Skip to main content Accessibility help
Hostname: page-component-55b6f6c457-9lvz7 Total loading time: 0.289 Render date: 2021-09-28T08:36:07.056Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

Distribution of phosphorus in an above-to-below-ground profile in a Bornean tropical rain forest

Published online by Cambridge University Press:  11 October 2010

Nobuo Imai*
Graduate School of Agriculture, Kyoto University, Oiwake-cho, Kitashirakawa, Sakyo-ku, Kyoto 606–8502, Japan
Kanehiro Kitayama
Graduate School of Agriculture, Kyoto University, Oiwake-cho, Kitashirakawa, Sakyo-ku, Kyoto 606–8502, Japan
Jupiri Titin
Forest Research Centre, Sabah Forestry Department, 90715 Sandakan, Sabah, P.O. Box 1407, Malaysia
1Corresponding author. Email:


Ecosystem pool of phosphorus (P) was determined as the sum of above-ground vegetation, roots, necromass and soils to 1 m deep in a tropical rain forest in Sabah, Malaysia. Relationships among soil P fractions, acid phosphatase activity and fine-root biomass across soil horizons were also determined to understand P availability. Ecosystem pools of P, and of simultaneously quantified nitrogen (N) and carbon (C) were 3.4, 12 and 370 Mg ha−1, respectively. Only 2.6% of the total ecosystem P was in the above-ground vegetation, contrasting to C (60%) and N (16%). Canopy foliage of dominant tree species showed an extremely high N to P ratio of 31.5, which implied the excessively short supply of P compared with ample N. Soil P primarily consisted of recalcitrant occluded fractions (78–91%) and only 4% was labile. Approximately three-quarters of labile soil P was an organic fraction (Po). The concentration of labile Po did not differ between soil horizons, while both phosphatase activity and fine-root density were the greatest in the topsoil (top 5 cm) and dramatically decreased with depth. This suggests that trees depend on the acquisition of P from the labile Po in the topsoil, despite a greater amount of labile P in the subsoil. Trees with a high foliar N/P ratio may invest N to acquire P from the topsoil by secreting phosphatase that consists of proteins, rather than investing C to extending roots to scavenge P in the subsoil.

