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Dynamics of mineral nutrient storage for mast reproduction in the tropical emergent tree Dryobalanops aromatica

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  • New insights into mechanism and evolution of mast flowering: feedback between theory and experiment
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Ecological Research

An Erratum to this article was published on 18 December 2012

Abstract

Limitations in resources are considered to be important in mass-fruiting trees, based on the speculation that they need to consume a large amount of stored resources in a very short period. To test this hypothesis, we studied the total reproductive costs per individual of the tree Dryobalanops aromatica (Dipterocarpaceae), and the dynamics of stored mineral nutrients, specifically nitrogen, phosphorus, and potassium; we then estimated the contribution of each of the stored resources to reproduction in a lowland dipterocarp forest in Sarawak, Malaysia. D. aromatica is an emergent and masting tree species, and it produced a large amount of mature fruit in a masting period running 2001–2002. The dynamics patterns were markedly different for each of the stored nutrients. The phosphorus concentration clearly decreased in the branch, stem and root during reproduction, but nitrogen fluctuated by only a small amount in any organ during this period. The potassium concentration fell in all organs during flowering, but even increased during fruit development. Stored phosphorus accounted for 67.7% of the total phosphorus requirements for reproduction, but nitrogen accounted for only 19.7%. Stored potassium did not appear to contribute anything, at least to fruit production. Our results suggest that D. aromatica supplies phosphorus needed for reproduction mainly from stored resources in the tree, unlike nitrogen or potassium. The accumulation of phosphorus could be the decisive factor in the occurrence and frequency of mast reproduction in the relatively poor soil conditions prevailing in the tropical rain forests of Southeast Asia.

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References

  • Appanah S (1993) Mass flowering of dipterocarp forests in the aseasonal tropics. J Biosci 18:457–474

    Article  Google Scholar 

  • Ashton PS (1964) Manual of the dipterocarp trees of Brunei State. Oxford University Press, London

    Google Scholar 

  • Ashton PS (1982) Dipterocarpaceae. Flora Malesiana Ser 1 9:237–552

  • Ashton PS, Hall P (1992) Comparisons of structure among mixed dipterocarp forests of north-western Borneo. J Ecol 80:459–481

    Article  Google Scholar 

  • Ashton PS, Givinish TJ, Appanah S (1988) Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. Am Nat 132:44–66

    Article  Google Scholar 

  • Baker TR, Swaine MD, Burslem DFRP (2003) Variation in tropical forest growth rates: combined effects of functional group composition and resource availability. Perspect Plant Ecol Evol Syst 6:21–36

    Article  Google Scholar 

  • Ballie IC (1996) Soils of the humid tropics. In: Richards PW (ed) The tropical rain forest, 2nd edn. Cambridge University Press, Cambridge, pp 256–286

    Google Scholar 

  • Ballie IC, Ashton PS, Chin SP, Davies SJ, Palmiotto PA, Russo SE, Tan S (2006) Spatial association of humus, nutrients and soils in mixed dipterocarp forest at Lambir, Sarawak, Malaysian Borneo. J Trop Ecol 22:543–553

    Article  Google Scholar 

  • Bazzaz RA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67

    Article  Google Scholar 

  • Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–392

    Google Scholar 

  • Bullock JA (1981) In: Reichele DE (ed) Dynamic properties of forest ecosystems. Cambridge University Press, New York

  • Chan HT, Appanah S (1980) Reproductive biology of some Malaysian dipterocarp I—flowering biology. Malay For 38:160–170

    Google Scholar 

  • Chapin FS, Schulze E-D, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • Corlett RT (2009) The ecology of tropical East Asia. Oxford University Press, New York

    Google Scholar 

  • Cuevas E, Medina E (1988) Nutrient dynamics within Amazonian forests. Oecologia 76:222–235

    Article  Google Scholar 

  • Curran LM, Caniago I, Paoli GD, Astianti D, Kusneti M, Leighton M, Nirarita CE, Haeruman H (1999) Impact of El Niño and logging on canopy tree recruitment in Borneo. Science 286:2184–2188

    Article  PubMed  CAS  Google Scholar 

  • Foxworthy FW (1932) Dipterocarpaceae of the Malay Peninsula. Malayan Forest Record No. 10, Printers, Singapore

  • Goto S (1990) Digestion method (in Japanese). In: Editorial committee of methods for experiments in plant nutrition (eds) Manual of plant nutrition. Hakuyusha, Tokyo, pp 125–128

  • Henkel TW, Mayor JR, Woolley LP (2005) Mast fruiting and seedling survival of the ectomycorrhizal monodominant Dicymbe corymbosa (Caesalpiniaceae) in Guyana. New Phytol 167:543–556

