Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T05:37:39.518Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential growth responses in seedlings of ten species of Dipterocarpaceae to experimental shading and defoliation

Published online by Cambridge University Press:  01 June 2012

C. E. Timothy Paine ,
Martin Stenflo ,
Christopher D. Philipson ,
Philippe Saner ,
Robert Bagchi ,
Robert C. Ong  and
Andy Hector
C. E. Timothy Paine*
Affiliation:
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057, Zurich, Switzerland
Martin Stenflo
Affiliation:
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057, Zurich, Switzerland
Christopher D. Philipson
Affiliation:
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057, Zurich, Switzerland
Philippe Saner
Affiliation:
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057, Zurich, Switzerland
Robert Bagchi
Affiliation:
Department of Biological and Biomedical Science, University of Durham, Durham DH1 3LE, UK
Robert C. Ong
Affiliation:
Sabah Forestry Department, Forest Research Centre, Forestry Department Sabah, Sandakan, Sabah, Malaysia
Andy Hector
Affiliation:
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057, Zurich, Switzerland
*
1Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

The responses of plants to shade and foliar herbivory jointly affect growth rates and community assembly. We grew 600 seedlings of ten species of the economically important Dipterocarpaceae in experimental gradients of shading (0.3–47.0% of full sunlight) and defoliation (0, 25%, 50% or 75% of leaf area removed). We assessed stem diameters initially, after 2 and 4 mo, and calculated relative growth rates (RGR) with a linear model. Shading interacted with defoliation, reducing RGR by 21.6% in shaded conditions and 8.9% in well-lit conditions. We tested three hypotheses for interspecific trade-offs in growth responses to shading and defoliation. They could be positively related, because both reduce a plant's access to carbon, or inversely related because of trade-offs between herbivore resistance and tolerance. We observed, however, that species varied in their response to shading, but not defoliation, precluding an interspecific trade-off and suggesting that plants tolerate shade and herbivory with differing strategies. Shading most strongly reduced the growth of species with less-dense wood and larger seeds. The strong and variable growth responses to shade, contrasted with the weak and uniform responses to defoliation, suggest that variation in light availability more strongly affects the growth of tropical tree seedlings, and thus community assembly, than does variation in herbivory.

Keywords

allocation trade-offsdefenceDipterocarpaceaeherbivoryrelative growth rateSabahshade tolerance
Type
Research Article
Information
Journal of Tropical Ecology , Volume 28 , Issue 4 , July 2012 , pp. 377 - 384
Copyright
Copyright © Cambridge University Press 2012

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

ASHTON, P. S. 1982. Flora Malesiana—Dipterocarpaceae. Martinus Nijhoff/Dr. W. Junk, Dordrecht. 552 pp.Google Scholar
BARAZA, E., GÓMEZ, J. M., HÓDAR, J. A. & ZAMORA, R. 2004. Herbivory has a greater impact in shade than in sun: response of Quercus pyrenaica seedlings to multifactorial environmental variation. Canadian Journal of Botany 82:357–364.CrossRefGoogle Scholar
BEBBER, D., BROWN, N. & SPEIGHT, M. 2002. Drought and root herbivory in understorey Parashorea Kurz (Dipterocarpaceae) seedlings in Borneo. Journal of Tropical Ecology 18:795–804.Google Scholar
BECKER, P. 1983. Effects of insect herbivory and artificial defoliation on survival of Shorea seedlings. Pp. 241–252 in Sutton, S. L., Whitmore, T. C. & Chadwick, A. C. (eds.). Tropical rainforest: ecology and management. Blackwell Scientific Publications, Oxford.Google Scholar
BLUNDELL, A. G. & PEART, D. R. 2001. Growth strategies of a shade-tolerant tropical tree: the interactive effects of canopy gaps and simulated herbivory. Journal of Ecology 89:608–615.Google Scholar
CHAMBERLAIN, T. C. 1880. The method of multiple working hypotheses. Science 15:92–96.Google Scholar
CHAVE, J., COOMES, D. A., JANSEN, S., LEWIS, S. L., SWENSON, N. G. & ZANNE, A. E. 2009. Towards a worldwide wood economics spectrum. Ecology Letters 12:351–366.Google Scholar
COLEY, P. D. & BARONE, J. A. 1996. Herbivory and plant defenses in tropical forests. Annual Review of Ecology, Evolution, and Systematics 27:305–335.Google Scholar
COLEY, P., BRYANT, J. & CHAPIN, F. 1985. Resource availability and plant antiherbivore defense. Science 230:895–899.Google Scholar
DUDLEY, S. A. & SCHMITT, J. 1996. Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. American Naturalist 147:445–465.CrossRefGoogle Scholar
EICHHORN, M. P., COMPTON, S. G. & HARTLEY, S. E. 2006. Seedling species determines rates of leaf herbivory in a Malaysian rain forest. Journal of Tropical Ecology 22:513.Google Scholar
EICHHORN, M. P., NILUS, R., COMPTON, S. G., HARTLEY, S. E. & BURSLEM, D. F. R. P. 2010. Herbivory of tropical rain forest tree seedlings correlates with future mortality. Ecology 91:1092–1101.Google Scholar
FINE, P. V. A., MESONES, I. & COLEY, P. D. 2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305:663–665.CrossRefGoogle ScholarPubMed
GRIME, J. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111:1169–1194.Google Scholar
HECTOR, A., PHILIPSON, C. D., SANER, P., CHAMAGNE, J., DZULKIFLI, D., O'BRIEN, M., SNADDON, J. L., ULOK, P., WEILENMANN, M., REYNOLDS, G. & GODFRAY, H. C. J. 2011. The Sabah Biodiversity Experiment: a long-term test of the role of tree diversity in restoring tropical forest structure and functioning. Philosophical Transactions of the Royal Society of London Series B – Biological Sciences 366:3303–3315.Google Scholar
HOWE, H. F. 1990. Survival and growth of juvenile Virola surinamensis in Panama: effects of herbivory and canopy closure. Journal of Tropical Ecology 6:259–280.CrossRefGoogle Scholar
KITAJIMA, K. 1994. Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98:419–428.Google Scholar
KOBE, R. 1997. Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos 80:226–233.CrossRefGoogle Scholar
LANDIS, R. M. & PEART, D. R. 2005. Early performance predicts canopy attainment across life histories in subalpine forest trees. Ecology 86:63–72.CrossRefGoogle Scholar
LEIMU, R. & KORICHEVA, J. 2006. A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies. Oikos 112:1–9.Google Scholar
LENTZ, K. A. & CIPOLLINI, D. F. 1998. Effect of light and simulated herbivory on growth of endangered northeastern bulrush, Scirpus ancistrochaetus Schuyler. Plant Ecology 139:125–131.CrossRefGoogle Scholar
LOUDA, S. M. & RODMAN, J. E. 1996. Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine cordifolia A. Gray, Bittercress). Journal of Ecology 84:229.Google Scholar
MASCHINSKI, J. & WHITHAM, T. G. 1989. The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing. American Naturalist 134:1–19.Google Scholar
MEIJER, W. & WOOD, G. H. S. 1964. Dipterocarps of Sabah. Forest Department, Sandakan. 344 pp.Google Scholar
MONTGOMERY, R. A. & CHAZDON, R. L. 2002. Light gradient partitioning by tropical tree seedlings in the absence of canopy gaps. Oecologia 131:165–174.Google Scholar