Research Article
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


AUGUSTO, L. & BERT, D. 2005. Estimating stemwood nutrient concentration with an increment borer: a potential source of error. Forestry 78:451455.CrossRefGoogle Scholar
BERTAULT, J.-G. & SIST, P. 1997. An experimental comparison of different harvesting intensities with reduced-impact and conventional logging in East Kalimantan, Indonesia. Forest Ecology and Management 94:209218.CrossRefGoogle Scholar
BURGHOUTS, T. B. A., VAN STRAALEN, N. M. & BRUIJNZEEL, L. A. 1998. Spatial heterogeneity of element and litter turnover in a Bornean rain forest. Journal of Tropical Ecology 14:477506.CrossRefGoogle Scholar
CHACÓN, N., DEZZEO, N., MUÑOZ, B. & RODRÍGUEZ, J. M. 2005. Implications of soil organic carbon and the biogeochemistry of iron and aluminum on soil phosphorus distribution in flooded forests of the lower Orinoco River, Venezuela. Biogeochemistry 73:555566.CrossRefGoogle Scholar
CREWS, T. E., KITAYAMA, K., FOWNES, J. H., RILEY, R. H., HERBERT, D. A., MUELLER-DOMBOIS, D. & VITOUSEK, P. M. 1995. Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:14071424.CrossRefGoogle Scholar
CROSS, A. F. & SCHLESINGER, W. H. 1995. A literature review and evaluation of the Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197214.CrossRefGoogle Scholar
FELDPAUSCH, T. R., RONDON, M. A., FERNANDES, E. C. M., RIHA, S. J. & WANDELLI, E. 2004. Carbon and nutrient accumulation in secondary forests regenerating on pastures in central Amazonia. Ecological Applications 14:S164S176.CrossRefGoogle Scholar
FRIZANO, J., JOHNSON, A. H., VANN, D. R. & SCATENA, F. N. 2002. Soil phosphorus fractionation during forest development on landslide scars in the Luquillo Mountains, Puerto Rico. Biotropica 34:1726.CrossRefGoogle Scholar
FRIZANO, J., VANN, D. R., JOHNSON, A. H., JOHNSON, C. M., VIEIRA, I. C. G. & ZARIN, D. J. 2003. Labile phosphorus in soils of forest fallows and primary forest in the Bragantina region, Brazil. Biotropica 35:211.Google Scholar
GARCIA-MONTIEL, D. C., NEILL, C., MELILLO, J., THOMAS, S., STEUDLER, P. A. & CERRI, C. C. 2000. Soil phosphorus transformations following forest clearing for pasture in the Brazilian Amazon. Soil Science Society of America Journal 64:17921804.CrossRefGoogle Scholar
HARMON, M. E., WHIGHAM, D. F. & SEXTON, J. 1995. Decomposition and mass of woody detritus in the dry tropical forest of the Northeastern Yucatan Peninsula, Mexico. Biotropica 27:305316.CrossRefGoogle Scholar
HEDIN, L. O. 2004. Global organization of terrestrial plant–nutrient interactions. Proceedings of the National Academy of Sciences USA 101:1084910850.CrossRefGoogle ScholarPubMed
HIDAKA, A. & KITAYAMA, K. 2009. Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen-use efficiency of tree leaves along nutrient-availability gradients. Journal of Ecology 97:984991.CrossRefGoogle Scholar
HIETZ, P., DUNISCH, O. & WANEK, W. 2010. Long-term trends in nitrogen isotope composition and nitrogen concentration in Brazilian rainforest trees suggest changes in nitrogen cycle. Environmental Science & Technology 44:11911196.CrossRefGoogle ScholarPubMed
HILLINGER, C., HÖLL, W. & ZIEGLER, H. 1996. Lipids and lipolytic enzymes in the trunkwood of Robinia pseudoacacia L. during heartwood formation. I. Radial distribution of lipid classes. Trees 10:366375.CrossRefGoogle Scholar
HÖLL, W. & LIPP, J. 1987. Concentration gradients of free sterols, steryl esters and lipid phosphorus in the trunkwood of Scots pine (Pinus sylvestris L.). Trees 1:7981.CrossRefGoogle Scholar
HOULTON, B. Z., WANG, Y.-P., VITOUSEK, P. M. & FIELD, C. B. 2008. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327330.CrossRefGoogle ScholarPubMed
HUGHES, R. F., KAUFFMAN, J. B. & JARAMILLO, V. J. 1999. Biomass, carbon, and nutrient dynamics of secondary forests in a humid tropical region of Mexico. Ecology 80:18921907.Google Scholar
ITOH, A., YAMAKURA, T., OHKUBO, T., KANZAKI, M., PALMIOTTO, P. A., LAFRANKIE, J. V., ASHTON, P. S. & LEE, H. S. 2003. Importance of topography and soil texture in the spatial distribution of two sympatric dipterocarp trees in a Bornean rainforest. Ecological Research 18:307320.CrossRefGoogle Scholar
