Plant and Soil

, Volume 341, Issue 1–2, pp 295–307 | Cite as

Nitrogen and phosphorus retranslocation and N:P ratios of litterfall in three tropical plantations: luxurious N and efficient P use by Acacia mangium

  • Masahiro InagakiEmail author
  • Koichi Kamo
  • Kazuki Miyamoto
  • Jupiri Titin
  • Lenim Jamalung
  • Jaffirin Lapongan
  • Satoru Miura
Regular Article


Some tropical N2-fixing trees exhibit specific characteristics for phosphorus (P) acquisition and utilisation that contrast with the large nitrogen (N) fluxes in their litterfall. To investigate differences in N and P cycling in N2-fixing plantations, litterfall and fresh leaf quality of a N2-fixing Acacia mangium plantation were compared with that of a non-N2-fixing Swietenia macrophylla plantation and a coniferous Araucaria cunninghamii plantation. The N concentration in the A. mangium litterfall was higher than that in the litterfall of the two other species, whereas the P concentration in the A. mangium leaf litterfall was 0.16 mg g–1, which was only 12–22% of that of the other species. The P concentration in the reproductive parts of A. mangium was markedly higher (16.1 mg g–1) than those in the other fractions. The N:P ratio was higher in the leaf fall (81) compared to the fresh leaves (29) of A. mangium, in contrast to the N:P ratios in the leaf samples of the other two species. An analysis of a global litterfall dataset of tropical plantations indicated that N:P ratios in litterfall were significantly higher in N2-fixers than in non-N2-fixers, and those of A. mangium were high among species in the N2-fixer group. These results indicated that A. mangium efficiently retranslocated P in contrast to very large N cycling, under field conditions. These differences may be related to other physiological characteristics of A. mangium.


Litter quality Leguminous tree Nutrient demand Resorption N-to-P ratio 



Nutrient-use efficiency


Ratio of element concentration leaf litterfall to that in fresh leaves


Inductively coupled plasma atomic emission spectrometry


Standardised major axis



We thank Dr. K.V. Sankaran for access to his original litterfall dataset (published in Binkley et al. 1997). We thank staff of the Sabah Forest Research Centre for assistance with litterfall sampling and Mss. Jalimah Badin, Liza Minsuan and Petronella Anthony for sample treatment. We also thank Dr. Yoshiyuki Inagaki for his valuable advice on the model II regression and resorption, and Drs. Shinji Kaneko and Junko Nagakura for their valuable comments on an earlier draft of this manuscript. This study was carried out as a part of an international cooperative research project between the Sabah Forestry Department and the Japan International Research Center for Agricultural Sciences and was funded by the Ministry of Agriculture, Forestry and Fisheries of Japan, “Development of Agroforestry Technology for the Rehabilitation of Tropical Forests.”

Supplementary material

11104_2010_644_MOESM1_ESM.xls (58 kb)
Appendix 1 List of nutrient fluxes through litterfall in tropical plantations (XLS 57.5 kb)


  1. Aggangan NS, Moon HK, Han SH (2010) Growth response of Acacia mangium Willd. Seedlings to arbuscular mycorrhizal fungi and four isolates of the ectomycorrhizal fungus Pisolithus tinctorius (Pers.) Coker and Couch. New For 39:215–230Google Scholar
  2. Arai S, Ishizuka S, Ohta S, Ansori S, Tokuchi N, Tanaka N, Hardjono A (2008) Potential N2O emissions from leguminous tree plantation soils in the humid tropics. Glob Biogeochem Cycles 22:GB2028CrossRefGoogle Scholar
  3. Binkley D, Dunkin KA, DeBell D, Ryan MG (1992) Production and nutrient cycling in mixed plantations of Eucalyptus and Albizia in Hawaii. For Sci 35:393–408Google Scholar
  4. Binkley D, O’connell AM, Sankaran KV (1997) Stand development and productivity. In: Nambiar EKS, Brown AG (eds) Management of soil, nutrients and water in tropical plantation forests. ACIAR, Canberra, pp 419–442Google Scholar
  5. Binkley D, Giardina C, Bashkin MA (2000) Soil phosphorus pools and supply under the influence of Eucalyptus saligna and nitrogen-fixing Albizia falcataria. For Ecol Manage 128:241–247CrossRefGoogle Scholar
  6. Björck M (2002) Analysis of foliar nutrients in predicting productivity of Acacia mangium forest plantations in Sabah, Malaysia. MSc Dissertation, Department of Forest Ecology, Swedish University of Agricultural SciencesGoogle Scholar
  7. Bouillet JP, Laclau JP, Gonçalves JLM, Moreira MZ, Trivelin PCO, Jourdan C, Silva EV, Piccolo MC, Tsai SM, Galiana A (2008) Mixed-species plantations of Acacia mangium and Eucalyptus grandis in Brazil 2: nitrogen accumulation in the stands and biological N2 fixation. For Ecol Manage 255:3918–3930CrossRefGoogle Scholar
  8. Brasell HM, Unwin GL, Stocker GC (1980) The quantity, temporal distribution and mineral-element content of litterfall in two forest types at two sites in tropical Australia. J Ecol 68:123–139CrossRefGoogle Scholar
  9. Bubb KA, Xu ZH, Simpson JA, Saffigna PG (1998) Some nutrient dynamics associated with litterfall and litter decomposition in hoop pine plantations of southeast Queensland, Australia. For Ecol Manage 110:343–352CrossRefGoogle Scholar
  10. Chapin FS III, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, New YorkGoogle Scholar
  11. Cuevas E, Lugo AE (1998) Dynamics of organic matter and nutrient return from litterfall in stands of ten tropical tree plantation species. For Ecol Manage 112:263–279CrossRefGoogle Scholar
  12. Dent DH, Bagchi R, Robinson D, Majalap-Lee N, Burslem DFRP (2006) Nutrient fluxes via litterfall and leaf litter decomposition vary across a gradient of soil nutrient supply in a lowland tropical rain forest. Plant Soil 228:197–215CrossRefGoogle Scholar
  13. Falster DS, Warton DI, Write IJ (2006) SMATR: standardized major axis tests and routines. Version 2.0.
  14. Fife DN, Nambiar EKS, Saur E (2008) Retranslocation of foliar nutrients in evergreen tree species planted in a Mediterranean environment. Tree Physiol 28:187–196PubMedGoogle Scholar
  15. Forrester DI, Bauhus J, Cowie AL, Vanclay JK (2006) Mixed-species plantations of Eucalyptus with nitrogen-fixing trees: a review. For Ecol Manage 233:211–230CrossRefGoogle Scholar
  16. Gentili F, Huss-Danell K (2003) Local and systematic effects of phosphorus and nitrogen on nodulation and nodule function in Alnus incana. J Exp Bot 54:2757–2767CrossRefPubMedGoogle Scholar
  17. Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266CrossRefGoogle Scholar
  18. Güsewell S, Gessner MO (2009) N: P rations influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219CrossRefGoogle Scholar
  19. Hardiyanto EB, Wicaksono A (2008) Inter-rotation site management, stand growth and soil properties in Acacia mangium plantations in south Sumatra, Indonesia. In: Nambiar SEK (ed) Site management and productivity in tropical plantation forests: proceedings of workshops in Piracicaba (Brazil) 22–26 November 2004 and Bogor (Indonesia) 6–9 November 2006. CIFOR, Jakarta, pp 107–122Google Scholar
  20. Hättenschwiler S, Aeschlimann B, Coûteaux M-M, Roy J, Bonal D (2008) High variation in foliage and leaf litter chemistry among 45 tree species of a Neotropical rainforest community. New Phytol 179:165–175CrossRefPubMedGoogle Scholar
  21. Hikosaka K, Osone Y (2009) A paradox of leaf-trait convergence: why is leaf nitrogen concentration higher in species with higher photosynthetic capacity? J Plant Res 122:245–251CrossRefPubMedGoogle Scholar
