Skip to main content
SpringerLink
Log in

The ecology of very small-seeded shade-tolerant trees and shrubs in lowland rain forest in Singapore

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

A study was made in Bukit Timah Nature Reserve of niche differentiation among 11 woody species that have very small seeds (22–460 µg) and establish in deep shade, i.e., where the indirect site factor (isf) under cloudy conditions is ≤2%, and one taxonomically related light-demander (seed mass 33 µg). Comparative observations were made on changing light requirement with age. The species varied from shrubs and treelets (Urophyllum) via small to medium-height trees (Ficus, Pternandra) to tall trees (Gynotroches and Pellacalyx). In general, the shorter species fruited in deep shade while the taller needed direct irradiance. All produced ripe fruit at least once a year.

In 1–3% isf seedling mortality over 11 months was 24% for Urophyllum hirsutum and 57% for Pternandra echinata (two strongly shade-tolerant species); survivors produced appreciable new stem and leaf tissue. For two more light-demanding species (Ficus grossularioides and F. fistulosa) mean lamina area was much larger in small gaps (10% isf) than in the understorey (<3% isf), while for Urophyllum hirsutum it was much smaller. These three species showed the greatest difference in SLA. There were few significant intraspecific differences between gaps and understorey in concentrations of N, P or K. In a valley where there was no significant difference in isf between a path and adjacent understorey, seedlings of species with seeds <1 mg mean dry mass were five times as dense on transects along steep pathside banks as in the understorey 5 m upslope. The mean mid-bank slope was 66° (cf. 20° upslope). On mid-bank transects litter had a cover of 36% (cf. 95% upslope), and was thinner (0.8 vs 3.2 cm). The soil at 0–7 cm depth into the mid-bank had much lower concentrations of organic matter, total N and P (but not total K) and fine roots than that of upslope transects. All species were found to have vesicular-arbuscular mycorrhiza when 1–2 m tall in deep shade, several having very dense infections. Seedling form and responses are discussed in relation to potential adaptive value and possible evolutionary origin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alexander, I. 1989. Mycorrhizas in tropical forests. Pp. 169-188. In: Proctor, J. (ed.) Mineral Nutrients in Tropical Forest and Savanna Ecosystems. Blackwell, Oxford.

    Google Scholar 

  • Allsop, N. & Stock, W.D. 1992. Mycorrhizas, seed size and seedling establishment in a low nutrient environment. Pp. 59-64. In: Read, D. J., Lewis, D. H., Fitter, A. H. & Alexander, I. J. (eds.), Mycorrhizas in Ecosystems. CAB International, Wallingford.

    Google Scholar 

  • Anderson, M. C. 1964. Studies of the woodland light climate. I. The photographic computation of light conditions. J. Ecol. 52: 27-41.

    Google Scholar 

  • Anon. 1976. Geology of the Republic of Singapore. Public Works Department, Singapore.

    Google Scholar 

  • Anon. 1993. Bukit Timah Nature Reserve. National Parks Board, Singapore.

    Google Scholar 

  • Baylis, G. T. S. 1975. The magnolioid mycorrhiza and mycotrophy in root systems derived from it. Pp. 373-389. In: Sanders, F. E., Mosse, B. & Tinker, P. B. (eds), Endomycorrhiza. Academic Press, London.

    Google Scholar 

  • Bazzaz, F. A. & Pickett, S. T. A. 1980. Physiological ecology of tropical succession: a comparative review. Ann. Rev. Ecol. Syst. 11: 287-311.

    Article  Google Scholar 

  • Bongers, F. & Popma, J. 1988. Is exposure-related variation in leaf characteristics of tropical rain forest species adaptive? Pp. 191-200. In: Werger, M. J. A, Van der Aart, P. J.M., During, H. J. & Verhoeven, J. T. A. (eds), Plant Form and Vegetation Structure. S.P.B. Academic Publishing, The Hague.

    Google Scholar 

  • Brundrett, M. 1991. Mycorrhizas in natural ecosystems. Adv. Ecol. Res. 21: 171-313.

    Google Scholar 

  • Coley, P. D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol. Monog. 53: 209-233.

