Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T04:57:26.679Z Has data issue: false hasContentIssue false
  • English
  • Français

Biotic and abiotic drivers of dipterocarp seedling survival following mast fruiting in Malaysian Borneo

Published online by Cambridge University Press:  16 December 2014

Chiaki Oshima ,
Yuji Tokumoto  and
Michiko Nakagawa
Chiaki Oshima
Affiliation:
Faculty of Agriculture, Nagoya University, Chikusa, Nagoya, 464-8601Japan
Yuji Tokumoto
Affiliation:
Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601Japan
Michiko Nakagawa*
Affiliation:
Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601Japan
*
1Corresponding author. Email: miko@agr.nagoya-u.ac.jp
Get access Rights & Permissions [Opens in a new window]

Abstract:

South-East Asian tropical rain forests experience sporadic, but profuse, seed production after general flowering, leading to the synchronous emergence of various seedlings and subsequent seedling dynamics, which play a crucial role in determining species distribution and coexistence. We examined the relative importance of both biotic (initial height, conspecific seedling density) and abiotic (canopy openness, per cent sand, soil water content) drivers using survival data for 1842 seedlings of 12 dipterocarp species for 1.5 y following mast fruiting in an old-growth Bornean tropical rain forest. More than 30% of all dipterocarp seedlings survived 1.5 y after mast fruiting. When all species were analysed together, we found that initial seedling height, canopy openness and conspecific seedling density affected dipterocarp seedling survival. Negative density dependence indicated that predators were not satiated, but dipterocarp seedlings rather suffered from host-specific natural enemies or intraspecific competition. Species-level analyses of seven dipterocarp species showed large variation in response to biotic and abiotic factors. These results suggest that interspecific differences in the relative importance of biotic and abiotic effects on seedling survival might contribute to species coexistence.

Keywords

density dependenceDipterocarpaceaeJanzen-Connell hypothesisLambirmastingpredator satiation hypothesisseedling recruitment
Type
Research Article
Information
Journal of Tropical Ecology , Volume 31 , Issue 2 , March 2015 , pp. 129 - 137
Copyright
Copyright © Cambridge University Press 2014 

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

AIBA, M. & NAKASHIZUKA, T. 2005. Sapling structure and regeneration strategy in 18 Shorea species co-occurring in a tropical rainforest. Annals of Botany 96:313–321.Google 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 18:379–388.CrossRefGoogle Scholar
ANDERSON, D. G., BURNHAM, K. P. & WHITE, G. C. 1998. Comparison of Akaike information criterion and consistent Akaike information criterion for model selection and statistical inference from capture-recapture studies. Journal of Applied Statistics 25:263–282.CrossRefGoogle Scholar
APPANAH, S. 1985. General flowering in the climax rain forest of South-east Asia. Journal of Tropical Ecology 1:225–240.Google Scholar
ASHTON, P. S., GIVNISH, T. J. & APPANAH, S. 1988. Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. American Naturalist 132:44–66.CrossRefGoogle Scholar
BAGCHI, R., PHILIPSON, C. D., SLADE, E. M., HECTOR, A., PHILIPS, S., VILLANUEVA, J. F., LEWIS, O. T., LYAL, C. H. C., NILUS, R., MADRAN, A., SCHOLES, J. D. & PRESS, M. C. 2011. Impacts of logging on density-dependent predation of dipterocarp seeds in a south east Asian rainforest. Philosophical Transactions of the Royal Society B: Biological Sciences 366:3246–3255.CrossRefGoogle Scholar
BAGCHI, R., GALLERY, R. E., GRIPENBERG, S., GURR, S. J., NARAYAN, L., ADDIS, C. E., FRECKLETON, R. P. & LEWIS, O. T. 2014. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506:85–88.Google Scholar
BAI, X., QUEENBOROUGH, S. A., WANG, X., ZHANG, J., LI, B., YUAN, Z., XING, D., LIN, F., YE, J. & HAO, Z. 2012. Effects of local biotic and neighbors and habitat heterogeneity on tree and shrub seedling survival in an old-growth temperate forest. Oecologia 170:755–765.Google Scholar
BEBBER, D. P., BROWN, N. D. & SPEIGHT, M. R. 2004. Dipterocarp seedling population dynamics in Bornean primary lowland forest during the 1997–98 El Niño–Southern Oscillation. Journal of Tropical Ecology 20:11–19.Google Scholar
BLUNDELL, A. G. & PEART, D. R. 2004. Seedling recruitment failure following dipterocarp mast fruiting. Journal of Tropical Ecology 20:229–231.Google Scholar
BOLKER, B. M., BROOKS, M. E., CLARK, C. J., GEANGE, S. W., POULSEN, J. R., STEVENS, M. H. H. & WHITE, J.-S. S. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24:127–135.CrossRefGoogle ScholarPubMed
BROWN, N. D. & WHITMORE, T. C. 1992. Do dipterocarp seedlings really partition tropical rain forest gaps? Philosophical Transactions of the Royal Society B: Biological Sciences 335:369–378.Google Scholar
BROWN, N., PRESS, M. & BEBBER, D. 1999. Growth and survivorship of dipterocarp seedlings: differences in shade persistence create a special case of dispersal limitation. Philosophical Transactions of the Royal Society B: Biological Sciences 354:1847–1855.Google Scholar
BURSLEM, D. F. R. P., GRUBB, P. J. & TURNER, I. M. 1996. Responses to simulated drought and elevated nutrient supply among shade-tolerant tree seedlings of lowland tropical forest in Singapore. Biotropica 28:636–648.CrossRefGoogle Scholar
CANNON, C. H., CURRAN, L. M., MARSHALL, A. J. & LEIGHTON, M. 2007. Long-term reproductive behaviour of woody plants across seven Bornean forest types in the Gunung Palung National Park (Indonesia): suprannual synchrony, temporal productivity and fruiting diversity. Ecology Letters 10:956–969.Google Scholar
CAO, K.-F. & BOOTH, E. W. 2001. Leaf anatomical structure and photosynthetic induction for seedlings of five dipterocarp species under contrasting light conditions in a Bornean heath forest. Journal of Tropical Ecology 17:163–175.CrossRefGoogle Scholar
CHEN, L., MI, X., COMITA, L. S., ZHANG, L., REN, H. & MA, K. 2010. Community-level consequences of density dependence and habitat association in a subtropical broad-leaved forest. Ecology Letters 13:695–704.CrossRefGoogle Scholar
COMITA, L. S. & ENGELBRECHT, B. M. J. 2009. Seasonal and spatial variation in water availability drive habitat associations in a tropical forest. Ecology 90:2755–2765.Google Scholar
COMITA, L. S. & HUBBELL, S. P. 2009. Local neighbourhood and species’ shade tolerance influence survival in a diverse seedling bank. Ecology 90:328–334.CrossRefGoogle Scholar
COMITA, L. S., URIARTE, M., THOMPSON, J., JONCKHEERE, I., CANHAM, C. D. & ZIMMERMAN, J. K. 2009. Abiotic and biotic drivers of seedling survival in a hurricane-impacted tropical forest. Journal of Ecology 97:1346–1359.CrossRefGoogle Scholar
COMITA, L. S., MULLER-LANDAU, H. C., AGUILAR, S. & HUBBELL, S. P. 2010. Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329:330–332.Google Scholar
COMITA, L. S., QUEENBOROUGH, S. A., MURPHY, S. J., ECK, J. L., XU, K., KRISHNADAS, M., BECKMAN, N. & ZHU, Y. 2014. Testing predictions of the Janzen–Connell hypothesis: a meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival. Journal of Ecology 102:845–856.Google Scholar
CONNELL, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Pp. 298–312 in den Boer, P. J. & Gradwell, G. R. (eds.). Dynamics of populations. Centre for Agricultural Publishing and Documentation, Wageningen.Google Scholar
CURRAN, L. M. & LEIGHTON, M. 2000. Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecological Monographs 70:101–128.Google Scholar
CURRAN, L. M. & WEBB, C. O. 2000. Experimental tests of the spatiotemporal scale of seed predation in mast-fruiting Dipterocarpaceae. Ecological Monographs 70:129–148.Google Scholar
DAVIES, S. J., TAN, S., LAFRANKIE, J. V. & POTTS, M. D. 2005. Soil-related floristic variation in the hyperdiverse dipterocarp forest in Lambir Hills, Sarawak. Pp. 22–34 in Roubik, D., Sakai, S. & Hamid, A. (eds.). Pollination ecology and rain forest diversity, Sarawak studies. Springer-Verlag, New York.Google Scholar
DELISSIO, L. J. & PRIMACK, R. B. 2003. The impact of drought on the population dynamics of canopy-tree seedlings in an aseasonal Malaysian rain forest. Journal of Tropical Ecology 19:489–500.Google Scholar
DELISSIO, L. J., PRIMACK, R. B., HALL, P. & LEE, H. S. 2002. A decade of canopy-tree seedling survival and growth in two Bornean rain forests: persistence and recovery from suppression. Journal of Tropical Ecology 18:645–658.CrossRefGoogle Scholar
EVERHAM, E. M., MYSTER, R. W. & VANDEGENACHTE, E. 1996. Effects of light, moisture, temperature, and litter on the regeneration of five tree species in the tropical montane wet forest of Puerto Rico. American Journal of Botany 83:1063–1068.Google Scholar
GELMAN, A. & HILL, J. 2006. Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, Cambridge. 648 pp.CrossRefGoogle Scholar
HARMS, K. E., WRIGHT, S. J., CALDERÓN, O., HERNÁNDEZ, A. & HERRE, E. A. 2000. Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404:493–495.Google Scholar
ICHIE, T., NINOMIYA, I. & OGINO, K. 2001. Utilization of seed reserves during germination and early seedling growth by Dryobalanops lanceolata (Dipterocarpaceae). Journal of Tropical Ecology 17:371–378.CrossRefGoogle Scholar
ISHIZUKA, S., TANAKA, S., SAKURAI, K., HIRAI, H., HIROTANI, H., OGINO, K., LEE, H. S. & KENDAWANG, J. J. 1998. Characterization and distribution of soils at Lambir Hills National Park in Sarawak, Malaysia, with special reference to soil hardness and soil texture. Tropics 8:31–44.Google Scholar
ITOH, A. 1995. Effects of forest floor environment on germination and seedling establishment of two Bornean rainforest emergent species. Journal of Tropical Ecology 11:517–527.Google Scholar
ITOH, A., YAMAKURA, T., OGINO, K. & LEE, H. S. 1995. Survivorship and growth of seedlings of four dipterocarp species in a tropical rainforest of Sarawak, East Malaysia. Ecological Research 10:327–338.Google Scholar
JANZEN, D. H. 1970. Herbivores and number of tree species in tropical forests. American Naturalist 104:501.Google Scholar
JANZEN, D. H. 1974. Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6:69–103.CrossRefGoogle Scholar
JOHNSON, D. J., BEAULIEU, W. T., BEVER, J. D. & CLAY, K. 2012. Conspecific negative density dependence and forest diversity. Science 336:904–907.Google Scholar
KOBE, R. K. 1999. Light gradient partitioning among tropical tree species through differential seedling mortality and growth. Ecology 80:187–201.Google Scholar
KOBE, R. K. & VRIESENDORP, C. F. 2011. Conspecific density dependence in seedlings varies with species shade tolerance in a wet tropical forest. Ecology Letters 14:503–510.Google Scholar
KUME, T., TANAKA, N., KURAJI, K., KOMATSU, H., YOSHIFUJI, N., SAITOH, T. M., SUZUKI, M. & KUMAGAI, T. 2011. Ten-year evapotranspiration estimates in a Bornean tropical rainforest. Agricultural and Forest Meteorology 151:1183–1192.Google Scholar
LAMONTAGNE, J. M. & BOUTIN, S. 2007. Local-scale synchrony and variability in mast seed production patterns of Picea glauca. Journal of Ecology 95:991–1000.Google Scholar
LEE, H. S., DAVIES, S. J., LAFRANKIE, J. V., TAN, S., YAMAKURA, T., ITOH, A., OHKUBO, T. & ASHTON, P. S. 2002. Floristic and structural diversity of mixed dipterocarp forests in Lambir Hills National Park, Sarawak, Malaysia. Journal of Tropical Forest Science 14:379–400.Google Scholar
LIN, L., COMITA, L. S., ZHENG, Z. & CAO, M. 2012. Seasonal differentiation in density-dependent seedling survival in a tropical rain forest. Journal of Ecology 100:905–914.Google Scholar
MAYCOCK, C. R., THEWLIS, R. N., GHAZOUL, J., NILUS, R. & BURSLEM, D. F. R. P. 2005. Reproduction of dipterocarp during low intensity masting events in a Bornean rain forest. Journal of Vegetation Science 16:635–646.Google Scholar
NAKAGAWA, M., MATSUSHITA, M., KUROKAWA, H., SAMEJIMA, H., TAKEUCHI, Y., AIBA, M., KATAYAMA, A., TOKUMOTO, Y., KUME, T., YOSHIFUJI, N., KURAJI, K., NAGAMASU, H., SAKAI, S. & NAKASHIZUKA, T. 2012. Possible negative effect of general flowering on tree growth and aboveground biomass increment in a Bornean tropical rainforest. Biotropica 44:715–719.Google Scholar
NG, F. S. P. 1991. Manual of forest fruits, seeds and seedlings. Forest Research Institute Malaysia, Kuala Lumpur. 400 pp.Google Scholar
NORDEN, N., CHAVE, J., BELBENOIT, P., CAUBÈRE, A., CHÂTELET, P., FORGET, P.-M. & THÉBAUD, C. 2007. Mast fruiting is a frequent strategy in woody species of eastern South America. PloS ONE 2:e1079.Google Scholar
NORTON, D. A. & KELLY, D. 1988. Mast seedling over 33 years by Dacrydium cupressinum Lamb. (rimu) (Podocarpaceae) in New Zealand: the importance of economies of scale. Functional Ecology 2:399–408.Google Scholar
PAINE, C. E. T., HARMS, K. E., SCHNITZER, S. A. & CARSON, W. P. 2008. Weak competition among tropical tree seedlings: implications for coexistence. Biotropica 40:432–440.CrossRefGoogle Scholar
PHILIPSON, C. D., SANER, P., MARTHEWS, T. R., NILUS, R., REYNOLDS, G., TURNBULL, L. A. & HECTOR, A. 2012. Light-based regeneration niches: evidence from 21 dipterocarp species using size-specific RGRs. Biotropica 44:627–636.CrossRefGoogle Scholar
QUEENBOROUGH, S. A., BURSLEM, D. F. R. P., GARWOOD, N. C. & VALENCIA, R. 2007. Neighborhood and community interactions determine the spatial pattern of tropical tree seedling survival. Ecology 88:2248–2258.Google Scholar
QUEENBOROUGH, S. A., BURSLEM, D. F. R. P., GARWOOD, N. C. & VALENCIA, R. 2009. Taxonomic scale-dependence of habitat niche partitioning and biotic neighbourhood on survival of tropical tree seedlings. Proceedings of the Royal Society B: Biological Sciences 276:4197–4205.Google Scholar
RUSSO, S. E., DAVIES, S. J., KING, D. A. & TAN, S. 2005. Soil-related performance variation and distributions of tree species in a Bornean rain forest. Journal of Ecology 93:879–889.Google Scholar
SAKAI, S. 2002. General flowering in lowland mixed dipterocarp forests of South-east Asia. Biology Journal of the Linnean Society 75:233–247.CrossRefGoogle Scholar
SAKAI, S., MOMOSE, K., YUMOTO, T., NAGAMITSU, T., NAGAMASU, H., HAMID, A. A. & NAKASHIZUKA, T. 1999. Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. American Journal of Botany 86:1414–1436.Google Scholar
SAKAI, S., HARRISON, R., MOMOSE, K., KURAJI, K., NAGAMASU, H., YASUNARI, T., CHONG, L. & NAKASHIZUKA, T. 2006. Irregular droughts trigger mass flowering in aseasonal tropical forests in Asia. American Journal of Botany 93:1134–1139.Google Scholar
SHIBATA, M., TANAKA, H., IIDA, S., ABE, S., MASAKI, T., NIIYAMA, K. & NAKASHIZUKA, T. 2002. Synchronized annual seed production by 16 principal tree species in a temperate deciduous forest, Japan. Ecology 83:1727–1742.CrossRefGoogle Scholar
SHIBATA, M., MASAKI, T., TANAKA, H., NIIYAMA, K., IIDA, S., ABE, S. & NAKASHIZUKA, T. 2010. Effects of abiotic and biotic factors and stochasticity on tree regeneration in a temperate forest community. Ecoscience 17:137–145.CrossRefGoogle Scholar
SORK, V. L., BRAMBLE, J. & SEXTON, O. 1993. Ecology of mast-fruiting in three species of North American deciduous oaks. Ecology 74:528–541.Google Scholar
SUN, I.-F., CHEN, Y.-Y., HUBBELL, S. P., WRIGHT, S. J. & NOOR, N. S. M. 2007. Seed predation during general flowering events of varying magnitude in a Malaysian rain forest. Journal of Ecology 95:818–827.Google Scholar
TAKEUCHI, Y. & NAKASHIZUKA, T. 2007. Effect of distance and density on seed/seedling fate of two dipterocarp species. Forest Ecology and Management 247:167–174.Google Scholar
TAKEUCHI, Y., KENTA, T. & NAKASHIZUKA, T. 2005. Comparison of sapling demography of four dipterocarp species with different seed-dispersal strategies. Forest Ecology and Management 208:237–248.Google Scholar
TOKUMOTO, Y., MATSUSHITA, M., TAMAKI, I., SAKAI, S. & NAKAGAWA, M. 2009. How does flowering magnitude affect seed survival in Shorea pilosa (Dipterocarpaceae) at predispersal stage in Malaysia? Plant Species Biology 24:104–108.Google Scholar
TURNER, I. M. 1990. The seedling survivorship and growth of three Shorea species in a Malysian tropical rain forest. Journal of Tropical Ecology 6:469–478.Google Scholar
VISSER, M. D., JONGEJANS, E., VAN BREUGEL, M., ZUIDEMA, P. A., CHEN, Y.-Y., KASSIM, A. R. & DE KROON, H. 2011. Strict mast fruiting for a tropical dipterocarp tree: a demographic cost-benefit analysis of delayed reproduction and seed predation. Journal of Ecology 99:1033–1044.Google Scholar
WALKER, L. R., LODGE, D. J., GUZMÁN-GRAJALES, S. M. & FETCHER, N. 2003. Species-specific seedling responses to hurricane disturbance in a Puerto Rican rain forest. Biotropica 35:472–485.Google Scholar
WEBB, C. O. & PEART, D. R. 1999. Seedling density dependence promotes coexistence of Bornean rain forest trees. Ecology 80:2006–2017.Google Scholar
WHITMORE, T. C. 1984. Tropical rain forests of the Far East. (Second edition). Oxford University Press, Oxford. 352 pp.Google Scholar
YAGIHASHI, T., OTANI, T., TANI, N., NAKAYA, T., RAHMAN, K. A., MATSUI, T. & TANOUCHI, H. 2010. Habitats suitable for the establishment of Shorea curtisii seedlings in a hill forest in Peninsular Malaysia. Journal of Tropical Ecology 26:551–554.Google Scholar