Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-28T05:15:01.720Z Has data issue: false hasContentIssue false

Traits associated with nutrient impoverishment and shade-tolerance in tree juveniles of three Bornean rain forests with contrasting nutrient availability

Published online by Cambridge University Press:  27 March 2015

Ryota Aoyagi*
Affiliation:
Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto, Japan606-8502
Kanehiro Kitayama
Affiliation:
Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto, Japan606-8502
*
1Corresponding author. Email: [email protected].

Abstract:

In this study, we tested the hypothesis that functional traits associated with nutrient impoverishment contribute to enhancing shade-tolerance (survival at low light) for the juveniles of canopy tree species in Bornean rain forests. To test the hypothesis, survival and functional traits (biomass allocation, leaf dynamics and foliar nutrient concentration) were investigated as a function of light conditions for saplings of 13 species in three forests with different levels of nutrient availability. As predicted by the hypothesis, the species in the severely nutrient-poor site (a tropical heath forest on nutrient-poor soils) showed greater shade-tolerance (>91% survival for 8 mo at 5% global site factor) than in the other two sites (mixed dipterocarp forests) (54–87% survival). Across the species, greater shade-tolerance was associated with a higher biomass allocation to roots, a slower leaf production and a higher foliar C concentration, which are considered as C-conservation traits under nutrient impoverishment. These results suggest that the juveniles of the canopy species occurring on nutrient-poor soils can enhance shade-tolerance by the same mechanisms as the adaptation to nutrient impoverishments. Tree species in nutrient-poor environments may be selected for surviving also in shaded conditions.