    Google Scholar 

  • Coomes, D. A. & Grubb, P. J. In press. Responses of juveniles to above-and below-ground competition in nutrient-starved Amazonain rainforest. Ecology 79.

  • Corlett, R. T. 1988. Bukit Timah: the history and significance of a small rain-forest reserve. Env. Conser. 17: 37-44.

    Google Scholar 

  • Corlett, R. T. 1990. Flora and reproductive phenology of the rain forest at Bukit Timah, Singapore. J. Trop. Ecol. 6: 55-63.

    Google Scholar 

  • Corlett, R. T. 1994. What is secondary forest? J. Trop. Ecol. 10: 445-447.

    Google Scholar 

  • Denslow, J. S., Schultz, J. C., Vitousek, P. M. & Strain, B. R. 1990 Growth responses of tropical shrubs to treefall gap environments. Ecology 71: 165-179.

    Google Scholar 

  • Ellison, A. M., Denslow, J. S., Loiselle, B. A. & Bren&#x00E9;es M., D. 1993. Seed and seedling ecology of neotropical Melastomataceae. Ecology 74: 1733-1749.

    Google Scholar 

  • Evans, G. C., Whitmore, T. C. & Wong, Y. K. 1960. The distribution of light reaching the ground vegetation in a tropical rain forest. J. Ecol. 48: 193-204.

    Google Scholar 

  • Field, C. & Mooney, H. A. 1986. The photosynthesis-nitrogen relationship in wild plants. Pp. 25-55. In: Givnish T. J. (ed.), On the Economy of Plant Form and Function. Cambridge University Press, Cambridge.

    Google Scholar 

  • Floyd, A. G. 1990. Australian Rainforest in New South Wales, Vol. 1. Surrey Beatty, Chipping Norton, N.S.W.

    Google Scholar 

  • Foster, S. A. & Janson, C. H. 1985. The relationship between seed size and establishment conditions in tropical woody plants. Ecology 66: 773-780.

    Google Scholar 

  • Freeden, A. L., Griffin, K. & Field, C. B. 1991. Effects of light quantity and quality and soil nitrogen status on nitrate reductase activity in rainforest species of the genus Piper. Oecologia 86: 441-446.

    Google Scholar 

  • Grubb, P. J. 1977a. The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol. Rev. 52: 107-145.

    Article  Google Scholar 

  • Grubb, P. J. 1977b. Control of forest growth and distribution on wet tropical mountains: with special reference to mineral nutrition. Ann. Rev. of Ecol. Syst. 8: 83-107.

    Article  Google Scholar 

  • Grubb, P. J. 1996. Rainforest dynamics: the need for new paradigms. Pp. 215-233. In: Edwards, D. S., Booth, W. E. & Choy, S. C. (eds), Tropical Rainforest Research: Current Issues. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Grubb, P. J. 1998. Seeds and fruits of tropical rainforest plants: interpretation of the range in seed size, degree of defence and flesh/seed quotients. Pp. 1-24. In: Newbery, D. M., Prins, H. & Brown, N. D. (eds), Dynamics of Tropicical Communities. Symposia of the British Ecological Society 37.

  • Grubb, P. J. & Coomes, D. A. 1997. Seed mass and nutrient content in nutrient-starved tropical rainforest in Venezuela. Seed Sci. Res. 7: 269-280.

    Google Scholar 

  • Grubb, P. J., Lee, W. G., Kollmann, J. & Wilson, J. B. 1996. Interaction of irradiance and soil nutrient supply on growth of seedlings on ten European tall-shrub species and Fagus sylvatica. J. of Ecol. 84: 827-840.

    Google Scholar 

  • Grubb, P. J. & Metcalfe, P. J. 1996. Adaptation and inertia in theAustralian tropical lowland rain-forest flora: contradictory trends in intergeneric and intrageneric comparisons of seed size in relation to light demand. Functional Ecol. 10: 512-520.

    Google Scholar 

  • Grubb, P. J., Turner, I. M. & Burslem, D. F. R. P. 1994. Mineral nutrient status of coastal hill dipterocarp forest and adinandra belukar in Singapore: analysis of soil, leaves and litter. J. Trop. Ecol. 10: 559-577.

    Google Scholar 

  • Hill, R. D. 1972. Soil moisture under forest, Bukit Timah Nature Reserve, Singapore. Garden’s Bulletin, Singapore 26: 85-93.

    Google Scholar 

  • Hubbell, S. P. & Foster, R. B. 1986. Canopy gaps and the dynamics of neotropical forest. Pp. 73-96. In: Crawley, M. J. (ed.) Plant Ecology. Blackwell, Oxford.

    Google Scholar 

  • Janos, D. P. 1980. Mycorrhizae influence tropical succession. Biotropica Suppl. 12: 56-64.

    Google Scholar 

  • Kennedy, D. N. 1991. The role of colonising species in the regeneration of dipterocarp rain forest. PhD Thesis, University of Aberdeen.

  • Kiew, R. 1988. Herbaceous flowering plants. Pp. 56-76. In: Cranbrook, Earl of (ed.) Malaysia. Pergamon Press, Oxford.

    Google Scholar 

  • Kohyama, T. 1987. Significance of architecture and allometry in saplings. Funct. Ecology 1: 399-404.

    Google Scholar 

  • Kohyama, T. & Grubb, P. J. 1994. Below-and above-ground allometries of shade-tolerant seedlings in a Japanese warm-temperate rain forest. Funct. Ecol. 8: 229-236.

    Google Scholar 

  • Kormanik, P. P. & McGraw, A.-C. 1982. Quantification of vesiculararbuscular mycorrhizae in plant roots. Pp. 37-45. In: Schenck, N. C. (ed.), Methods and Principles in Mycorrhizal Research. The American Phytopathological Society, St Paul, Minnesota.

    Google Scholar 

  • Latham, R. E. 1992. Co-occurring tree species change rank in seedling performance with resources varied experimentally. Ecology 73: 2129-2144.

    Google Scholar 

  • Loach, K. 1970. Shade tolerance in tree seedlings. II. Growth analysis of plants raised under artificial shade. New Phytol. 69: 273-286.

    Google Scholar 

  • Louis, I. & Lim, G. 1987. Spore density and root colonization of vesicular-arbuscular mycorrhizas in tropical soil. Trans. Brit. Mycol. Soc. 88: 207-212.

    Google Scholar 

  • Metcalfe, D. J. 1996. Germination of small-seeded tropical rain forest plants exposed to different spectral compositions. Can. J. Bot. 74: 516-520.

    Google Scholar 

  • Metcalfe, D. J. & Grubb, P. J. 1995. Seedmass and light requirements for regeneration in Southeast Asian rain forest. Can. J. of Bot. 73: 817-826.

    Google Scholar 

  • Metcalfe, D. J. & Grubb, P. J. 1997. The responses to shade of seedlings of very small-seeded tree and shrub species from tropical rain forest in Singapore. Funct. Ecol. 11: 215-221.

    Google Scholar 

  • Metcalfe, D. J. & Turner, I. M. Soil seed bank from lowland rain forest in Singapore: canopy-gap and litter-gap demanders. J. Trop. Ecol., submitted.

  • Molofsky, J. & Augspurger, C. K. 1992. The effect of leaf litter on early seedling establishment in a tropical forest. Ecology 73: 68-77.

    Google Scholar 

  • Newton, A. C. & Healey, J. R. 1989. Establishment of Clethra occidentalison stems of the tree-fern Cyathea pubescensin a Jamaican montane rain forest. J. Trop. Ecol. 5: 441-445.

    Google Scholar 

  • Ng, F. S. P. (ed) 1978. Tree Flora of Malaya, Vol. 3. Longman, Kuala Lumpur.

    Google Scholar 

  • Ng, F. S. P. 1980. Germination ecology of Malaysian woody plants. Malaysian Forester 43: 406-437.

    Google Scholar 

  • Ng, F. S. P. (ed) 1989. Tree Flora ofMalaya, Vol. 4. Longman, Kuala Lumpur.

    Google Scholar 

  • Osunkoya, O. O., Ash, J. E., Hopkins, M. S. & Graham, A. W. 1994. Influence of seed size and seedling ecological attributes on shade-tolerance of rain-forest tree species in northern Queensland. J. Ecol. 82: 149-163.

    Google Scholar 

  • Phillips, J. M. & Hayman, D. S. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Brit. Mycol. Soc. 55: 158-161.