    Article  PubMed  Google Scholar 

  • Hill-Cottingham DG, Lloyd-Jones CP (1975) Nitrogen-15 in apple nutrient investigations. J Sci Food Agric 26:165–173

    Article  CAS  Google Scholar 

  • Ichie T, Kenzo T, Kitahashi Y, Koike T, Nakashizuka T (2005a) How does Dryobalanops aromatica supply carbohydrate resources in a masting year? Trees 19:703–710

    Article  Google Scholar 

  • Ichie T, Kenta T, Nakagawa M, Sato K, Nakashizuka T (2005b) Resource allocation to reproductive organs during masting in the tropical emergent tree, Dipterocarpus tempehes. J Trop Ecol 21:237–241

    Article  Google Scholar 

  • Inoue T, Yumoto T, Hamid AA, Lee HS, Ogino K (1995) Construction of a canopy observation system in a tropical rainforest of Sarawak. Selbyana 16:24–35

    Google Scholar 

  • Isagi Y, Sumimura K, Sumida A, Ito H (1997) How does masting happen and synchronize? J Theor Biol 187:231–239

    Article  Google Scholar 

  • Itioka T, Inoue T, Kaliang H, Kato M, Nagamitsu T, Momose K, Sakai S, Yumoto T, Mohamad SU, Hamid AA, Yamane S (2001) Six-year population fluctuation of the giant honey bee Apis dorsata (Hymenoptera: Apidae) in a tropical lowland dipterocarp forest in Sarawak. Ann Entomol Soc Am 94:545–549

    Article  Google Scholar 

  • Itoh A (1995) Effects of forest floor environment on germination and seedling establishment of two Bornean rainforest emergent species. J Trop Ecol 11:517–527

    Article  Google Scholar 

  • Itoh A, Yamakura T, Ogino K, Lee HS (1995) Survivorship and growth of seedlings of four dipterocarp species in a tropical rainforest of Sarawak, East Malaysia. Ecol Res 10:327–338

    Article  Google Scholar 

  • Janzen DH (1974) Tropical blackwater rivers, animals and mast fruiting by the Dipterocarpaceae. Biotropica 6:69–103

    Article  Google Scholar 

  • Kachi N, Okuda T, Yap SK (1993) Seedling establishment of a canopy tree species in Malaysian tropical rain forests. Plant Species Biol 8:167–174

    Article  Google Scholar 

  • Kato T (1986) Nitrogen metabolism and utilization in Citrus. Hortic Rev 8:181–216

    Google Scholar 

  • Kato M, Inoue T, Hamid AA, Nagamitsu T, Merdek MB, Nona AR, Itino T, Yamane S, Yumoto T (1995) Seasonality and vertical structure of light-attracted insect communities in a dipterocarp forest in Sarawak. Res Popul Ecol 37:59–79

    Article  Google Scholar 

  • Kelly D (1994) The evolutionary ecology of mast seeding. Trends Ecol Evol 9:465–470

    Article  PubMed  CAS  Google Scholar 

  • Kelly D, Sork VL (2002) Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Evol Syst 33:427–447

    Article  Google Scholar 

  • Kira T (1978) Primary productivity of Pasoh forest—a synthesis. Malay Nat J 30:291–297

    Google Scholar 

  • Kitayama K (2005) Comment on ‘‘Ecosystem properties and forest decline in contrasting long-term chronosequences’’. Science 308:633

    Google Scholar 

  • Koenig WD, Mumme RL, Carmen WJ, Stanback MT (1994) Acorn production by oaks in central coastal California, variation within and among years. Ecology 75:99–109

    Article  Google Scholar 

  • Leake JR, Duran AL, Hardy KE, Johnson I, Beerling DJ, Banwart SA, Smits MM (2008) Biological weathering in soil: the role of symbiotic root-associated fungi biosensing minerals and directing photosynthates-energy into grain-scale mineral weathering. Mineral Mag 72:85–89

    Article  CAS  Google Scholar 

  • Millard P, Grelet G-A (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095

    Article  PubMed  CAS  Google Scholar 

  • Millard P, Sommerkorn M, Grelet G-A (2007) Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytol 175:11–28

    Article  PubMed  CAS  Google Scholar 

  • Momose K, Nagamitsu T, Inoue T (1996) The reproductive ecology of an emergent dipterocarp in a lowland rain forest in Sarawak. Plant Species Biol 11:189–198

    Article  Google Scholar 

  • Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, Sakai S, Harrison RD, Itioka T, Hamid AA, Inoue T (1998) Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am J Bot 85:1477–1501

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa M, Tanaka K, Nakashizuka T, Ohkubo T, Kato T, Maeda T, Sato K, Miguchi H, Nagamasu H, Ogino K, Teo S, Hamid AA, Lee HS (2000) Impact of severe drought associated with the 1997–1998 El Niño in a tropical forest in Sarawak. J Trop Ecol 16:355–367

    Article  Google Scholar 

  • Nakashizuka T, Lee HS, Chong L (2002) Studies on canopy processes of a tropical rain forest in Lambir Hills National Park. In: Itioka T, Nakashizuka T, Chong L (eds) Proceedings of the international symposium. Canopy processes and ecological roles of tropical rain forest. Center for Ecological Research, Kyoto University, Japan, pp 2–7

  • Newbery DM (2005) Ectomycorrhizas and mast fruiting in trees: linked by climate-driven resources? New Phytol 167:324–326

    Article  PubMed  CAS  Google Scholar 

  • Newbery DM, Alexander IJ, Rother JA (1997) Phosphorus dynamics in a lowland African rain forest: the influence of ectomycorrhizal trees. Ecol Monogr 67:367–409

    Google Scholar 

  • Newbery DM, Songwe NS, Chuyong GB (1998) Phenology and dynamics of an African rainforest at Korup, Cameroon. In: Newbery DM, Prins HHT, Brown ND (eds) Dynamics of tropical communities. Blackwell Science, London, pp 267–308

    Google Scholar 

  • Newbery DM, Chuyong GB, Zimmermann L (2006) Mast fruiting of large ectomycorrhizal African rain forest trees: importance of dry season intensity, and the resource-limitation hypothesis. New Phytol 170:561–579

    Article  PubMed  Google Scholar 

  • Ng FSP (1977) Gregarious flowering of dipterocarps in Kepong, 1976. Malay For 40:126–137

    Google Scholar 

  • Niiyama K, Kajimoto T, Matsuura Y, Yamashita T, Matsuo N, Yashiro Y, Ripina A, Kassima AR, Noora NS (2010) Estimation of root biomass based on excavation of individual root systems in a primary dipterocarp forest in Pasoh Forest Reserve, Peninsular Malaysia. J Trop Ecol 26:271–284

    Article  Google Scholar 

  • Numata S, Yasuda M, Okuda T, Kachi N, Nur Supardi MN (2003) Temporal and spatial patterns of mass flowerings on the Malay Peninsula. Am J Bot 90:1025–1031

    Article  PubMed  Google Scholar 

  • Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348

    Article  Google Scholar 

  • Ozanne CMP, Anhuf D, Boulter SL, Kitching RL, Köner C, Meinzer FC, Mitchell AW, Nakashizuka T, Silva Dias PL, Stork NE, Wright SJ, Yoshimura M (2003) Biodiversity meets the atmosphere: a global view of forest canopies. Science 301:183–186

    Article  PubMed  CAS  Google Scholar 

  • Paoli GD, Curran LM, Zak DR (2005) Phosphorus efficiency of Bornean rain forest productivity: evidence against the unimodal efficiency hypothesis. Ecology 86:1548–1561

    Article  Google Scholar 

  • Potts MD (2003) Drought in a Bornean everwet rain forest. J Ecol 91:467–474

    Article  Google Scholar 

  • Rineau F, Rose C, Le Thiec D, Garbaye J (2010) Liming in a beech forest results in more mineral elements stored in the mantle of Lactarius subdulcis ectomycorrhizas. Fungal Biol 114:1007–1014

    Article  PubMed  CAS  Google Scholar 

  • Sakai S (2002) General flowering in lowland mixed dipterocarp forests of South-east Asia. Biol J Linn Soc 75:233–247

    Article  Google Scholar 

  • Sakai S, Momose K, Yumoto T, Nagamitsu T, Nagamasu H, Hamid AA, Nakashizuka T (1999) Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. Am J Bot 86:1414–1436

    Article  PubMed  CAS  Google Scholar 

  • Sakai S, Nakashizuka T, Ichie T, Nomura M, Chong L (2002) Lambir Hills Canopy Crane, Malaysia. In: Michell AW, Secoy K, Jackson T (eds) Global canopy handbook. Techniques of access and study in the forest roof. Canopy Biology Programme, Oxford, pp 77–79

  • Sakai S, Harrison RD, Momose K, Kuraji K, Nagamasu H, Yasunari T, Chong L, Nakashizuka T (2006) Irregular droughts trigger mass flowering in aseasonal tropical forests in Asia. Am J Bot 93:1134–1139

    Article  PubMed  Google Scholar 

  • Satake A, Bjørnstad ON (2008) A resource budget model to explain intraspecific variation in mast reproductive dynamics. Ecol Res 23:3–10

    Article  Google Scholar 

  • Satake A, Iwasa Y (2000) Pollen coupling of forest trees: forming synchronized and periodic reproduction out of chaos. J Theor Biol 203:63–84

    Article  PubMed  CAS  Google Scholar 

  • Satake A, Iwasa Y (2002a) Spatially limited pollen exchange and a long-range synchronization of trees. Ecology 83:993–1005

    Article  Google Scholar 

  • Satake A, Iwasa Y (2002b) The synchronized and intermittent reproduction of forest trees is mediated by the Moran effect, only in association with pollen coupling. J Ecol 90:830–838

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, London

    Google Scholar 

  • Sork VL, Bramble J, Sexton O (1993) Ecology of mast-fruiting in three species of North American deciduous oaks. Ecology 74:528–541

    Article  Google Scholar 

  • Tromp J (1983) Nutrient reserves in roots of fruit trees, in particular carbohydrates and nitrogen. Plant Soil 71:401–413

    Article  CAS  Google Scholar 

  • Turner IM, Brown ND, Newton AC (1993) The effect of fertilizer application on dipterocarp seedling growth and mycorrhizal infection. For Ecol Manag 57:329–337

    Article  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resources. New Phytol 157:423–447

    Article  CAS  Google Scholar 

  • Vincent AJ (1961) A survey of the Kapur (Dryobalanops aromatica Gaertn. f.): silvicultural treatment research plots in naturally and artificially regenerated forest, Malaya. Forest Research Institute Research Pamphelet, No. 36, Kepong, Kuala Lumpur, Malaysia

  • Vogt KA, Vogt DJ, Palmiotto PA, Boon P, O’Hara J, Asbjornsen H (1996) Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species. Plant Soil 187:159–219

    Article  CAS  Google Scholar 

  • Wood GHS (1956) The dipterocarp flowering season in north Borneo. Malay For 19:193–201

    Google Scholar 

  • Yamakura T, Hagihara A, Sukardjo S, Ogawa H (1986) Aboveground biomass of tropical rain forest stands in Indonesian Borneo. Plant Ecol 68:71–82

    Google Scholar 

  • Yamauchi A (1996) Theory of mast reproduction in plants: storage-size dependent strategy. Evolution 50:1795–1807

    Article  Google Scholar 

  • Yasuda M, Matsumoto J, Osada N, Ichikawa S, Kachi N, Tani M, Okuda T, Furukawa A, Nik AR, Manokaran N (1999) The mechanism of general flowering in Dipterocarpaceae in the Malay Peninsula. J Trop Ecol 15:437–449

    Article  Google Scholar 

  • Yumoto T, Inoue T, Hamid AA (1996) Monitoring and inventorying system in canopy observation system in canopy biology program in Sarawak, Malaysia. Biodiversity and the dynamics of ecosystem, DIWPA series, vol 1. In: Turner IM, Diong CH, Lim SSL, Ng PKL (eds) The international network for DIVERSITAS in Western Pacific and Asia DIWPA. Center for Ecological Research, Kyoto University, Japan, pp 203–215

    Google Scholar 

  • Zagt RJ (1997) Pre-dispersal and early post-dispersal demography, and reproductive litter production, in the tropical tree Dicymbe altsonii in Guyana. J Trop Ecol 13:511–526

    Article  Google Scholar 

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Acknowledgments

We thank the Forest Department, Sarawak and Sarawak Forestry Corporation, and also Prof. T. Nakashizuka, Prof. N. Yamamura for their support of this study. Climate data were provided by Prof. M. Suzuki, Dr. K. Kuraji, and Dr. T. Kumagai, and helpful comments by Dr. T. Kenzo and Ms. M. Yamashita. We also thank Ms. Y. Kuzume for her help with the laboratory work. This research was partly supported by the Project of the Research Institute for Humanity and Nature (P2-5, D-04), by a Grant-in-Aid for Scientific Research (no. 18780116) from the Ministry of Education, Science and Culture, Japan, and by the Environment Research and Technology Development Fund (RF-1010) of the Ministry of the Environment, Japan.

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  1. Faculty of Agriculture, Kochi University, Nankoku, 783-8502, Japan

    Tomoaki Ichie

  2. Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601, Japan

    Michiko Nakagawa

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  1. Tomoaki Ichie
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  2. Michiko Nakagawa
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Correspondence to Tomoaki Ichie.

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Ichie, T., Nakagawa, M. Dynamics of mineral nutrient storage for mast reproduction in the tropical emergent tree Dryobalanops aromatica . Ecol Res 28, 151–158 (2013). https://doi.org/10.1007/s11284-011-0836-1

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