2004b) Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). J Exp Bot 55:1033–1044CrossRefPubMedGoogle Scholar
  120. Shane MW, Szota C, Lambers H (2004c) A root trait accounting for the extreme phosphorus sensitivity of Hakea prostrata (Proteaceae). Plant Cell Environ 27:991–1004CrossRefGoogle Scholar
  121. Shane MW, Stigter K, Fedosejevs ET, Plaxton WC (2014) Senescence-inducible cell wall and intracellular purple acid phosphatases: implications for phosphorus remobilization in Hakea prostrata (Proteaceae) and Arabidopsis thaliana (Brassicaceae). J Exp Bot 65:6097–6106CrossRefPubMedPubMedCentralGoogle Scholar
  122. Skopp J, Jawson MD, Doran JW (1990) Steady-state aerobic microbial activity as a function of soil water content. Soil Sci Soc Am J 54:1619–1625CrossRefGoogle Scholar
  123. Smith FR, Yeaton RI (1998) Disturbance by the mound-building termite, Trinervitermes trinervoides, and vegetation patch dynamics in a semi-arid, southern African grassland. Plant Ecol 137:41–53CrossRefGoogle Scholar
  124. Starks TL, Shubert LE (1979) Algal colonization on a reclaimed surface mined area in western North Dakota. In: Wali MK (ed) Ecology and coal resource development. Pergamon Press, New York, pp 652–660CrossRefGoogle Scholar
  125. Strauss SL, Day TA, Garcia-Pichel F (2012) Nitrogen cycling in desert biological soil crusts across biogeographic regions in the Southwestern United States. Biogeochemistry 108:171–182CrossRefGoogle Scholar
  126. Sulpice R, Ishihara H, Schlereth A, Cawthray GR, Encke B, Giavalisco P, Ivakov A, Arrivault S, Jost R, Krohn N, Kuo J, Laliberte E, Pearse SJ, Raven JA, Scheible W-R, Teste F, Veneklaas EJ, Stitt M, Lambers H (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant Cell Environ 37:1276–1298CrossRefPubMedPubMedCentralGoogle Scholar
  127. Takeshita M, Araya T (2004) Soil nutrient loss caused by intensive land use and the retention of nutrients inside termite mounds in Niger, Africa. Jpn J Ecol (Otsu) 54:117–124Google Scholar
  128. Tayasu I, Sugimoto A, Wada E, Abe T (1994) Xylophagous termites depending on atmospheric nitrogen. Naturwissenschaften 81:229–231CrossRefGoogle Scholar
  129. Tennakoon KU, Pate JS, Arthur D (1997) Ecophysiological aspects of the woody root hemiparasite Santalum acuminatum (R Br) A DC and its common hosts in south western Australia. Ann Bot 80:245–256CrossRefGoogle Scholar
  130. Tongway DJ, Ludwig JA (1994) Small-scale resource heterogeneity in semi-arid landscapes. Pac Conserv Biol 1:201–208CrossRefGoogle Scholar
  131. Tongway DJ, Ludwig JA, Whitford WG (1989) Mulga log mounds: fertile patches in the semi-arid woodlands of eastern Australia. Aust J Ecol 14:263–268CrossRefGoogle Scholar
  132. Ullmann I, Lange OL, Ziegler H, Ehleringer J, Schulze ED, Cowan IR (1985) Diurnal courses of leaf conductance and transpiration of mistletoes and their hosts in Central Australia. Oecologia 67:577–587CrossRefPubMedGoogle Scholar
  133. van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334CrossRefGoogle Scholar
  134. van Etten EJB, Burrows ND (2018) Fire regimes and ecology of arid Australia. In: Lambers H (ed) On the ecology of Australia’s arid zone. Springer, DordrechtGoogle Scholar
  135. Veluci RM, Neher DA, Weicht TR (2006) Nitrogen fixation and leaching of biological soil crust communities in mesic temperate soils. Microb Ecol 51:189–196CrossRefPubMedGoogle Scholar
  136. Watt M, Evans JR (1999) Proteoid roots. Physiology and development. Plant Physiol 121:317–323CrossRefPubMedPubMedCentralGoogle Scholar
  137. Weber B, Wu D, Tamm A, Ruckteschler N, Rodriguez-Caballero E, Steinkamp J, Meusel H, Elbert W, Behrendt T, Soergel M, Cheng Y, Crutzen PJ, Su H, Poeschi U (2015) Biological soil crusts accelerate the nitrogen cycle through large NO and HONO emissions in drylands. Proc Natl Acad Sci U S A 112:15384–15389CrossRefPubMedPubMedCentralGoogle Scholar
  138. Weber B, Büdel B, Belnap J (2017) Biological soil crusts: an organising principle in drylands, Ecological series 226. Springer, DordrechtGoogle Scholar
  139. Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E (2006a) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29:919–927CrossRefGoogle Scholar
  140. Weisskopf L, Tomasi N, Santelia D, Martinoia E, Langlade NB, Tabacchi R, Abou-Mansour E (2006b) Isoflavonoid exudation from white lupin roots is influenced by phosphate supply, root type and cluster-root stage. New Phytol 171:657–668PubMedGoogle Scholar
  141. Whitford W, Eldridge DJ (2013) Effects of ants and termites on soil and geomorphological processes. In: Schroder JF (ed) A treatise on geomophology, Methods in geomorphology, vol 14. Academic Press, San DiegoGoogle Scholar
  142. Williams WJ, Eldridge DJ (2011) Deposition of sand over a cyanobacterial soil crust increases nitrogen bioavailability in a semi-arid woodland. Appl Soil Ecol 49:26–31CrossRefGoogle Scholar
  143. Winkworth R (1967) The composition of several arid spinifex grasslands of central Australia in relation to rainfall, soil water relations, and nutrients. Aust J Bot 15:107–130CrossRefGoogle Scholar
  144. Witkowski ETF, Lamont BB (1996) Disproportionate allocation of mineral nutrients and carbon between vegetative and reproductive structures in Banksia hookeriana. Oecologia 105:38–42CrossRefPubMedGoogle Scholar
  145. 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 ML, 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 428:821–827CrossRefGoogle Scholar
  146. Zhang YM, Nie HL (2011) Effects of biological soil crusts on seedling growth and element uptake in five desert plants in Junggar Basin, western China. Chin J Plant Ecol 35:380–388CrossRefGoogle Scholar
  147. Zhang Y, Aradottir AL, Serpe M, Boeken B (2016) Interactions of biological soil crusts with vascular plants. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Springer, Dordrect, pp 385–406CrossRefGoogle Scholar
  148. Zhu YY, Yan F, Zorb C, Schubert S (2005) A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.) grown under phosphorus-deficient conditions? Plant Cell Physiol 46:892–901CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess PlateauNorthwest A&F UniversityYanglingChina
  2. 2.Schoolof Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  3. 3.School of Biological SciencesThe University of Western AustraliaCrawley (Perth)Australia

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