Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-11T00:32:52.811Z Has data issue: false hasContentIssue false

Climate-induced abortion and predation: reproductive success of the pioneer shrub Dillenia suffruticosa in Malaysian Borneo

Published online by Cambridge University Press:  23 December 2015

Yuji Tokumoto*
Affiliation:
Graduate School of Engineering, Osaka University, Suita, 565–0871, Japan
Michiko Nakagawa
Affiliation:
Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464–8601, Japan
*
1Corresponding author. Email: tokumoto.ug@gmail.com

Abstract:

In South-East Asian tropical plants, the excess production of reproductive organs is believed to be controlled by resource booms. However, the continuously flowering shrub Dillenia suffruticosa (Dilleniaceae) is often infested by fruit predators and occasionally produces fruits where mature seeds are absent. These reproductive features may support an alternative hypothesis for excess production of reproductive organs: the reproductive assurance hypothesis. We marked 1190 reproductive organs in 180 inflorescences of 41 plant individuals and examined the relationships among the reproductive organ features and the effects of both climate and predators. During the flower budding stage, the fate of reproductive organs was primary climate-induced. The percentage of flower/fruit abscission increased as the cumulative temperature and photosynthetically active radiation (PAR) decreased and the cumulative precipitation increased, supporting the resource boom hypothesis. Insect predation was the most common fate of immature fruits. As PAR increased, the prevalence of insect predation and production of mature seed increased. At a reduced PAR, the production of fruits with many immature seeds could serve as compensatory reproductive organs for insect predators, consistent with the reproductive assurance hypothesis. The excess production of reproductive organs might be a result of adaptation to climate fluctuations in the South-East Asian tropics.

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

BURD, M. 1998. “Excess” flower production and selective fruits abortion: a model of potential benefits. Ecology 79:21232132.Google Scholar
CAMPBELL, D. R. & HALAMA, K. J. 1993. Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology 74:10431051.CrossRefGoogle Scholar
CUNNINGHAM, S. A. 1997. The effect of light environment, leaf area, and stored carbohydrates on inflorescence production by a rain forest understory palm. Oecologia 111:3644.CrossRefGoogle ScholarPubMed
DAVIES, S. J. & ASHTON, P. S. 1996. Phenology and fecundity in 11 sympatric pioneer species of Macaranga (Euphorbiaceae) in Borneo. American Journal of Botany 86:17861795.CrossRefGoogle Scholar
DAVIES, S. J. & SEMUI, H. 2006. Competitive dominance in a secondary successional rain-forest community in Borneo. Journal of Tropical Ecology 22:5364.CrossRefGoogle Scholar
ENDRESS, P. K. 1982. Syncarpy and alternative modes of escaping disadvantages of apocarpy in primitive angiosperms. Taxon 31:4852.CrossRefGoogle Scholar
ENDRESS, P. K. 1997. Relationship between floral organization, architecture, and pollination mode in Dillenia (Dilleniaceae). Plant Systematics and Evolution 206:99118.CrossRefGoogle Scholar
FIGUEROA-CASTRO, D. M. & VALVERDE, P. L. 2011. Flower orientation in Pachycereus weberi (Cactaceae): effects on ovule production, seed production and seed weight. Journal of Arid Environments 75:12141217.CrossRefGoogle Scholar
FLANAGAN, L. B. & JOHNSON, B. G. 2005. Interacting effects of temperature, soil moisture and plant biomass production on ecosystem respiration in a northern temperate grassland. Agricultural and Forest Meteorology 130:237253.CrossRefGoogle Scholar
GHAZOUL, J., LISTON, K. A. & BOYLE, T. J. B. 1998. Disturbance induced density-dependent seed set in Shorea siamensis (Dipterocarpaceae), a tropical forest tree. Journal of Ecology 86:462473.CrossRefGoogle Scholar
GOTO, R., OKAMOTO, T., KIERS, T. E., KAWAKITA, A. & KATO, M. 2010. Selective flower abortion maintains moth cooperation in a newly discovered pollination mutualism. Ecology Letters 13:321329.CrossRefGoogle Scholar
HADFIELD, J. D. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software 33:122.CrossRefGoogle Scholar
HARRISON, R. D. 2003. Fig wasp dispersal and the stability of a keystone plant resource in Borneo. Proceedings of the Royal Society of London Series B: Biological Sciences 270: S76–S79.CrossRefGoogle ScholarPubMed
HOLTSFORD, T. P. 1985. Nonfruiting hermaphroditic flowers of Calochortus leichtlinii (Liliaceae): potential reproductive functions. American Journal of Botany 72:16871694.CrossRefGoogle Scholar
HOOGLAND, R. D. 1952. A revision of the genus Dillenia. Blumea 7:1145.Google Scholar
HOOGLAND, R. D. & WADHWA, B. M. 1996. Proposal to conserve the name Wormia suffruticosa against Wormia subsessilis (Dilleniaceae). Taxon 45:130.CrossRefGoogle Scholar
HORN, J. W. 2009. Phylogenetics of Dilleniaceae using sequence data from four plastid loci (rbcL, infA, rps4, rpl16 Intron). International Journal of Plant Science 170:794813.CrossRefGoogle Scholar
ICHIE, T., KITAHASHI, Y., MATSUKI, S., MARUYAMA, Y. & KOIKE, T. 2002. The use of a portable non-destructive type nitrogen meter for leaves of woody plants in field studies. Photosynthetica 40:289292.CrossRefGoogle Scholar
ISHIZAKI, S., NARUMI, T., MIZUSHIMA, M. & OHARA, M. 2010. Effects of the specialist herbivore Luehdorfia puziloi on the performance of a woodland herbaceous plant, Asarum heterotropoides. Plant Species Biology 25:6167.CrossRefGoogle Scholar
KAMOI, T., KENZO, T., KURAJI, K. & MOMOSE, K. 2008. Abortion of reproductive organs as an adaptation to fluctuating daily carbohydrate production. Oecologia 154:663677.CrossRefGoogle ScholarPubMed
KENTA, T., SHIMIZU, K. K., NAKAGAWA, M., OKADA, K., HAMID, A. A. & NAKASHIZUKA, T. 2002. Multiple factors contribute to outcrossing in a tropical emergent Dipterocarpus tempehes, including a new pollen-tube guidance mechanism for self-incompatibility. American Journal of Botany 89:6066.CrossRefGoogle Scholar
KENTA, T., INARI, N., NAGAMITSU, T., GOKA, K. & HIURA, T. 2007. Commercialized European bumblebee can cause pollination disturbance: an experiment on seven native plant species in Japan. Biological Conservation 134:298309.CrossRefGoogle Scholar
KENZO, T., YONEDA, R., AZANI, M. A. & MAJID, N. M. 2010. Measurement of integrated light intensity by using simple recording film in tropical rainforest. Kantoshinrinkenkyu 61:137140. (in Japanese)Google Scholar
KNIGHT, T. M., STEES, J. A., VAMOSI, J. C., MAZAR, S. J., BURD, M., CAMPBELL, D. R., DUDASH, M. R., JOHNSTON, M. O., MITCHELL, R. J. & ASHMAN, T.-L. 2005. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution, and Systematics 36:467497.CrossRefGoogle Scholar
KOCHUMMEN, K. M. 1972. Dilleniaceae. Pp. 183–193 in Whitmore, T. C. (ed.). Tree flora of Malaya Volume one. Longman Malaysia SDN. BERHAD, Kuala Lumpur.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 151:11831192.CrossRefGoogle Scholar
LAY, C. R., LINHART, Y. B. & DIGGLE, P. K. 2011. The good, the bad and the flexible: plant interactions with pollinators and herbivores over space and time are moderated by plant compensatory responses. Annals of Botany 108:749763.CrossRefGoogle ScholarPubMed
LEE, H. S., ASHTON, P. S., YAMAKURA, T., DAVIES, S. J., ITOH, A., CHAI, E. O., OHKUBO, T. & LAFRANKIE, J. V. 2003. The 52-ha forest research plot at Lambir Hills National Park, Sarawak, Malaysia: diameter tables, distribution maps and species documentation. Sarawak Forest Department and Smithsonian Tropical Research Institute, Kuching Sarawak, Malaysia.Google Scholar
MEDRANO, M., GUITIÁN, P. & GUITIÁN, J. 2000. Patterns of fruit and seed set within inflorescences of Pancratium maritimum (Amaryllidaceae): nonuniform pollination, resource limitation, or architectural effect? American Journal of Botany 87:493501.CrossRefGoogle ScholarPubMed
MICHALOUD, G., CARRIÈRE, S. & KOBBI, M. 1996. Exception to the one: one relationship between African fig trees and their fig wasp pollinators: possible evolutionary scenarios. Journal of Biogeography 23:513520.CrossRefGoogle Scholar
MIYAKAWA, T., SATOH, M., MIURA, H., TOMITA, H., YASHIRO, H., NODA, A. T., YAMADA, Y., KODAMA, C., KIMOTO, M. & YONEYAMA, K. 2014. Madden–Julian Oscillation prediction skill of a new-generation global model demonstrated using a supercomputer. Nature Communications 5: art. 3769.CrossRefGoogle ScholarPubMed
MOMOSE, K. 2004. Plant reproductive interval and population density in aseasonal tropics. Ecological Research 19:245253.CrossRefGoogle Scholar
MOMOSE, K., NAGAMITSU, T. & INOUE, T. 1996. The reproductive ecology of an emergent dipterocarp in a lowland rain forest in Sarawak. Plant Species Biology 11:189198.CrossRefGoogle Scholar
MOTHERSHEAD, K. & MARQUIS, R. J. 2000. Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81:3040.Google Scholar
MUÑOS, A. A., CELEDON-NEGHME, C., CAVIERES, L. A. & ARROYO, M. T. K. 2005. Bottom-up effects of nutrient availability on flower production, pollinator visitation, and seed output in a high-Andean shrub. Oecologia 143:126135.CrossRefGoogle Scholar
NAKAGAWA, M., TAKEUCHI, Y., KENTA, T. & NAKASHIZUKA, T. 2005. Predispersal seed predation by insects vs. vertebrates in six dipterocarp species in Sarawak, Malaysia. Biotropica 37:389396.CrossRefGoogle Scholar
NEWSTROM, L. E., FRANKIE, G. W. & BAKER, H. G. 1994. A new classification for plant phenology based on flowering patterns in lowland tropical rain forest trees at La Selva, Costa Rica. Biotropica 26:141159.CrossRefGoogle Scholar
NIESENBAUM, R. A. 1993. Light or pollen – seasonal limitations on female reproductive success in the understory shrub Lindera benzoin. Journal of Ecology 81:315323.CrossRefGoogle Scholar
OBESO, J. R. 2002. Tansley review no. 139. The costs of reproduction in plants. New Phytologist 155:321348.CrossRefGoogle Scholar
OGAWA, K., ABDULLAH, A., AWANG, M. & FURUKAWA, A. 2005. Diel changes in the CO2 exchange rates of reproductive organs of the tropical tree Durio zibethinus. Journal of Plant Research 118:187192.CrossRefGoogle ScholarPubMed
PAYNE, J. & FRANCIS, C. M. 2005. A field guide to the mammals of Borneo. The Sabah Society, Petaling Jaya. 332 pp.Google Scholar
RIVERA, G. & BORCHERT, R. 2001. Induction of flowering in tropical trees by a 30-min reduction in photoperiod: evidence from field observations and herbarium specimens. Tree Physiology 21:201212.CrossRefGoogle ScholarPubMed
SAKAI, S. 2000. Reproductive phenology of gingers in a lowland mixed dipterocarp forest in Borneo. Journal of Tropical Ecology 16:337354.CrossRefGoogle Scholar
SAKAI, S., MOMOSE, K., YUMOTO, T., NAGAMITSU, T., NAGAMASU, H., HAMID, A. A. & NAKASHIZUKA, T. 1999a. Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. American Journal of Botany 86:14141436.CrossRefGoogle Scholar
SAKAI, S., MOMOSE, K., YUMOTO, T., KATO, M. & INOUE, T. 1999b. Beetle pollination of Shorea parviforia (section Mutica, Dipterocarpaceae) in a general flowering period in Sarawak, Malaysia. American Journal of Botany 86:6269.CrossRefGoogle Scholar
SCHNEIDER, C. A., RASBAND, W. S. & ELICEIRI, K. W. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9:671675.CrossRefGoogle ScholarPubMed
SHEM-TOV, S. & GUTTERMAN, Y. 2003. Influence of water regime and photoperiod treatments on resource allocation and reproductive success of two annuals occurring in the Negev Desert of Israel. Journal of Arid Environments 55:123142.CrossRefGoogle Scholar
SHIPP, J. L., GRACE, B. W. & SCHAALJE, G. B. 1987. Effects of microclimate on daily flight activity of Simulium arcticum Malloch (Diptera: Simuliidae). International Journal of Biometeorology 31:920.CrossRefGoogle Scholar
SOMANATHAN, H. & BORGES, R. M. 2010. Influence of exploitation on population structure, spatial distribution and reproductive success of dioecious species in a fragmented cloud forest in India. Biological Conservation 94:243256.CrossRefGoogle Scholar
SPIEGELHALTER, D. J., BEST, N. G., CARLIN, B. R. & VAN DER LINDE, A. 2002. Bayesian measures of model complexity and fit. Proceedings of the Royal Society of London Series B: Biological Sciences 64:583--639.CrossRefGoogle Scholar
STEPHENSON, A. G. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology, Evolution, and Systematics 12:253279.CrossRefGoogle Scholar
TOKUMOTO, Y., MATSUSHITA, M., TAMAKI, I., SAKAI, S. & NAKAGAWA, M. 2009. How does flowering magnitude affect seed survival in Shorea pilosa (Dipterocarpaceae) at the predispersal stage in Malaysia? Plant Species Biology 24:104108.CrossRefGoogle Scholar
TOKUMOTO, Y., SAKAI, S., MATSUSHITA, M., OHKUBO, T. & NAKAGAWA, M. 2014. Spatiotemporal variability in the reproductive success of the continually flowering shrub Dillenia suffruticosa in Borneo. Biotropica 46:583590.CrossRefGoogle Scholar
VAN DER PIJL, L. 1954. Xylocopa and flowers in the tropics. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C, Biological and Medical Sciences 57:413–423.Google Scholar
WATANABE, T. 1997. Aluminum-induced growth stimulation in relation to calcium, magnesium, and silicate nutrition in Melastoma malabathricum L. Soil Science and Plant Nutrition 43:827837.CrossRefGoogle Scholar
WESSELINGH, R. A. 2007. Pollen limitation meets resource allocation: towards a comprehensive methodology. New Phytologist 174:2637.CrossRefGoogle ScholarPubMed
ZHANG, S., HU, H., ZHOU, Z., XU, K., YAN, N. & LI, S. 2005. Photosynthesis in relation to reproductive success of Cypripedium flavum. Annals of Botany 96:4349.CrossRefGoogle ScholarPubMed