JOHNSON, A. H., FRIZANO, J. & VANN, D. R. 2003. Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487499.CrossRefGoogle ScholarPubMed
JOHNSON, C. M., VIEIRA, I. C. G., ZARIN, D. J., FRIZANO, J. & JOHNSON, A. H. 2001. Carbon and nutrient storage in primary and secondary forests in eastern Amazonia. Forest Ecology and Management 147:245252.CrossRefGoogle Scholar
KAUFFMAN, J. B., CUMMINGS, D. L., WARD, D. E. & BABBITT, R. 1995. Fire in the Brazilian Amazon: 1. Biomass, nutrient pools, and losses in slashed primary forests. Oecologia 104:397408.CrossRefGoogle ScholarPubMed
KITAYAMA, K. & AIBA, S.-I. 2002. Ecosystem structure and productivity of tropical rain forests along altitudinal gradients with contrasting soil phosphorus pools on Mount Kinabalu, Borneo. Journal of Ecology 90:3751.CrossRefGoogle Scholar
KITAYAMA, K., MAJALAP-LEE, N. & AIBA, S.-I. 2000. Soil phosphorus fractionation and phosphorus-use efficiencies of tropical rainforests along altitudinal gradients of Mount Kinabalu, Borneo. Oecologia 123:342349.CrossRefGoogle ScholarPubMed
KITAYAMA, K., AIBA, S.-I., TAKYU, M., MAJALAP, N. & WAGAI, R. 2004. Soil phosphorus fractionation and phosphorus-use efficiency of a Bornean tropical montane rain forest during soil aging with podozolization. Ecosystems 7:259274.CrossRefGoogle Scholar
KLEINE, M. & HEUVELDOP, J. 1993. A management of planning concept for sustained yield of tropical forests in Sabah, Malaysia. Forest Ecology and Management 61:277297.CrossRefGoogle Scholar
LAURANCE, W. F. 2007. Forest destruction in tropical Asia. Current Science 93:15441550.Google Scholar
LAWRENCE, D. & SCHLESINGER, W. H. 2001. Changes in soil phosphorus during 200 years of shifting cultivation in Indonesia. Ecology 82:27692780.CrossRefGoogle Scholar
LAWRENCE, D., D'ODORICO, P., DIEKMANN, L., DELONGE, M., DAS, R. & EATON, J. 2007. Ecological feedbacks following deforestation create the potential for a catastrophic ecosystem shift in tropical dry forest. Proceedings of the National Academy of Sciences USA 104:2069620701.CrossRefGoogle ScholarPubMed
McGRODDY, M. E., DAUFRESNE, T. & HEDIN, L. O. 2004. Scaling of C:N:P stoichiometry in forests worldwide: Implications of terrestrial redfield-type ratios. Ecology 85:23902401.CrossRefGoogle Scholar
MURPHY, J. & RILEY, J. P. 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27:3136.CrossRefGoogle Scholar
NIIYAMA, K., KAJIMOTO, T., MATSUURA, Y., YAMASHITA, T., MATSUO, N., YASHIRO, Y., RIPIN, A., KASSIM, A. R. & NOOR, N. S. 2010. Estimation of root biomass based on excavation of individual root systems in a primary dipterocarp forest in Pasoh Forest Reserve, Peninsular Malaysia. Journal of Tropical Ecology 26:271284.CrossRefGoogle Scholar
NUSSBAUM, R., ANDERSON, J. & SPENCER, T. 1995. Factors limiting the growth of indigenous tree seedlings planted on degraded rainforest soils in Sabah, Malaysia. Forest Ecology and Management 74:149159.CrossRefGoogle Scholar
OGAWA, H. 1969. An attempt at classifying forest types based on the relationship between tree height and dbh. Pp. 3–17 in Kira, T. (ed.). Comparative study of primary productivity in forest ecosystems. JIBP-PT-F progress reports for 1968 (in Japanese).Google Scholar
OLANDER, L. P. & VITOUSEK, P. M. 2000. Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175190.CrossRefGoogle Scholar
OLANDER, L. P. & VITOUSEK, P. M. 2004. Biological and geochemical sinks for phosphorus in soil from a wet tropical forest. Ecosystems 7:404419.CrossRefGoogle Scholar
OLANDER, L. P., BUSTAMANTE, M. M., ASNER, G. P., TELLES, E., PRADO, Z. & CAMARGO, P. B. 2005. Surface soil changes following selective logging in an eastern Amazon forest. Earth Interactions 9:119.CrossRefGoogle Scholar
PAOLI, G. D. & CURRAN, L. M. 2007. Soil nutrients limit fine litter production and tree growth in mature lowland forest of southwestern Borneo. Ecosystems 10:503518.CrossRefGoogle Scholar
PIISPANEN, R. & SARANPÄÄ, P. 2002. Neutral lipids and phospholipids in Scots pine (Pinus sylvestris) sapwood and heartwood. Tree Physiology 22:661666.CrossRefGoogle ScholarPubMed
REICH, P. B. & OLEKSYN, J. 2004. Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of the National Academy of Sciences USA 101:1100111006.CrossRefGoogle ScholarPubMed