  22. Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330CrossRefPubMedGoogle Scholar
  23. Inagaki M, Titin J (2009) Evaluation of site environments for agroforestry production. In: Gotoh T, Yokota Y (eds) Development of agroforestry technology for the rehabilitation of tropical forests JIRCAS working report 60. JIRCAS, Tsukuba, pp 26–31Google Scholar
  24. Inagaki M, Kamo K, Yamada T, Titin J (2008) Soil water conditions according to landscape position and aboveground vegetation in an Acacia mangium plantation in Sabah, Malaysia. JARQ, Jpn Agric Res Q 42:69–76Google Scholar
  25. Inagaki M, Inagaki Y, Kamo K, Titin J (2009) Fine-root production in response to nutrient application at three forest plantations in Sabah, Malaysia: higher nitrogen and phosphorus demand by Acacia Mangium. J For Res 14:178–182CrossRefGoogle Scholar
  26. Inagaki M, Kamo K, Titin J, Jamalung L, Lapongan J, Miura S (2010) Nutrient dynamics through fine litterfall in three plantations in Sabah, Malaysia, in relation to nutrient supply to surface soil. Nutr Cycl Agroecosyst 88:381–395CrossRefGoogle Scholar
  27. Isaac SR, Nair MA (2006) Litter dynamics of six multipurpose trees in a homegarden in Southern Kerala, India. Agrofor Syst 67:203–213CrossRefGoogle Scholar
  28. IUSS Working Group WRB (2007) World reference base for soil resources 2006, first update 2007. World soil resources reports no. 103. FAO, RomeGoogle Scholar
  29. Jamaludheen V, Kumar BM (1999) Litter of multipurpose trees in Kerala, India: variations in the amount, quality, decay rates and release of nutrients. For Ecol Manage 115:1–11CrossRefGoogle Scholar
  30. Kadir WR, Van Cleemput O, Zaharah AR (1998) Nutrient retranslocations during the early growth of two exotic plantation species. In: Schulte A, Ruhiyat D (eds) Soils of tropical forest ecosystems: characteristics, ecology and management. Springer, Berlin, pp 132–136Google Scholar
  31. Kerkhoff AJ, Enquist BJ, Elser JJ, Fagan WF (2005) Plant allometry, stoichiometry and the temperature-dependence of primary productivity. Glob Ecol Biogeogr 14:585–598CrossRefGoogle Scholar
  32. Kerkhoff AJ, Fagan WF, Elser JJ, Enquist BJ (2006) Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. Am Nat 168:103–122CrossRefGoogle Scholar
  33. Khanna PK (1998) Nutrient cycling under mixed-species tree systems in southeast Asia. Agrofor Syst 38:99–120CrossRefGoogle Scholar
  34. Kimaro AA, Timmer VR, Mugasha AG, Chamshama SAO, Kimaro DA (2007) Nutrient use efficiency and biomass production of tree species for rotational woodlot systems in semi-arid Morogoro, Tanzania. Agrofor Syst 71:175–184CrossRefGoogle Scholar
  35. Kojima K (2004) Environmental stress responses of tropical trees. J Jpn For Soc 86:61–68 (In Japanese with English summary)Google Scholar
  36. Kunhamu TK, Kumar BM, Viswanath S (2009) Does thinning affect litterfall, litter decomposition, and associated nutrient release in Acacia mangium stands of Kerala in peninsular India? Can J For Res 39:792–801CrossRefGoogle Scholar
  37. Lee YK, Lee DK, Woo SY, Park PS, Jang YH, Abraham ERG (2006) Effect of Acacia plantations on net photosynthesis, tree species composition, soil enzyme activities, and microclimate on Mt. Makiling. Photosynthetica 44:299–308CrossRefGoogle Scholar
  38. Lisanework N, Michelsen A (1994) Litterfall and nutrient release by decomposition in three plantations compared with a natural forest in the Ethiopian highland. For Ecol Manage 65:149–164CrossRefGoogle Scholar
  39. Lugo AE (1992) Comparison of tropical tree plantations with secondary forests of similar age. Ecol Monogr 62:1–41CrossRefGoogle Scholar
  40. Majalap N (1999) Effects of Acacia mangium on soils in Sabah. Dissertation, Department of Plant and Soil Science, The University of AberdeenGoogle Scholar
  41. Majid NM, Alias MA, Paudyal BK (1998) Foliar sampling guidelines for different aged Acacia mangium plantations in Peninsular Malaysia. J Trop For Sci 10:431–437Google Scholar
  42. Martínez-Sánchez JL (2005) Nitrogen and phosphorus resorption in a Neotropical rain forest of a nutrient-rich soil. Rev Biol Trop 53:353–359PubMedGoogle Scholar
  43. Maruyama Y, Toma T, Ishida A, Matsumoto Y, Morikawa Y, Ang LH, Yap SK, Iwasa M (1997) Photosynthesis and water use efficiency of 19 tropical tree species. J Trop For Sci 9:434–438Google Scholar
