Plant and Soil

, Volume 334, Issue 1–2, pp 33–46

Does phosphate acquisition constrain legume persistence in the fynbos of the Cape Floristic Region?

  • Simon C. Power
  • Michael D. Cramer
  • G. Anthony Verboom
  • Samson B. M. Chimphango
Regular Article


Abundance of Fabaceae declines in representation through post-fire-succession in fynbos vegetation of the Cape Floristic Region (CFR). This reduction in legume occurrence coincides with a known decline in post-fire soil P availability. It was hypothesized that the disappearance of legume species during post-fire succession is due to an inability to acquire P effectively from sparingly soluble sources. P-acquisition strategies and response to P supply were compared between legume (Aspalathus, Cyclopia, Indigofera, Podalyria) and non-legume (Elegia, Leucadendron, Protea) genera when supplied with 1 or 10 mg P kg−1 dry sand. Each genus consisted of a seeder (non-persistent) and resprouter (persistent) species. Non-legumes showed a greater investment in below-ground biomass, more root clusters, with higher concentrations of carboxylates exuded by cluster roots and carboxylates that were better suited to the mobilization of sparingly soluble P compared to legumes. The growth response to increased P supply was 53% higher in legumes than in non-legumes. The lack of a growth response to an elevated P supply in the non-legumes was attributed to N-limitation. Legume resprouters had a higher investment in cluster-root biomass and a lower capacity to down-regulate P-uptake than the seeders. Therefore the inability to acquire sufficient P from low concentration and sparingly soluble soil P-sources may contribute to the lack of indigenous legume persistence in fynbos vegetation of the CFR.


Carboxylates Cluster roots Fabaceae Mycorrhizae Post-fire succession Regeneration strategy Resprouter Seeder 



Cape Floristic Region


  1. Allsopp N, Stock WD (1993) Mycorrhizal status of plants growing in the Cape Floristic Region, South Africa. Bothalia 23:91–104Google Scholar
  2. Bell DT (2001) Ecological response syndromes in the flora of Southwestern Western Australia: fire resprouters verse reseeders. Bot Rev 67:417–440CrossRefGoogle Scholar
  3. Bell DT, Koch JM (1980) Post-fire succession in the northern Jarrah forest of Western Australia. Aus J Ecol 5:9–14CrossRefGoogle Scholar
  4. Bellingham PJ, Sparrow AD (2000) Resprouting as a life history strategy in woody plant communities. Oikos 89:409–416CrossRefGoogle Scholar
  5. Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants-an economic analogy. Annu Rev Ecol Syst 16:363–392Google Scholar
  6. Bond WJ, Midgley JJ (2003) The evolutuionary ecology of sprouting in woody plants. Int J Plant Sci 164:103–114CrossRefGoogle Scholar
  7. Bond WJ, van Wilgen BW (1996) Fire and the evolutionary ecology of plants. In: Bond WJ, van Wilgen BW (eds) Fire and plants. Chapman and Hall, London, pp 123–147Google Scholar
  8. Boulet FM, Lambers H (2005) Characterisation of arbuscular mycorrhizal fungi colonisation in cluster roots of Hakea verrucosa F. Muell (Proteaceae), and its effect on growth and nutrient acquisition in ultamafic soil. Plant Soil 269:357–367CrossRefGoogle Scholar
  9. Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–45CrossRefGoogle Scholar
  10. Brouwer R (1983) Functional equilibrium: sense or nonsense? Neth J Agri Sci 31:335–348Google Scholar
  11. Brown G, Mitchell DT (1986) Influence of fire on the soil phosphorus status in sandplain lowland fynbos, south western Cape. S Afr J Bot 52:67–72Google Scholar
  12. Brundrett MC (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
  13. Cocks MP (1994) The ecology and nitrogen-fixing ability of selected Aspalathus spp. in fynbos ecosystems. Dissertation, University of Cape Town, South AfricaGoogle Scholar
  14. Cocks MP, Stock WD (2001) Field patterns of nodulation in fifteen Aspalathus species and their ecological role in the fynbos vegetation of southern Africa. Basic Appl Ecol 2:115–125CrossRefGoogle Scholar
  15. Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other cluster roots. Bot Acta 108:183–200Google Scholar
  16. Gardener WK, Barber DA, Parberry DG (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil 70:107–124CrossRefGoogle Scholar
  17. Gedroc JJ, McConnaughay KDM, Coleman JS (1996) Plasticity in root/shoot partitioning: optimal, ontogenetic or both? Funct Ecol 10:44–50CrossRefGoogle Scholar
  18. Gilbert GA, Knight JD, Vance CP, Allan DL (1999) Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant Cell Environ 22:801–810CrossRefGoogle Scholar
  19. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  20. Goldblatt P, Manning J (2000) Cape Plants: a conspectus of the Cape flora of South Africa. National Botanical Institute of South Africa, Pretoria and MGB Press, Missouri Botanical Gardens, St. Louis, USAGoogle Scholar
  21. Grierson PF, Comerford NB (2000) Non-destructive measurement of acid phosphatase activity in the rhizosphere using nitrocellulose membranes and image analysis. Plant Soil 218:49–57CrossRefGoogle Scholar
  22. Haaksma ED, Linder HP (2000) Restios of the fynbos. Botanical Society of South Africa, Cape TownGoogle Scholar
  23. Hansen A, Pate JS, Hansen AP (1991) Growth and reproductive performance of a seeder and resprouter species of Bossiaea as a function of plant age after fire. Ann Bot 67:497–509Google Scholar
  24. Hoffman MT, Mitchell DT (1986) The root morphology of some legume spp. in the south-western Cape and the relationship of vesicular-arbuscular mycorrhizas with dry mass and phosphorus content of Acacia saligna seedlings. S Afr J Bot 52:316–320Google Scholar
  25. Hoffmann MT, Moll EJ, Boucher C (1987) Post-fire succession at Pella, a South African lowland fynbos site. S Afr J Bot 53:370–374Google Scholar
  26. Jones DL (1998) Organic acids in the rhizosphere-a critical review. Plant Soil 205:25–44CrossRefGoogle Scholar
  27. Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behaviour in soils—misconceptions and knowledge gaps. Plant Soil 248:31–41CrossRefGoogle Scholar
  28. Kalra YP (1998) Handbook of standard methods of plant analysis. CRC Press, Boca RatonGoogle Scholar
  29. Keeley JE, Zedler PH (1978) Reproduction of chaparral shrubs after fire: a comparison of sprouting and seeding strategies. Am Midl Nat 99:142–160CrossRefGoogle Scholar
  30. Keerthisinghe G, Hocking PJ, Ryan PR, Delhaize E (1998) Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus). Plant Cell Environ 21:467–478CrossRefGoogle Scholar
  31. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect V-A mycorrhiza’s. Mycol Res 92:486–488CrossRefGoogle Scholar
  32. Kruger FJ (1979) Succession after fire in selected fynbos communities of the South-Western Cape. Dissertation, University of the Witwatersrand, Johannesburg, South AfricaGoogle Scholar
  33. Kruger FJ (1983) Plant community diversity and dynamics in relation to fire. In: Kruger FJ, Mitchell DT, Jarvus JUM (eds) Mediterranean-type ecosystems: role of nutrients. Ecological Studies 43. Springer, Berlin, pp 466–472Google Scholar
  34. Kruger FJ, Bigalke RC (1984) Fire in fynbos. In: Booysen P de V, Tainton NM (eds) Ecological effects of fire in South African ecosystems. Ecological studies 48. Springer, Berlin, pp 67–114Google Scholar
  35. Lambers H, Atkin OK, Millernaar FF (2002) Respiratory patterns in roots in relation to their functioning. In: Waisel Y, Eshel A, Kafkaki U (eds) Plant roots: the hidden half, 3rd edn. Marcel Dekker, New York, pp 521–552Google Scholar
  36. Lambers H, Cramer MD, Shane MW, Wouterlood M, Poot P, Veneklaas EJ (2003) Structure and functioning of cluster roots and plant responses to phosphate deficiency. Plant Soil 248:ix–xixCrossRefGoogle Scholar
  37. 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 98:693–713CrossRefPubMedGoogle Scholar
  38. Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. TREE 23:95–103PubMedGoogle Scholar
  39. Lamont B (1982) Mechanisms for enhancing nutrient uptake in plants, with particular reference to Mediterranean South Africa and Western Australia. Bot Rev 48:59–689CrossRefGoogle Scholar
  40. Lamont B (2003) Structure, ecology and physiology of cluster roots—a review. Plant Soil 248:1–19CrossRefGoogle Scholar
  41. Le Maitre DC (1992) The relative advantages of seedling and sprouting in fire-prone environments: a comparison of life histories of Protea neriifolia and Protea nitida. In: van Wilgen BW, Richardson DM, Kruger FJ, van Hensbergen HJ (eds) Fire in South African mountain fynbos. Ecosystem, community and species response at Swartboskloof. Springer-Verlag, Berlin, pp 122–144Google Scholar
  42. Le Maitre DC, Midgley JJ (1992) Plant reproductive ecology. In: Cowling RM (ed) The ecology of fynbos, nutrients, fire and diversity. Oxford University Press, Cape Town, pp 135–175Google Scholar
  43. Markham JH, Zedeveld C (2007) Nitrogen fixation makes biomass allocation to roots independent of soil nitrogen supply. Can J Bot 85:787–793CrossRefGoogle Scholar
  44. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102Google Scholar
  45. Marschner H, Horst RV, WJ MP (1987) Root induced changes of nutrient availability in the rhizosphere. J Plant Nutr 10:1175–1184CrossRefGoogle Scholar
  46. McConnaughay KDM, Coleman JS (1998) Can plants track changes in nutrient availability via changes in biomass partitioning? Plant Soil 202:201–209CrossRefGoogle Scholar
  47. McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants: ontogeny or optimality? Test along three resource gradients. Ecology 80:2581–2593CrossRefGoogle Scholar
  48. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phyto 115:495–501CrossRefGoogle Scholar
  49. Motomizu S, Wakimoto T, Toei K (1983) Spectrophotometric determination of phosphate in river waters with molybdate blue and malachite green. Analyst 108:361–367CrossRefGoogle Scholar
  50. Neumann G, Martinoia E (2002) Cluster roots-an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162–167CrossRefPubMedGoogle Scholar
  51. Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Römheld V, Martinoia E (2000) Physiological aspects of cluster root function and development in phosphorus-deficient White Lupin (Lupinus albus L.). Ann Bot 85:909–919CrossRefGoogle Scholar
  52. Pate JS, Froend RH, Bowen BJ, Hansen A, Kuo J (1990) Seedling and storage characterstics of seeder and resprouter species of Mediterranean-type ecosystems of S.W Australia. Ann Bot 65:585–601Google Scholar
  53. Purnell HM (1960) Studies of the family Proteaceae. I Anatomy and morphology of the roots of some Victorian species. Aust J Bot 8:38–50CrossRefGoogle Scholar
  54. Rebelo A (2001) Proteas: a field guide to the Proteas of Southern Africa. Fernwood, Cape TownGoogle Scholar
  55. Schutte AL, van Wyk BE, Vlok J (1995) Fire survival strategy-a character of taxonomic, ecological and evolutionary importance in fynbos legumes. Plant Syst Evol 195:243–259CrossRefGoogle Scholar
  56. Shane MW, Lambers H (2005) Mangenese accumulation in leaves of Hakea prostrata R. Br (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol Plant 274:441–450CrossRefGoogle Scholar
  57. Shane MW, Lambers H (2006) Systematic suppression of cluster-root formation and net P-uptake rates in Grevillea crithmifoliaat elevated P supply: a proteacean with resistance to for developing systems of ‘P toxicity’. J Exp Bot 57:413–423CrossRefPubMedGoogle Scholar
  58. Shane MW, De Vos M, De Roock S, Cawthray GR, Lambers H (2003a) Effects of external phosphorus supply on internal concentration, growth and exudation of cluster roots in Hakea prostrata R.Br. Plant Soil 248:209–219CrossRefGoogle Scholar
  59. Shane MW, De Vos M, De Roock S, Lambers H (2003b) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant Cell Environ 26:265–273CrossRefGoogle Scholar
  60. Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray G, Millar HA, Day DA, Lambers H (2004) Developmental physiology of cluster root carboxylate synthesis and exudation in Harsh Hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physio 135:549–560CrossRefGoogle Scholar
  61. Shane MW, Cramer MD, Lambers H (2008) Root of edaphically controlled Proteaceae turnover on the Agulhas Plain, South Africa: phosphate uptake regulation and growth. Plant Cell Environ 31:1825–1833CrossRefPubMedGoogle Scholar
  62. Shea SR, McCormick J, Portlock CC (1979) The effect of fires on regeneration of leguminous species in the northern jarrah (Eucalyptus marginata) forest of Western Australia. Aust J Ecol 4:195–205CrossRefGoogle Scholar
  63. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San DiegioGoogle Scholar
  64. Sokal RR, Rolhf FJ (1995) Biometry: the principles and practice of statistics in biological research. W.H Freeman and Co, San FransiscoGoogle Scholar
  65. Spriggs AC (2004) Symbiotic N2 fixation in cultivated Cyclopia Vent. Spp. (honeybush): towards sustainable cultivation in the Western Cape of South Africa. Dissertation, University of Cape Town, South AfricaGoogle Scholar
  66. Stock WD, Lewis OAM (1986) Soil nitrogen and the role of fire as a mineralizing agent in a South African coastal fynbos ecosystem. J Ecol 74:317–328CrossRefGoogle Scholar
  67. Vitousek PM, Field CB (1999) Ecosystems contraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46:179–202Google Scholar
  68. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  69. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rasetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(58):1–45CrossRefGoogle Scholar
  70. Watt M, Evans JR (2003) Phosphorus acquisition from soil by white lupin (Lupinus albus L.) and soybean (Glycine max L.), species with contrasting root development. Plant Soil 248:271–283CrossRefGoogle Scholar
  71. Westman WE (1981) Diversity relation and succession in California sage scrub. Ecology 62:170–184CrossRefGoogle Scholar
  72. Witkowski ETF (1991) Growth and competition between seedlings of Protea repens (L.) L. and the alien invasive Acacia saligna (Labill.) Wendl. in relation to nutrient availability. Funct Ecol 5:101–110CrossRefGoogle Scholar
  73. Witkowski ETF, Mitchell DT (1987) Variations in soil phosphorus in the fynbos biome, South Africa. J Ecol 75:1159–1171CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Simon C. Power
    • 1
  • Michael D. Cramer
    • 1
    • 2
  • G. Anthony Verboom
    • 1
  • Samson B. M. Chimphango
    • 1
  1. 1.Department of BotanyUniversity of Cape TownCape TownSouth Africa
  2. 2.School of Plant Biology, Faculty of Natural and Agricultural SciencesThe University of Western AustraliaPerthAustralia

Personalised recommendations