Ecological Research

, Volume 28, Issue 2, pp 143–150 | Cite as

Dynamics of internal carbon resources during masting behavior in trees

Special Feature New insights into mechanism and evolution of mast flowering: feedback between theory and experiment


Several proximate factors of masting have been provided. Here, I focus on the role of internal factors, especially the relationship between internal carbon resources and modular structures in trees. I summarize various studies of carbon resource allocation for reproduction during masting events in terms of the proximate factors of masting and discuss the modular structure in which trees accumulate and consume carbon resources as well as the timing when internal carbon resources affect masting since trees have complex resource dynamics among organs. The resource budget model, which provides a simple mechanistic explanation of the masting mechanism, is supported by various study lines. This model assumes decreasing levels of stored photosynthate after flowering and fruiting. According to several studies, however, carbon reserves do not decrease after fruiting in species in which the modules autonomously allocate current photosynthate for fruiting. In addition, it is important to elucidate when carbon resources affect masting events because during their long developmental processes, trees pass through various stages until they produce maturing fruits to create successful masting events. To explore the mechanisms of masting in future studies, it would be important to figure out how and when candidate factors (including nutrients other than carbon) may influence the entire reproduction process, for example, using field manipulation experiments.


Mass flowering Modular structure Proximate factor Resource budget model Resource dynamics 


  1. Agusti M, Andreu I, Juan M, Almela V, Zacarias L (1998) Effects of ringing branches on fruit size and maturity of peach and nectarine cultivars. J Hortic Sci Biotechnol 73:537–540Google Scholar
  2. Allen RB, Platt KH (1990) Annual seedfall variation in Nothofagus solandri (Fagaceae), Canterbury, New Zealand. Oikos 57:199–206CrossRefGoogle Scholar
  3. Ashman TL (1992) Indirect costs of seed production within and between seasons in a gynodioecious species. Oecologia 92:266–272CrossRefGoogle Scholar
  4. Ashton PS, Givnish 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 132:44–66CrossRefGoogle Scholar
  5. Bell G (1980) The costs of reproduction and their consequences. Am Nat 116:45–75CrossRefGoogle Scholar
  6. Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P (1993) Physiological signals that induce flowering. Plant Cell 5:1147–1155PubMedGoogle Scholar
  7. Büsgen M, Münch E (1929) The structure and life of forest trees. Chapman and Hall Ltd., LondonGoogle Scholar
  8. Caesar JC, Macdonald AD (1983) Shoot development in Betula papyrifera. II. Comparison of vegetative and reproductive short-shoot growth. Can J Bot 61:3066–3071CrossRefGoogle Scholar
  9. Caesar JC, Macdonald AD (1984) Shoot development in Betula papyrifera. V. Effect of male inflorescence formation and flowering on long shoot development. Can J Bot 62:1708–1713CrossRefGoogle Scholar
  10. Calfapietra C, Ainsworth EA, Beier C, De Angelis P, Ellsworth DS, Godbold DL, Hendrey GR, Hickler T, Hoosbeek MR, Karnosky DF, King J, Körner Ch, Leakey ADB, Lewin KF, Liberloo M, Long SP, Lukac M, Matyssek R, Miglietta F, Nagy J, Norby RJ, Oren R, Percy KE, Rogers A, Scarascia-Mugnozza G, Stitt M, Taylor G, Ceulemans R (2010) Challenges in elevated CO2 experiments on forests. Trends Plant Sci 15:5–10PubMedCrossRefGoogle Scholar
  11. Candolfi-Vasconcelos MC, Candolfi MP, Koblet W (1994) Retranslocation of carbon reserves from the woody storage tissues into the fruit as a response to defoliation stress during the ripening period in Vitis vinifera L. Planta 192:567–573CrossRefGoogle Scholar
  12. Cecich RA, Sullivan NH (1999) Influence of weather at time of pollination on acorn production of Quercus alba and Quercus velutina. Can J For Res 29:1817–1823Google Scholar
  13. Corbesier L, Lejeune P, Bernier G (1998) The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: comparison between the wild type and a starchless mutant. Planta 206:131–137PubMedCrossRefGoogle Scholar
  14. Corbesier L, Perilleux C, Bernier G (2002) C:N ratio increases in the phloem sap during floral transition of the long-day plants Sinapis alba and Arabidopsis thaliana. Plant Cell Physiol 43:684–688PubMedCrossRefGoogle Scholar
  15. Crone E, Miller E, Sala A (2009) How do plants know when other plants are flowering? Resource depletion, pollen limitation and mast-seeding in a perennial wildflower. Ecol Lett 12:1119–1126PubMedCrossRefGoogle Scholar
  16. Dickson RE (1991) Assimilate distribution and storage. In: Raghavendra AS (ed) Physiology of trees. Wiley-Interscience, New York, pp 51–85Google Scholar
  17. Drobyshev I, Övergaard R, Saygin I, Niklasson M, Hickler T, Karlsson M, Sykes MT (2010) Masting behaviour and dendrochronology of European beech (Fagus sylvatica L.) in southern Sweden. For Ecol Manag 259:2160–2171CrossRefGoogle Scholar
  18. Falkengren-Grerup U, Eriksson H (1990) Changes in soil, vegetation and forest yield between 1947 and 1988 in beech and oak sites of southern Sweden. For Ecol Manag 38:37–53CrossRefGoogle Scholar
  19. Farmer RE (1981) Variation in seed yield of white oak. For Sci 27:377–380Google Scholar
  20. Fenner M (1998) The phenology of growth and reproduction in plants. Perspect Plant Ecol Evol Syst 1:78–91CrossRefGoogle Scholar
  21. Han Q, Kabeya D, Iio A, Kakubari Y (2008) Masting in Fagus crenata and its influence on the nitrogen content and dry mass of winter buds. Tree Physiol 28:1269–1276PubMedCrossRefGoogle Scholar
  22. Han Q, Kabeya D, Hoch G (2011) Leaf traits, shoot growth and seed production in mature Fagus sylvatica trees after 8 years of CO2 enrichment. Ann Bot. doi:10.1093/aob/mcr082 (in press)
  23. Harper JL (1977) Population biology of plants. Academic Press, New YorkGoogle Scholar
  24. Hasegawa S, Koba K, Tayasu I, Takeda H, Haga H (2003) Carbon autonomy of reproductive shoots of Siberian alder (Alnus hirsuta var. sibirica). J Plant Res 116:183–188PubMedCrossRefGoogle Scholar
  25. Healy WM, Lewis AM, Boose EF (1999) Variation of red oak acorn production. For Ecol Manag 116:1–11CrossRefGoogle Scholar
  26. Hilton GM, Packham JR (1997) A sixteen-year record of regional and temporal variation in the fruiting of beech (Fagus sylvatica L.) in England (1980–1995). Forestry 70:7–16CrossRefGoogle Scholar
  27. Hilton GM, Packham JR (2003) Variation in the masting of common beech (Fagus sylvatica L.) in northern Europe over two centuries (1800–2001). Forestry 76:319–328CrossRefGoogle Scholar
  28. Hoch G (2005) Fruit-bearing branchlets are carbon autonomous in mature broad-leaved temperate forest trees. Plant Cell Environ 28:651–659CrossRefGoogle Scholar
  29. Hoch G, Keel SG (2006) 13C Labelling reveals different contributions of photoassimilates from infructescences for fruiting. Plant Biol 8:606–614PubMedCrossRefGoogle Scholar
  30. Hoch G, Richter A, Ch Körner (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081CrossRefGoogle Scholar
  31. Houle G (1999) Mast seeding in Abies balsamea, Acer saccharum and Betula alleghaniensis in an old growth, cold temperate forest of north-eastern North America. J Ecol 87:413–422CrossRefGoogle Scholar
  32. Ichie T, Kenta T, Nakagawa M, Sato K, Nakashizuka T (2005a) Resource allocation to reproductive organs during masting in the tropical emergent tree, Dipterocarpus tempehes. J Trop Ecol 21:237–241CrossRefGoogle Scholar
  33. Ichie T, Kenzo T, Kitahashi Y, Koike T, Nakashizuka T (2005b) How does Dryobalanops aromatica supply carbohydrate resources for reproduction in a masting year? Trees 19:703–710CrossRefGoogle Scholar
  34. Ims RA (1990) The ecology and evolution of reproductive synchrony. Trends Ecol Evol 5:135–140PubMedCrossRefGoogle Scholar
  35. Inouye DW (2000) The ecological and evolutionary significance of frost in the context of climate change. Ecol Lett 3:457–463CrossRefGoogle Scholar
  36. Isagi Y, Sugimura K, Sumida A, Ito H (1997) How does masting happen and synchronize? J Theor Biol 187:231–239CrossRefGoogle Scholar
  37. Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492CrossRefGoogle Scholar
  38. Janzen DH (1976) Why bamboos wait so long to flower. Annu Rev Ecol Syst 7:347–391CrossRefGoogle Scholar
  39. Karlsson PS (1994) The significance of internal nutrient cycling in branches for growth and reproduction of Rhododendron lapponicum. Oikos 70:191–200CrossRefGoogle Scholar
  40. Kelly D (1994) The evolutionary ecology of mast seeding. Trends Ecol Evol 9:465–470PubMedCrossRefGoogle Scholar
  41. Kelly D, Hart DE, Allen RB (2001) Evaluating the wind pollination benefits of mast seeding. Ecology 82:117–126CrossRefGoogle Scholar
  42. Koenig WD, Knops JMH (2000) Patterns of annual seed production by Northern Hemisphere trees: a global perspective. Am Nat 155:59–69PubMedCrossRefGoogle Scholar
  43. Koenig WD, Mumme RL, Carmen WJ, Stanback MK (1994) Acorn production by oaks in central coastal California: variation within and among years. Ecology 75:99–109CrossRefGoogle Scholar
  44. Kon H (2009) Is fluctuation of mast seeding predictable? In: Northern forestry in Japan: Q&A (the 60th anniversary publication of the foundation of Northern Forestry Association). Northern Forestry Association, Hokkaido, Japan, pp 52–53 (in Japanese)Google Scholar
  45. Kon H, Noda T (2007) Experimental investigation on weather cues for mast seeding of Fagus crenata. Ecol Res 22:802–806CrossRefGoogle Scholar
  46. Kon H, Noda T, Terazawa K, Koyama H, Yasaka M (2005) Proximate factors causing mast seeding in Fagus crenata: the effects of resource level and weather cues. Can J Bot 83:1402–1409CrossRefGoogle Scholar
  47. Körner Ch (2003) Carbon limitation in trees. J Ecol 91:4–17CrossRefGoogle Scholar
  48. Körner Ch, Asshoff R, Bignucolo O, Hättenschwiller S, Keel SG, Pelaez-Riedl S, Pepin S, Siegwolf RTW, Zotz G (2005) Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309:1360–1362PubMedCrossRefGoogle Scholar
  49. Lamlom SH, Savidge RA (2003) A reassessment of carbon content in wood: variation within and between 41 North American species. Biomass Bioenerg 25:381–388CrossRefGoogle Scholar
  50. Liberloo M, Tulva I, Raïm O, Kull O, Ceulemans R (2007) Photosynthetic stimulation under long-term CO2 enrichment and fertilization is sustained across a closed Populus canopy profile (EUROFACE). New Phytol 173:537–549PubMedCrossRefGoogle Scholar
  51. Lloyd DG (1980) Sexual strategies in plants. I. An hypothesis of serial adjustment of maternal investment during one reproductive session. New Phytol 86:69–79CrossRefGoogle Scholar
  52. Lloyd DG, Webb CJ (1977) Secondary sex characteristics in seed plants. Bot Rev 43:177–216CrossRefGoogle Scholar
  53. Lovett Doust J (1989) Plant reproductive strategies and resource allocation. Trends Ecol Evol 4:230–234PubMedCrossRefGoogle Scholar
  54. Lovett Doust J, Lovett Doust L (1988) Modules of reproduction and reproduction in a dioecious clonal shrub, Rhus typhina. Ecology 69:741–750CrossRefGoogle Scholar
  55. Masaka K, Maguchi S (2001) Modeling the masting behaviour of Betula platyphylla var. japonica using the resource budget model. Ann Bot 88:1049–1055CrossRefGoogle Scholar
  56. Maynard Smith J (1976) Evolution and the theory of games. Am Sci 64:41–45Google Scholar
  57. McKone MJ, Kelly D, Lee WG (1998) Effect of climate change on mast-seeding species: frequency of mass flowering and escape from specialist insect seed predators. Glob Change Biol 4:591–596CrossRefGoogle Scholar
  58. Miyazaki Y, Hiura T, Kato E, Funada R (2002) Allocation of resources to reproduction in Styrax obassia in a masting year. Ann Bot 89:767–772PubMedCrossRefGoogle Scholar
  59. Miyazaki Y, Hiura T, Funada R (2007) Allocation of photo-assimilated 13C from reproductive and non-reproductive shoots to fruits in Styrax obassia. Plant Species Biol 22:53–57CrossRefGoogle Scholar
  60. Miyazaki Y, Osawa T, Waguchi Y (2009) Resource level as a proximate factor influencing fluctuations in male flower production in Cryptomeria japonica D. Don. J For Res 14:358–364CrossRefGoogle Scholar
  61. Monks A, Kelly D (2006) Testing the resource-matching hypothesis in the mast seeding tree Nothofagus truncata (Fagaceae). Austral Ecol 31:366–375CrossRefGoogle Scholar
  62. Nakamura M, Muller O, Tayanagi S, Nakaji T, Hiura T (2010) Experimental branch warming alters tall tree leaf phenology and acorn production. Agr For Met 150:1026–1029CrossRefGoogle Scholar
  63. Neilson RP, Wullstein LH (1980) Catkin freezing and acorn production in Gambel oak in Utah, 1978. Am J Bot 67:426–428CrossRefGoogle Scholar
  64. Newell E (1991) Direct and delayed costs of reproduction in Aesculus californica. J Ecol 79:365–378CrossRefGoogle Scholar
  65. Nilsson SG, Wästljung U (1987) Seed predation and cross-pollination in mast-seeding beech (Fagus sylvatica) patches. Ecology 68:260–265CrossRefGoogle Scholar
  66. Norton DA, Kelly D (1988) Mast seedeing over 33 years by Dacrydium cupressinum Lamb. (rimu) (Podocarpaceae) in New Zealand: the importance of economics of scale. Funct Ecol 2:399–408CrossRefGoogle Scholar
  67. Numata S, Yasuda M, Okuda T, Kachi N, Noor NSM (2003) Temporal and spatial patterns of mass flowerings on the Malay Peninsula. Am J Bot 90:1025–1031PubMedCrossRefGoogle Scholar
  68. Obeso JR (1998) Effects of defoliation and girdling on fruit production in Ilex aquifolium. Funct Ecol 12:486–491CrossRefGoogle Scholar
  69. Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348CrossRefGoogle Scholar
  70. Ohto M, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K (2001) Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiol 127:252–261PubMedCrossRefGoogle Scholar
  71. Övergaard R, Gemmel P, Karlsson M (2007) Effects of weather conditions on mast year frequency in beech (Fagus sylvatica L.) in Sweden. Forestry 80:553–563CrossRefGoogle Scholar