RODIN, L. E. & BAZILEVICH, N. I. 1967. Production and mineral cycling in terrestrial vegetation. Oliver and Boyd, Edinburgh. 288 pp.Google Scholar
STARK, N. M. & JORDAN, C. F. 1978. Nutrient retention by the root mat of an Amazonian rain forest. Ecology 59:434437.CrossRefGoogle Scholar
STEWART, J. W. B. & TIESSEN, H. 1987. Dynamics of soil organic phosphorus. Biogeochemistry 4:4160.CrossRefGoogle Scholar
TABATABAI, M. A. & BREMNER, J. M. 1969. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biology and Biochemistry 1:301307.CrossRefGoogle Scholar
TIESSEN, H. & MOIR, J. O. 1993. Characterization of available P by sequential extraction. Pp. 7586 in Carter, M. R. (ed.). Soil sampling and methods of analysis. Lewis Publishers, Boca Raton.Google Scholar
TIESSEN, H., CHACON, P. & CUEVAS, E. 1994. Phosphorus and nitrogen status in soils and vegetation along a toposequence of dystrophic rainforests on the upper Rio Negro. Oecologia 99:145150.CrossRefGoogle ScholarPubMed
TRESEDER, K. K. & VITOUSEK, P. M. 2001. Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946954.CrossRefGoogle Scholar
TURNBULL, T. L., WARREN, C. R. & ADAMS, M. A. 2007. Novel mannose-sequestration technique reveals variation in subcellular orthophosphate pools do not explain the effects of phosphorus nutrition on photosynthesis in Eucalyptus globulus seedlings. New Phytologist 176:849861.CrossRefGoogle Scholar
TURNER, B. L., CADE-MENUN, B. J. & WESTERMANN, D. T. 2003. Organic phosphorus composition and potential bioavailability in semi-arid arable soils of the Western United States. Soil Science Society of America Journal 67:11681179.CrossRefGoogle Scholar
VILLAR, R., ROBLETO, J. R., DE JONG, Y. & POORTER, H. 2006. Differences in construction costs and chemical composition between deciduous and evergreen woody species are small as compared to differences among families. Plant, Cell and Environment 29:16291643.CrossRefGoogle Scholar
VINCENT, A. G., TURNER, B. L. & TANNER, E. V. J. 2010. Soil organic phosphorus dynamics following perturbation of litter cycling in a tropical moist forest. European Journal of Soil Science 61:4857.CrossRefGoogle Scholar
VITOUSEK, P. M. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285298.CrossRefGoogle Scholar
WALKER, T. W. & SYERS, J. K. 1976. The fate of phosphorus during pedogenesis. Geoderma 15:119.CrossRefGoogle Scholar
WRIGHT, I. J., REICH, P. B., WESTOBY, M., ACKERLY, D. D., BARUCH, Z., BONGERS, F., CAVENDER-BARES, J., CHAPIN, T., CORNELLSSEN, J. H. C., DIEMER, M., FLEXAS, J., GARNIER, E., GROOM, P. K., GULIAS, J., HIKOSAKA, K., LAMONT, B. B., LEE, T., LEE, W., LUSK, C., MIDGLEY, J. J., NAVAS, M. -L., NIINEMETS, Ü., OLEKSYN, J., OSADA, H., POORTER, H., POOL, P., PRIOR, L., PYANKOV, V. I., ROUMET, C., THOMAS, S. C., TJOELKER, M. G., VENEKLAAS, E. J. & VILLAR, R. 2004. The worldwide leaf economics spectrum. Nature 428:821827.CrossRefGoogle ScholarPubMed
WRIGHT, I. J., REICH, P. B., CORNELISSEN, J. H. C., FALSTER, D. S., GARNIER, E., HIKOSAKA, K., LAMONT, B. B., LEE, W., OLEKSYN, J., OSADA, N., POORTER, H., VILLAR, R., WARTON, D. I. & WESTOBY, M. 2005. Assessing the generality of global leaf trait relationships. New Phytologist 166:485496.CrossRefGoogle ScholarPubMed
YAMAKURA, T., HAGIHARA, A., SUKARDJO, S. & OGAWA, H. 1986. Aboveground biomass of tropical rain forest stands in Indonesian Borneo. Vegetatio 68:7182.Google Scholar
YAMAKURA, T., KANZAKI, M., ITOH, A., OHKUBO, T., OGINO, K., CHAI, E. O. K., LEE, H. S. & ASHTON, P. S. 1995. Topography of a large-scale research plot established within the Lambir rain forest in Sarawak. Tropics 5:4156.CrossRefGoogle Scholar
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Distribution of phosphorus in an above-to-below-ground profile in a Bornean tropical rain forest
Available formats

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Distribution of phosphorus in an above-to-below-ground profile in a Bornean tropical rain forest
Available formats

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Distribution of phosphorus in an above-to-below-ground profile in a Bornean tropical rain forest
Available formats

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *