Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-22T18:02:47.945Z Has data issue: false hasContentIssue false
  • English
  • Français

Physiological linkage in co-variation of foliar nitrogen and phosphorus in tropical tree species along a gradient of soil phosphorus availability

Published online by Cambridge University Press:  17 April 2015

Amane Hidaka  and
Kanehiro Kitayama
Amane Hidaka*
Affiliation:
Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan
Kanehiro Kitayama
Affiliation:
Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan
*
1Corresponding author. Current address: Network Center of Forest and Grassland Survey in Monitoring Sites 1000 Project, Japan Wildlife Research Center, c/o Tomakomai Research Station, Field Science Center for Northern Biosphere, Hokkaido University, Tomakomai, Hokkaido 053-0035, Japan. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

In order to understand the stoichiometric balance between foliar nitrogen (N) and phosphorus (P) on P-poor soils, we investigated how foliar N and P attributes (i.e. N and P concentrations in green and senesced leaves, N and P resorption efficiencies) of 30 tropical tree species co-vary along a gradient of soil P availability across three forests on Mount Kinabalu, Borneo. We found strong and positive correlations between foliar N and P in the concentrations and resorption efficiencies within each forest and across the three forests. Slopes of standardized major axis between foliar N and P concentrations for both green and senesced leaves were not different among the three forests, although the values of the scaling exponent in the relationships of foliar N to P across the three forests were significantly lower than 1. We suggest that down-regulation of N concentrations in green leaves on P-poor soils is one of several possible mechanisms explaining why N concentrations decrease with decreasing P concentrations in both green and senesced leaves toward a lower P availability in soils. On the other hand, the physiological and ecological reasons why N and P resorption efficiencies are positively correlated with each other across tree species remain unclear.

Keywords

leaf traitslitternitrogennutrient limitationphosphorusresorptionstoichiometrytropical montane rain forest
Type
Research Article
Information
Journal of Tropical Ecology , Volume 31 , Issue 3 , May 2015 , pp. 221 - 229
Copyright
Copyright © Cambridge University Press 2015 

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.)