  72. Perez-Ramos IM, Ourcival JM, Limousin JM, Rambal S (2010) Mast seeding under increasing drought: results from a long-term data set and from a rainfall exclusion experiment. Ecology 91:3057–3068PubMedCrossRefGoogle Scholar
  73. Piovesan G, Adams JM (2001) Masting behaviour in beech: linking reproduction and climatic variation. Can J Bot 79:1039–1047Google Scholar
  74. Rees M, Kelly D, Bjørnstad ON (2002) Snow tussocks, chaos, and the evolution of mast seeding. Am Nat 160:44–59PubMedCrossRefGoogle Scholar
  75. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267CrossRefGoogle Scholar
  76. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709PubMedCrossRefGoogle Scholar
  77. Satake A, Iwasa Y (2000) Pollen coupling of forest trees: forming synchronized and periodic reproduction out of chaos. J Theor Biol 203:63–84PubMedCrossRefGoogle Scholar
  78. Satake A, Iwasa Y (2002a) Spatially limited pollen exchange and a long-range synchronization of trees. Ecology 83:993–1005CrossRefGoogle Scholar
  79. 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 90:830–838CrossRefGoogle Scholar
  80. Sauter JJ, van Cleve B (1991) Biochemical and ultrastructural results during starch-sugar-conversion in ray cells of Populus during cold adaptation. J Plant Physiol 139:19–26CrossRefGoogle Scholar
  81. Schauber EM, Turchin P, Simon C, Kelly D, Lee WG, Allen RB, Payton IJ, Wilson PR, Cowan PE, Brockie RE (2002) Masting by eighteen New Zealand plant species: the role of temperature as a synchronizing cue. Ecology 83:1214–1225CrossRefGoogle Scholar
  82. Selas V (2000) Seed production of a masting dwarf shrub, Vaccinium myrtillus, in relation to previous reproduction and weather. Can J Bot 78:423–429Google Scholar
  83. Sharp WM, Chisman HH (1961) Flowering and fruiting in the white oaks. I. Staminate flowering through pollen dispersal. Ecology 42:365–372CrossRefGoogle Scholar
  84. Sharp WM, Sprague VG (1967) Flowering and fruiting in the white oaks: pistillate flowering, acorn development, weather, and yields. Ecology 48:243–251CrossRefGoogle Scholar
  85. Silvertown JW (1980) The evolutionary ecology of mast seeding in trees. Biol J Linn Soc Lond 14:235–250CrossRefGoogle Scholar
  86. Smith CC, Hamrick JL, Kramer CL (1990) The advantage of mast years for wind pollination. Am Nat 136:154–166CrossRefGoogle Scholar
  87. Sohn JJ, Policansky D (1977) The costs of reproduction in the Mayapple Podophyllum Peltatum (Berberidaceae). Ecology 58:1366–1374CrossRefGoogle Scholar
  88. Sork VL, Bramble JE (1993) Prediction of acorn crops in three species of North American oaks Quercus alba, Q rubra, and Q velutina. Ann Sci For 50(Suppl 1):128–136CrossRefGoogle Scholar
  89. Sork VL, Bramble JE, Sexton O (1993) Ecology of mast-fruiting in three species of North American deciduous oaks. Ecology 74:528–541CrossRefGoogle Scholar
  90. Sprugel DG, Hinckley TM, Schaap W (1991) The theory and practice of branch autonomy. Annu Rev Ecol Syst 22:309–334CrossRefGoogle Scholar
  91. Suzuki W, Osumi K, Masaki T (2005) Mast seeding and its spatial scale in Fagus crenata in northern Japan. For Ecol Manag 205:105–116CrossRefGoogle Scholar
  92. Tuomi J, Niemela P, Mannila R (1982) Resource allocation on dwarf shoots of birch (Betula pendula): reproduction and leaf growth. New Phytol 91:483–487CrossRefGoogle Scholar
  93. Tuomi J, Vuorisalo T, Niemela P, Nisula S, Jormalainen V (1988) Localized effects of branch defoliations on weight gain of female inflorescences in Betula pubescens. Oikos 51:327–330CrossRefGoogle Scholar
  94. Williamson MJ (1966) Premature abscissions in white oak acorn crops. For Sci 12:19–21Google Scholar
  95. Wolgast LJ, Trout JR (1979) Late spring frost affects yields of bear oak acorns. J Wild Manag 43:239–240CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2011

Authors and Affiliations

  1. 1.Creative Research Initiative SouseiHokkaido UniversitySapporoJapan
  2. 2.Graduate School of Environmental ScienceOkayama UniversityOkayamaJapan

Personalised recommendations