Type
Research Article
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

AGYEMAN, V. K., SWAINE, M. D. & THOMPSON, J. 1999. Responses of tropical forest tree seedlings to irradiance and the derivation of a light response index. Journal of Ecology 87:815827.CrossRefGoogle Scholar
AIBA, M. & NAKASHIZUKA, T. 2007. Variation in juvenile survival and related physiological traits among dipterocarp species co-existing in a Bornean forest. Journal of Vegetation Science 18:379388.CrossRefGoogle Scholar
BALTZER, J. L. & THOMAS, S. C. 2007. Determinants of whole-plant light requirements in Bornean rain forest tree saplings. Journal of Ecology 95:12081221.CrossRefGoogle Scholar
BARALOTO, C., GOLDBERG, D. E. & BONAL, D. 2005. Performance trade-offs among tropical tree seedlings in contrasting microhabitats. Ecology 86:24612472.CrossRefGoogle Scholar
BAZZAZ, F. A. 1979. The physiological ecology of plant succession. Annual Revew of Ecology and Systematics 10:351371.CrossRefGoogle Scholar
BLOOR, J. M. G. & GRUBB, P. J. 2003. Growth and mortality in high and low light: trends among 15 shade-tolerant tropical rain forest tree species. Journal of Ecology 91:7785.CrossRefGoogle Scholar
CANHAM, C. D., FINZI, A. C., PACALA, S. W. & BURBANK, D. H. 1994. Causes and consequences of resource heterogeneity in forests: interspecific variation in light transmission by canopy trees. Canadian Journal of Forest Research 24:337349.CrossRefGoogle Scholar
CANHAM, C. D., KOBE, R. K., LATTY, E. F. & CHAZDON, R. L. 1999. Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia 121:111.CrossRefGoogle ScholarPubMed
CHAPIN, F. S. 1980. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11:233260.CrossRefGoogle Scholar
CHUA, G. L. S., KOH, B. L., LAU, S., LEE, S. C., MATHIAS, M., TURNER, I. M. & YONG, J. W. H. 1995. The nutrient status of the plateau heath forest on Gunung Keriong, Pahang, Peninsular Malaysia. Journal of Tropical Forest Science 8:240246.Google Scholar
COOMES, D. & GRUBB, P. 2000. Impacts of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecological Monographs 70:171202.CrossRefGoogle Scholar
CRAINE, J. M. 2009. Resource strategies of wild plants. Princeton University Press, Princeton, pp. 149250.CrossRefGoogle Scholar
DENT, D. H. & BURSLEM, D. F. R. P. 2009. Performance trade-offs driven by morphological plasticity contribute to habitat specialization of Bornean tree species. Biotropica 41:424434.CrossRefGoogle Scholar
FINE, P. V. A., MESONES, I. & COLEY, P. D. 2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305:663665.CrossRefGoogle ScholarPubMed
FINE, P. V. A., MILLER, Z. J., MESONES, I., IRAZUZTA, S., APPEL, H. M., STEVENS, M. H. H., SÄÄKSJÄRVI, I., SCHULTZ, J. C. & COLEY, P. D. 2006. The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87:S150–62.CrossRefGoogle ScholarPubMed
GIVNISH, T. J. 1988. Adaptation to sun and shade. Australian Journal of Plant Physiology 15:6392.Google Scholar
IMAI, N., KITAYAMA, K. & TITIN, J. 2010. Distribution of phosphorus in an above-to-below-ground profile in a Bornean tropical rain forest. Journal of Tropical Ecology 26:627636.CrossRefGoogle Scholar
KITAJIMA, K. 1994. Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98:419428.CrossRefGoogle ScholarPubMed
KITAYAMA, K., NOREEN, M. L. & SHINICHIRO, A. 2000. Soil phosphorus fractionation and phosphorus-use efficiencies of tropical rainforests along altitudinal gradients of Mount Kinabalu, Borneo. Oecologia 123:342349.CrossRefGoogle ScholarPubMed
KOBE, R. K. 1997. Carbonhydrate allocation to storage as a basis of interspecific variation in sapling surivorship and growth. Oikos 80:226233.CrossRefGoogle Scholar
LUSK, C. H. 2002. Leaf area accumulation helps juvenile evergreen trees tolerate shade in a temperate rainforest. Oecologia 132:188196.CrossRefGoogle Scholar
LUSK, C. H. 2004. Leaf area and growth of juvenile temperate evergreens in low light: species of contrasting shade tolerance change rank during ontogeny. Functional Ecology 18:820828.CrossRefGoogle Scholar
MONTGOMERY, R. A. & CHAZDON, R. L. 2002. Light gradient partitioning by tropical tree seedlings in the absence of canopy gaps. Oecologia 131:165174.CrossRefGoogle ScholarPubMed
PALMIOTTO, P. A., DAVIES, S. J., VOGT, K. A., ASHTON, M. S., VOGT, D. J. & ASHTON, P. S. 2004. Soil-related habitat specialization in dipterocarp rain forest tree species in Borneo. Journal of Ecology 92:609623.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
POORTER, L. & KITAJIMA, K. 2007. Carbohydrate storage and light requirements of tropical moist and dry forest tree species. Ecology 88:10001011.CrossRefGoogle ScholarPubMed
REICH, P. B., WALTERS, M. B., ELLSWORTH, D. S. & UHL, C. 1994. Photosynthesis-nitrogen relations in Amazonian tree species. Oecologia 97:6272.CrossRefGoogle ScholarPubMed
RUSSO, S. E., BROWN, P., TAN, S. & DAVIES, S. J. 2007. Interspecific demographic trade-offs and soil-related habitat associations of tree species along resource gradients. Journal of Ecology 96:192203.CrossRefGoogle Scholar
SEINO, T., KITAYAMA, K. & LAKIM, M. B. 2007. Floristic composition and stand structure of the mixed dipterocarp forest in Tawau Hills Park, Sabah, Malaysia. Sabah Parks Nature Journal 8:6382.Google Scholar
STERNER, R. W. & ELSER, J. J. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton.Google Scholar
TILMAN, D. 1985. The resource-ratio hypothesis of plant succession. American Naturalist 125:827852.CrossRefGoogle Scholar
TURNER, I. M., LUCAS, P. W., BECKER, P., WONG, S. C., YONG, J. W. H. & CHOONG, M. F. 2000. Tree leaf form in Brunei: a heath forest and a mixed dipterocarp forest compared. Biotropica 32:5361.CrossRefGoogle Scholar
VALLADARES, F. & NIINEMETS, Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution, and Systematics 39:237257.CrossRefGoogle Scholar
VITOUSEK, P. M., PORDER, S., HOULTON, B. Z. & CHADWICK, O. A. 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications 20:515.CrossRefGoogle ScholarPubMed
WALKER, T. W. & SYERS, J. K. 1976. The fate of phosphorus during pedogenesis. Geoderma 15:119.CrossRefGoogle Scholar
WALTERS, M. B. & REICH, P. B. 1999. Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ? New Phytologist 143:143154.CrossRefGoogle Scholar
WRIGHT, S. J., MULLER-LANDAU, H. C., CONDIT, R. & HUBBELL, S. P. 2003. Gap-dependent recruitment, realized vital rates, and size distributions of tropical trees. Ecology 84:31743185.CrossRefGoogle Scholar