References

LITERATURE CITED

AERTS, R. 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? Journal of Ecology 84:597–608.CrossRefGoogle Scholar
AERTS, R. & CHAPIN, F. S. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30:1–67.Google Scholar
ÅGREN, G. I. 2008. Stoichiometry and nutrition of plant growth in natural communities. Annual Review of Ecology, Evolution, and Systematics 39:153–170.CrossRefGoogle Scholar
CAI, Z. & BONGERS, F. 2007. Contrasting nitrogen and phosphorus resorption efficiencies in trees and lianas from a tropical montane rain forest in Xishuangbanna, south-west China. Journal of Tropical Ecology 23:115–118.CrossRefGoogle Scholar
CERNUSAK, L. A., WINTER, K. & TURNER, B. L. 2010. Leaf nitrogen to phosphorus ratios of tropical trees: experimental assessment of physiological and environmental controls. New Phytologist 185:770–779.CrossRefGoogle ScholarPubMed
CHAPIN, F. S., MATSON, P. A. & VITOUSEK, P. M. 2011. Principles of terrestrial ecosystem ecology. (Second edition). Springer, New York. 350 pp.CrossRefGoogle Scholar
CLEVELAND, C. C., TOWNSEND, A. R., TAYLOR, P., ALVAREZ-CLARE, S., BUSTAMANTE, M. M. C., CHUYONG, G., DOBROWSKI, S. Z., GRIERSON, P., HARMS, K. E., HOULTON, B. Z., MARKLEIN, A., PARTON, W., PORDER, S., REED, S. C., SIERRA, C. A., SILVER, W. L., TANNER, E. V. J. & WIEDER, W. R. 2011. Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecology Letters 14:939–947.CrossRefGoogle ScholarPubMed
COLEY, P. D., BRYANT, J. P. & CHAPIN, F. S. 1985. Resource availability and plant anti-herbivore defense. Science 230:895–899.CrossRefGoogle Scholar
CORDELL, S., GOLDSTEIN, G., MEINZER, F. C. & VITOUSEK, P. M. 2001. Regulation of leaf life-span and nutrient-use efficiency of Metrosideros polymorpha trees at two extremes of a long chronosequence in Hawaii. Oecologia 127:198–206.CrossRefGoogle ScholarPubMed
ELSER, J. J., BRACKEN, M. E. S., CLELAND, E. E., GRUNER, D. S., HARPOLE, W. S., HILLEBRAND, H., NAGI, J. T., SEABLOOM, E. W., SHURIN, J. B. & SMITH, J. E. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10:1135–1142.CrossRefGoogle ScholarPubMed
ENDARA, M.-J. & COLEY, P. D. 2011. The resource availability hypothesis revisited: a meta-analysis. Functional Ecology 25:389–398.CrossRefGoogle Scholar
GÜSEWELL, S. 2005. Nutrient resorption of wetland graminoids is related to the type of nutrient limitation. Functional Ecology 19:344–354.CrossRefGoogle Scholar
HALL, S. J., ASNER, G. P. & KITAYAMA, K. 2004. Substrate, climate, and land use controls over soil N dynamics and N-oxide emissions in Borneo. Biogeochemistry 70:27–58.CrossRefGoogle Scholar
HARPOLE, W. S., NGAI, J. T., CLELAND, E. E., SEABLOOM, E. W., BORER, E. T., BRACKEN, M. E. S., ELSER, J. J., GRUNER, D. S., HILLEBRAND, H., SHURIN, J. B. & SMITH, J. E. 2011. Nutrient co-limitation of primary producer communities. Ecology Letters 14:852–862.CrossRefGoogle ScholarPubMed
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 Phytologist 179:165–175.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 97:984–991.CrossRefGoogle Scholar
HIDAKA, A. & KITAYAMA, K. 2011. Allocation of foliar phosphorus fractions and leaf traits of tropical tree species in response to decreased soil phosphorus availability on Mount Kinabalu, Borneo. Journal of Ecology 99:849–857.CrossRefGoogle Scholar
KERKHOFF, A. J., FAGAN, W. F., ELSER, J. J. & ENQUIST, B. J. 2006. Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. American Naturalist 168:E103–E122.CrossRefGoogle ScholarPubMed
KILLINGBECK, K. T. 1996. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727.CrossRefGoogle Scholar
KITAYAMA, K. 1992. An altitudinal transect study of the vegetation on Mount Kinabalu, Borneo. Vegetatio 102:149–171.CrossRefGoogle Scholar
KITAYAMA, K. & AIBA, S. 2002. Ecosystem structure and productivity of tropical rain forests along altitudinal gradients with contrasting soil phosphorus pools on Mount Kinabalu, Borneo. Journal of Ecology 90:37–51.CrossRefGoogle Scholar
KITAYAMA, K., AIBA, S., MAJALAP, N. & OHSAWA, M. 1998. Soil nitrogen mineralization rates of rainforests in a matrix of elevations and geological substrates on Mount Kinabalu, Borneo. Ecological Research 13:301–312.CrossRefGoogle Scholar
KITAYAMA, K., AIBA, S., 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 podzolization. Ecosystems 7:259–274.CrossRefGoogle Scholar
KOBE, R. K., LEPCZYK, C. A. & IYER, M. 2005. Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86:2780–2792.CrossRefGoogle Scholar
LAL, C. B., ANNAPURNA, C., RAGHUBANSHI, A. S. & SINGH, J. S. 2001. Effect of leaf habit and soil type on nutrient resorption and conservation in woody species of a dry tropical environment. Canadian Journal of Botany 79:1066–1075.CrossRefGoogle Scholar
MARSCHNER, H. 1995. Mineral nutrition of higher plants. (Second edition). Academic Press, London. 889 pp.Google Scholar
MATZEK, V. & VITOUSEK, P. M. 2009. N:P stoichiometry and protein:RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecology Letters 12:765–771.CrossRefGoogle ScholarPubMed
MAYOR, J. R., WRIGHT, S. J. & TURNER, B. L. 2014. Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forests. Journal of Ecology 102:36–44.CrossRefGoogle Scholar
NIKLAS, K. J., OWENS, T., REICH, P. B. & COBB, E. D. 2005. Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecology Letters 8:636–642.CrossRefGoogle Scholar
OSTERTAG, R. 2010. Foliar nitrogen and phosphorus accumulation responses after fertilization: an example from nutrient-limited Hawaiian forests. Plant and Soil 334:85–98.CrossRefGoogle Scholar
QUESADA, C. A., LLOYD, J., SCHWARZ, M., PATINO, S., BAKER, T. R., CZIMCZIK, C., FYLLAS, N. M., MARTINELLI, L., NARDOTO, G. B., SCHMERLER, J., SANTOS, A. J. B., HODNETT, M. G., HERRERA, R., LUIZÃO, F. J., ARNETH, A., LLOYD, G., DEZZEO, N., HILKE, I., KUHLMANN, I., RAESSLER, M., BRAND, W. A., GEILMANN, H., MORAES FILHO, J. O., CARVALHO, F. P., ARAUJO FILHO, R. N., CHAVES, J. E., CRUZ JUNIOR, O. F., PIMENTEL, T. P. & PAIVA, R. 2010. Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7:1515–1541.CrossRefGoogle Scholar
REED, S. C., TOWNSEND, A. R., DAVIDSON, E. A. & CLEVELAND, C. C. 2012. Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytologist 196:173–180.CrossRefGoogle ScholarPubMed
REICH, P. B., OLEKSYN, J. & WRIGHT, I. J. 2009. Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160:207–212.CrossRefGoogle ScholarPubMed
REICH, P. B., OLEKSYN, J., WRIGHT, I. J., NIKLAS, K. J., HEDIN, L. & ELSER, J. J. 2010. Evidence of a general 2/3-power law of scaling leaf nitrogen to phosphorus among major plant groups and biomes. Proceeding of the Royal Society of London. Series B: Biological Sciences 277:877–883.Google ScholarPubMed
TAKYU, M., AIBA, S. & KITAYAMA, K. 2002. Effects of topography on tropical lower montane forests under different geological conditions on Mount Kinabalu, Borneo. Plant Ecology 159:35–49.CrossRefGoogle Scholar
TAKYU, M., AIBA, S. & KITAYAMA, K. 2003. Changes in biomass, productivity and decomposition along topographical gradients under different geological conditions in tropical lower montane forests on Mount Kinabalu, Borneo. Oecologia 134:397–404.CrossRefGoogle ScholarPubMed
TOWNSEND, A. R., CLEVELAND, C. C., ASNER, G. P. & BUSTAMANTE, M. M. C. 2007. Controls over foliar N:P ratios in tropical rain forests. Ecology 88:107–118.CrossRefGoogle ScholarPubMed
TRESEDER, K. K. & VITOUSEK, P. M. 2001. Potential ecosystem-level effects of genetic variation among populations of Metrosideros polymorpha from a soil fertility gradient in Hawaii. Oecologia 126:266–275.CrossRefGoogle ScholarPubMed
TULLY, K. L., WOOD, T. E., SCHWANTES, A. M. & LAWRENCE, D. 2013. Soil nutrient availability and reproductive effort drive patterns in nutrient resorption in Pentaclethra macroloba. Ecology 93:930–940.CrossRefGoogle Scholar
VENEKLAAS, E. J., LAMBERS, H., BRAGG, J., FINNEGAN, P. M., LOVELOCK, C. E., PLAXTON, W. C., PRICE, C. A., SCHEIBLE, W.-R., SHANE, M. W., WHITE, P. J. & RAVEN, J. A. 2012. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195:306–320.CrossRefGoogle ScholarPubMed
VERGUTZ, L., MANZONI, S., PORPORATO, A., NOVAI, R. F. & JACKSON, R. B. 2012. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecological Monographs 82:205–220.CrossRefGoogle Scholar
VITOUSEK, P. M. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298.CrossRefGoogle Scholar
WARTON, D. I., DUURSMA, R. A., FALSTER, D. S. & TASKINEN, S. 2012. smatr 3 – an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3:257–259.CrossRefGoogle Scholar
WRIGHT, I. J. & WESTOBY, M. 2003. Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Functional Ecology 17:10–19.CrossRefGoogle Scholar
WRIGHT, I. J., REICH, P. B., WESTOBY, M., ACKERLY, D. D., BARUCH, Z., BONGERS, F., CAVENDER-BARES, J., CHAPIN, F. S., CORNELISSEN, 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, N., POORTER, H., POOT, P., PRIOR, L., PYANKOV, V. I., ROUMET, C., THOMAS, S. C., TJOELKER, M. G., VENEKLAAS, E. & VILLAR, R. 2004. The world-wide leaf economics spectrum. Nature 428:821–827.CrossRefGoogle Scholar
YUAN, Z.Y. & CHEN, H. Y. H. 2009. Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Global Ecology and Biogeography 18:11–18.CrossRefGoogle Scholar