  44. McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial Redfield-type ratios. Ecology 85:2390–2401CrossRefGoogle Scholar
  45. McKey D (1994) Legumes and nitrogen: the evolutionary ecology of a nitrogen-demanding lifestyle. In: Sprent JL, McKey D (eds) Advance in legume systematics, part 5: the nitrogen factor. Royal Botanic Gardens, Kew, pp 221–228Google Scholar
  46. National Climatic Data Center (2009) Global historical climatology network data base, version 2. Cited 9 Oct 2009
  47. Nguyen NT, Mohapatra PK, Fujita K (2006) Elevated CO2 alleviates the effects of low P on the growth of N2 fixing Acacia auricuriformis and Acacia mangium. Plant Soil 285:369–379CrossRefGoogle Scholar
  48. Ostertag R (2010) Foliar nitrogen and phosphorus accumulation responses after fertilization: an example from nutrient-limited Hawaiian forests. Plant Soil 334:85–98CrossRefGoogle Scholar
  49. Osunkoya OO, Othman FE, Kahar RS (2005) Growth and competition between seedlings of an invasive plantation tree, Acacia mangium, and those of a native Borneo heath-forest species, Melastoma beccarianum. Ecol Res 20:205–214CrossRefGoogle Scholar
  50. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006CrossRefPubMedGoogle Scholar
  51. Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160:207–212CrossRefPubMedGoogle Scholar
  52. Ribet J, Drevon JJ (1996) The phosphorus requirement of N2-fixing and urea-fed Acacia mangium. New Phytol 132:383–390CrossRefGoogle Scholar
  53. Richardson SJ, Allen RB, Doherty JE (2008) Shifts in Leaf N: P ratio during resorption reflect soil P in temperate rainforest. Funct Ecol 22:738–745CrossRefGoogle Scholar
  54. Sá TDA, De Oliveira VC, De Araújo AC, Junior SB (1999) Spectral irradiance and stomatal conductance of enriched fallows with fast-growing trees in eastern Amazonia, Brazil. Agrofor Syst 47:289–303CrossRefGoogle Scholar
  55. Swamy HR, Proctor J (1997) Fine litterfall and its nutrients in plantations of Acacia auriculiformis, Eucalyptus tereticornis and Tectona grandis in the Chikmagalur district of the western Ghats, India. J Trop For Sci 10:73–85Google Scholar
  56. Tobita H, Uemura A, Kitao M, Kitaoka S, Utsugi H (2010) Interactive effects of elevated CO2, phosphorus deficiency, and soil drought on nodulation and nitrogenase activity in Alnus hirsuta and Alnus maximowiczii. Symbiosis 50:59–69CrossRefGoogle Scholar
  57. Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N:P ratios in tropical rain forest. Ecology 88:107–118CrossRefPubMedGoogle Scholar
  58. Vadez V, Lim G, Durand P, Diem HG (1995) Comparative growth and symbiotic performance of four Acacia mangium provenances from Papua New Guinea in response to the supply of phosphorus at various concentrations. Biol Fertil Soils 19:60–64CrossRefGoogle Scholar
  59. van Heerwaarden LM, Toet S, Aerts R (2003) Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos 101:664–669CrossRefGoogle Scholar
  60. Vitousek P (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119:553–572CrossRefGoogle Scholar
  61. Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167CrossRefGoogle Scholar
  62. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(58):1–45CrossRefGoogle Scholar
  63. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291CrossRefPubMedGoogle Scholar
  64. Xuluc-Tolosa FJ, Vester HFM, Ramírez-Marcial N, Castellanos-Albores J, Lawrence D (2003) Leaf litter decomposition of tree species in three successional phases of tropical dry secondary forest in Campeche, Mexico. For Ecol Manage 174:401–412CrossRefGoogle Scholar
  65. Yuan Z, Chen HYH (2009a) Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Glob Ecol Biogeogr 18:11–18CrossRefGoogle Scholar
  66. Yuan Z, Chen HYH (2009b) Global trends in senesced-leaf nitrogen and phosphorus. Glob Ecol Biogeogr 18:532–542CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Masahiro Inagaki
    • 1
    Email author
  • Koichi Kamo
    • 2
  • Kazuki Miyamoto
    • 3
  • Jupiri Titin
    • 4
  • Lenim Jamalung
    • 4
  • Jaffirin Lapongan
    • 4
  • Satoru Miura
    • 1
  1. 1.Department of Forest Site EnvironmentForestry and Forest Products Research InstituteTsukubaJapan
  2. 2.Forest Science and Technology InstituteTsukubaJapan
  3. 3.Shikoku Research CenterForestry and Forest Products Research InstituteKochiJapan
  4. 4.Forest Research CentreSandakanMalaysia

Personalised recommendations