    Google Scholar 

  • Primack, R. B. 1992. Tropical community dynamics and conservation biology. BioScience 42: 818-821.

    Google Scholar 

  • Putz, F. E. & Appanah, S. 1987. Buried seeds, newly dispersed seeds, and the dynamics of a lowland forest in Malaysia. Biotropica 19: 326-333.

    Google Scholar 

  • Rabinowitz, D. 1981. Seven forms of rarity. Pp. 205-217. In: Synge, H. (ed.) The Biological Aspects of Rare Plant Conservation. John Wiley & Sons, Chichester.

    Google Scholar 

  • Raich, J. W. & Gong, W. K. 1990. Effects of canopy openings on tree seed germination in a Malaysian dipterocarp forest. J. Trop. Ecol. 6: 203-217.

    Google Scholar 

  • Read, J. & Hill, R. S. 1985. Photosynthetic responses to light of Australian and Chilean species of Nothofagusand their relevance to the rainforest dynamics. New Phytol. 101: 731-742.

    Google Scholar 

  • Reich, P. B., Walters, M. B. & Ellsworth, D. S. 1992. Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol. Monog. 62: 365-392.

    Google Scholar 

  • St John, T. V. 1980. Root size, root hairs and mycorrhizal infection: a re-examination of Baylis’s hypothesis with tropical trees. New Phytol. 84: 483-487.

    Google Scholar 

  • Sim, J. W. S., Tan, H. T. W., & Turner, I. M. 1992. Adinandra belukar: an anthropogenic heath forest in Singapore. Vegetatio 102: 125-137.

    Google Scholar 

  • Smits, W. T. M. 1992. Mycorrhizal studies in dipterocarp forests in Indonesia. Pp. 283-292. In: Read, D. J., Lewis, D. H., Fitter, A. H. & Alexander, I. J. (eds) Mycorrhizas in Ecosystems. CAB International, Wallingford.

    Google Scholar 

  • Stiles, F. G. & Roselli, L. 1993. Consumption of fruits of the Melastomataceae by birds; how diffuse is coevolution? Vegetatio 107/108: 57-73.

    Google Scholar 

  • Swaine, M. D. & Whitmore, T. C. 1988. On the definition of ecological species groups in tropical rain forests. Vegetatio 75: 81-86.

    Google Scholar 

  • Tan, H. T.W., Chua, K. S. & Turner, I.M. 1995. Rubiaceae of Bukit Timah Nature Reserve. Pp. 29-61. In: Chin, S. C., Corlett, R. T., Wee, Y. C. & Gee, S. Y. (eds.) Garden’s Bulletin Singapore Supplement No. 3.

  • Tsel’niker, Y. L. 1977. Regulation of processes of CO2 exchange and morphogenesis in seedlings of forest trees under conditions of shading. Soviet Plant Physiol. 24: 43-48.

  • Turner, I.M. 1993. The names used for Singapore plants since 1900. Garden’s Bulletin, Singapore 45: 1-287.

    Google Scholar 

  • Turner, I. M. 1994. A quantitative analysis of leaf form in woodyplants from the world’s major broadleaved forest types. J. Biog. 21: 413-419.

    Google Scholar 

  • Wayne, P. M. & Bazzaz, F. A. 1993. Birch seedling responses to daily time courses of light in experimental forest gaps and shadehouses. Ecology 74: 1500-1515.

    Google Scholar 

  • Wong, K. M. 1989. Rubiaceae. Pp. 324-425. In: Ng, F. S. P. (ed.) Tree Flora of Malaya Volume 4. Longman, Kuala Lumpur.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, UK

    Daniel J. Metcalfe & Peter J. Grubb

  2. School of Biological Sciences, National, University of Singapore, Lower Kent Ridge Road, Singapore, 119260

    I. M. Turner

Authors
  1. Daniel J. Metcalfe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter J. Grubb
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. M. Turner
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Metcalfe, D.J., Grubb, P.J. & Turner, I.M. The ecology of very small-seeded shade-tolerant trees and shrubs in lowland rain forest in Singapore. Plant Ecology 134, 131–149 (1998). https://doi.org/10.1023/A:1009789922595

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1009789922595

Search

Navigation