MYERS, J. A. & KITAJIMA, K. 2007. Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. Journal of Ecology 95:383–395.CrossRefGoogle Scholar
NEWMAN, M. F., BURGESS, P. F. & WHITMORE, T. C. 1996. Borneo Island light hardwoods. Royal Botanical Garden Edinburgh, Edinburgh. 275 pp.Google Scholar
NEWMAN, M. F., BURGESS, P. F. & WHITMORE, T. C. 1998. Borneo island medium and heavy hardwoods. Royal Botanical Garden Edinburgh, Edinburgh. 228 pp.Google Scholar
NÚÑEZ-FARFÁN, J., FORNONI, J. & VALVERDE, P. L. 2007. The evolution of resistance and tolerance to herbivores. Annual Review of Ecology, Evolution, and Systematics 38:541–566.Google Scholar
PAINE, C. E. T., MARTHEWS, T. R., VOGT, D. R., PURVES, D. W., REES, M., HECTOR, A. & TURNBULL, L. A. 2012. How to fit nonlinear plant growth models and calculate growth rates: an update for ecologists. Methods in Ecology and Evolution 3:245–256.CrossRefGoogle Scholar
PEARSON, T. R. H., BURSLEM, D. F. R. P., GOERIZ, R. E. & DALLING, J. W. 2003. Interactions of gap size and herbivory on establishment, growth and survival of three species of neotropical pioneer trees. Journal of Ecology 91:785–796.CrossRefGoogle Scholar
PHILIPSON, C. D., SANER, P., MARTHEWS, T. R., NILUS, R., REYNOLDS, G., TURNBULL, L. A. & HECTOR, A. in press. Light-based regeneration niches: evidence from 21 dipterocarp species using size-specific RGRs. Biotropica.Google Scholar
POORTER, L., WRIGHT, S. J., PAZ, H., ACKERLY, D. D., CONDIT, R., IBARRA-MANRIQUEZ, G., HARMS, K. E., LICONA, J. C., MARTÍNEZ-RAMOS, M., MAZER, S. J., MULLER-LANDAU, H. C., PEÑA-CLAROS, M., WEBB, C. O. & WRIGHT, I. J. 2008. Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. Ecology 89:1908–1920.Google Scholar
ROGERS, W. E. & SIEMANN, E. 2002. Effects of simulated herbivory and resource availability on native and invasive exotic tree seedlings. Basic and Applied Ecology 3:297–307.CrossRefGoogle Scholar
SALGADO-LUARTE, C. & GIANOLI, E. 2010. Herbivory on temperate rainforest seedlings in sun and shade: resistance, tolerance and habitat distribution. PloS ONE 5:e11460.Google Scholar
SANER, P. G. 2009. Ecosystem carbon dynamics in logged forest of Malaysian Borneo. Ph.D. dissertation, Universität Zürich. 217 pp.Google Scholar
SANER, P., PHILIPSON, C. D., ONG, R. C., MAJALAP, N., EGLI, S. & HECTOR, A. 2010. Positive effects of ectomycorrhizal colonization on growth of seedlings of a tropical tree across a range of forest floor light conditions. Plant and Soil 338:411–421.CrossRefGoogle Scholar
SANER, P., LOH, Y. Y., ONG, R. C. & HECTOR, A. 2012. Carbon stocks and fluxes in tropical lowland dipterocarp rainforests in Sabah, Malaysian Borneo. PloS ONE 7:e29642.Google Scholar
SHIPLEY, B., LECHOWICZ, M. J., WRIGHT, I. J. & REICH, P. B. 2006. Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87:535–541.Google Scholar
STRAUSS, S. Y. & AGRAWAL, A. A. 1999. The ecology and evolution of plant tolerance to herbivory. Trends in Ecology and Evolution 14:179–185.CrossRefGoogle ScholarPubMed
TURNBULL, L., PHILIPSON, C., PURVES, D., ATKINSON, R., CUNNIFF, J., GOODENOUGH, A., HAUTIER, Y., HOUGHTON, J., MARTHEWS, T. R., OSBORNE, C. P., PAUL-VICTOR, C., ROSE, K. E., SANER, P., TAYLOR, S. H., WOODWARD, F. I., HECTOR, A. & REES, M. (in press). Plant growth rates and seed size: a re-evaluation. Ecology.Google Scholar
VALLADARES, F. & NIINEMETS, Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution, and Systematics 39:237–257.Google Scholar
WARTON, D. I., DUURSMA, R. A., FALSTER, D. S. & TASKINEN, S. in press. smatr 3- an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution.Google Scholar
ZANGERL, A. R., HAMILTON, J. G., MILLER, T. J., CROFTS, A. R., OXBOROUGH, K., BERENBAUM, M. R. & DE LUCIA, E. H. 2002. Impact of folivory on photosynthesis is greater than the sum of its holes. Proceedings of the National Academy of Sciences USA 99:1088–1091.Google Scholar
ZUIDEMA, P. A., BRIENEN, R. J. W., DURING, H. J. & GÜNERALP, B. 2009. Do persistently fast-growing juveniles contribute disproportionately to population growth? A new analysis tool for matrix models and its application to rainforest trees. American Naturalist 174:709–719.Google Scholar