The effects of defoliation on carbon allocation: Can carbon limitation reduce growth in favour of storage?

Tree Physiology

Volumn 33, Issue 11, 2013, Pages 1216-1228

  Wiley, Erin ^a   Huepenbecker, Sarah ^b   Casper, Brenda B ^a   Helliker, Brent R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Carbon reserves; Non structural carbon; Tree growth

Indexed keywords

BIOMASS; BIOMASS ALLOCATION; CARBON; DEFOLIATION; GROWTH RATE; LEAF AREA; SURVIVAL; TREE; WATER AVAILABILITY;

CARBON; NITROGEN;

ARTICLE; CARBON RESERVES; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NON-STRUCTURAL CARBON; OAK; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; PLANT STEM; SEEDLING; TREE; TREE GROWTH; WOOD;

CARBON RESERVES; NON-STRUCTURAL CARBON; TREE GROWTH;

CARBON; NITROGEN; PHOTOSYNTHESIS; PLANT LEAVES; PLANT STEMS; QUERCUS; SEEDLING; TREES; WOOD;

EID: 84890295202     PISSN: 0829318X     EISSN: 17584469     Source Type: Journal    
DOI: 10.1093/treephys/tpt093     Document Type: Article

References (68)

1. Baud S, Boutin JP, Miquel M, Lepiniec L, Rochat C (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 40:151-160.
2. Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63:625-644.
3. Calfapietra C, Tulva I, Eensalu E, Perez M, De Angelis P, Scarascia-Mugnozza G, Kull O (2005) Canopy profiles of photosynthetic parameters under elevated CO2 and N fertilization in a poplar plantation. Environ Pollut 137:525-535.
4. Canham C, Kobe R, Latty E, Chazdon R (1999) Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia 121:1-11.
5. Chapin F, Schultz E, Mooney H (1990) The ecology and economics of storage in plants. Ann Rev Ecol Syst 21:423-447.
6. Delaney KJ, Haile FJ, Peterson RKD, Higley LG (2008) Impairment of leaf photosynthesis after insect herbivory or mechanical injury on-common milkweed, Asclepias syriaca. Environ Entomol 37: 1332-1343.
7. Ephron B (1981) Nonparametric estimates of standard error: the jackknife, the bootstrap and other methods. Biometrika 68:589-599.
8. Ericsson A, Larsson S, Tenow O (1980) Effects of early and late season defoliation on growth and carbohydrate dynamics in Scots pine. J Appl Ecol 17:747-769.
9. Eyles A, Pinkard EA, Mohammed C (2009) Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Physiol 29:753-764.
10. Eyles A, Smith D, Pinkard E, Smith I, Corkrey R, Elms S, Beadle C, Mohammed C (2011) Photosynthetic responses of field-grown Pinus radiata trees to artificial and aphid-induced defoliation. Tree Physiol 31:592-603.
11. Freeman RS, Brody AK, Neefus CD (2003) Flowering phenology and compensation for herbivory in Ipomopsis aggregata. Oecologia 136:394-401.
12. Fu X, Harberd N (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740-743.
13. Galiano L, Martínez-Vilalta J, Lloret F (2011) Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode. New Phytol 190:750-759.
14. Galvez DA, Landhäusser SM, Tyree MT (2011) Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation? Tree Physiol 31:250-257.
15. Gibon Y, Pyl E, Sulpice R, Lunn J, Hohne M, Gunther M, Stitt M (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ 32:859-874.
16. Gleason S, Ares A (2004) Photosynthesis, carbohydrate storage and survival of a native and an introduced tree species in relation to light and defoliation. Tree Physiol 24:1087-1097.
17. Handa I, Körner C, Hattenschwiler S (2005) A test of the tree-line carbon limitation hypothesis by in situ CO2 enrichment and defoliation. Ecology 86:1288-1300.
18. Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067-1081.
19. Hoogesteger J, Karlsson P (1992) Effects of defoliation on radial stem growth and photosynthesis in the mountain birch (Betula pubescens ssp. tortuosa). Funct Ecol 6:317-323.
20. Huttunen L, Niemelä P, Peltola H, Heiska S, Rousi M, Kellomäki S (2007) Is a defoliated silver birch seedling able to overcompensate the growth under changing climate? Environ Exp Bot 60:227-238.
21. Imaji A, Seiwa K (2010) Carbon allocation to defense, storage, and growth in seedlings of two temperate broad-leaved tree species. Oecologia 162:273-281.
22. Keskitalo J, Bergquist G, Gardeström P, Jansson S (2005) A cellular timetable of autumn senescence. Plant Physiol 139:1635-1648.
23. Knops JMH, Reinhart K (2000) Specific leaf area along a nitrogen fertilization gradient. Am Midl Nat 144:265-272.
24. Körner C (2003) Carbon limitation in trees. J Ecol 91:4-17.
25. Kruger EL, Volin JC, Lindroth RL (1998) Influences of atmospheric CO2 enrichment on the responses of sugar maple and trembling aspen to defoliation. New Phytol 140:85-94.
26. Lacointe A, Deleens E, Ameglio T, Saint-joanis B, Lelarge C, Vandame M, Song GC, Daudet FA (2004) Testing the branch autonomy theory: a 13C/14C double-labelling experiment on differentially shaded branches. Plant Cell Environ 27:1159-1168.
27. Langstrom B, Tenow O, Ericsson A, Hellqvist C, Larsson S (1990) Effects of shoot pruning on stem growth, needle biomass, and dynamics of carbohydrates and nitrogen in Scots pine as related to season and tree age. Can J For Res 20:514-523.
28. Le Roux X, Lacointe A, Escobar-Gutierrez A, Le Dizes S (2001) Carbon-based models of individual tree growth: a critical appraisal. Ann For Sci 58:469-506.
29. Li M, Hoch G, Körner C (2002) Source/sink removal affects mobile carbohydrates in Pinus cembra at the Swiss treeline. Trees 16: 331-337.
30. Lilley JLS, Gee CW, Sairanen I, Ljung K, Nemhauser JL (2012) An endogenous carbon-sensing pathway triggers increased auxin flux and hypocotyl elongation. Plant Physiol 160:2261-2270.
31. Markkola A, Kuikka K, Rautio P, Härmä E, Roitto M, Tuomi J (2004) Defoliation increases carbon limitation in ectomycorrhizal symbiosis of Betula pubescens. Oecologia 140:234-240.
32. Mattson WJ, Kuokkanen K, Niemelä P, Julkunen-Tiitto R, Kellomäki S, Tahvanainen J (2004) Elevated CO2 alters birch resistance to Lagomorpha herbivores. Glob Change Biol 10:1402-1413.
33. McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155: 1051-1059.
34. McDowell NG, Sevanto S (2010) The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytol 186:264-266.
35. Millard P, Hester A, Wendler R, Baillie G (2001) Interspecific defoliation responses of trees depend on sites of winter nitrogen storage. Funct Ecol 15:535-543.
36. Myers J, Kitajima K (2007) Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. J Ecol 95: 383-395.
37. Nasholm T (1994) Removal of nitrogen during needle senescence in Scots pine (Pinus sylvestris L.). Oecologia 99:290-296.
38. Palacio S, Hester A, Maestro M, Millard P (2008) Browsed Betula pubescens trees are not carbon-limited. Funct Ecol 22:808-815.
39. Palacio S, Hernández R, Maestro-Martínez M, Camarero J (2012) Fast replenishment of initial carbon stores after defoliation by the pine processionary moth and its relationship to the re-growth ability of trees. Trees 26:1627-1640.
40. Palacio S, Hester AJ, Maestro M, Millard P (2013) Simulated browsing affects leaf shedding phenology and litter quality of oak and birch saplings. Tree Physiol 33:438-445.
41. Pinkard E, Battaglia M, Mohammed C (2007) Defoliation and nitrogen effects on photosynthesis and growth of Eucalyptus globules. Tree Physiol 27:1053-1063.
42. Piper FI (2011) Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen Nothofagus species of differential drought resistance. Ann For Sci 68:415-424.
43. Reed R, Brady S, Muday G (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiol 118:1369-1378.
44. Reich PB, Teskey RO, Johnson PS, Hinckley TM (1980) Periodic root and shoot growth in oak. For Sci 26:590-598.
45. Reichenbacker R, Schultz R, Hart E (1996) Artificial defoliation effect on Populus growth, biomass production, and total nonstructural carbohydrate concentration. Environ Entomol 25:632-642.
46. Ryan MG (2011) Tree responses to drought. Tree Physiol 31: 237-239.
47. Sala A, Hoch G (2009) Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant Cell Environ 32:22-30.
48. Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32:764-775.
49. Salemaa M, Jukola-Sulonen E (1990) Vitality rating of Picea abies by defoliation class and other vigour indicators. Scand J For Res 5:413-426.
50. Sanz-Pérez V, Castro-Díez P, Joffre R (2009) Seasonal carbon storage and growth in Mediterranean tree seedlings under different water conditions. Tree Physiol 29:1105-1116.
51. Silpi U, Lacointe A, Kasempsap P et al. (2007) Carbohydrate reserves as a competing sink: evidence from tapping rubber trees. Tree Physiol 27:881-889.
52. Smith A, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126-1149.
53. Snyder KA, Williams DG (2007) Root allocation and water uptake patterns in riparian tree saplings: Responses to irrigation and defoliation. For Ecol Manag 246:222-231.
54. Susiluoto S, Hilasvuori E, Berninger F (2010) Testing the growth limitation hypothesis for subarctic Scots pine. J Ecol 98:1186-1195.
55. Tuomi J, Niemela P, Siren S (1990) The Panglossian paradigm and delayed inducible accumulation of foliar phenolics in mountain birch. Oikos 59:399-410.
56. VanArendonk J, Niemann GJ, Boon JJ, Lambers H (1997) Effects of nitrogen supply on the anatomy and chemical composition of leaves of four grass species belonging to the genus Poa, as determined by image-processing analysis and pyrolysis mass spectrometry. Plant Cell Environ 20:881-897.
57. Van der Heyden F, Stock W (1995) Nonstructural carbohydrate allocation following different frequencies of simulated browsing in three semiarid shrubs. Oecologia 102:238-245.
58. Vanderklein D, Reich P (1999) The effect of defoliation intensity and history on photosynthesis, growth and carbon reserves of two conifers with contrasting leaf lifespans and growth habits. New Phytol 144:121-132.
59. Volin JC, Kruger EL, Lindroth RL (2002) Responses of deciduous broadleaf trees to defoliation in a CO2 enriched atmosphere. Tree Physiol 22:435-448.
60. Watson D, Loach K, Motomats T, Milford G (1972) Effects of shading and of seasonal differences in weather on growth, sugar content and sugar yield of sugar-beet crops. Ann Appl Biol 71:159-185.
61. Webb W (1981) Relation of starch content to content to conifer mortality and growth loss after defoliation by the Douglas-Fir Tussock Moth. For Sci 27:224-232.
62. Wiley E, Helliker B (2012) A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol 195:285-289.
63. Willaume M, Pagès L (2006) How periodic growth pattern and source/sink relations affect growth in oak tree seedlings. J Exp Bot 57: 815-826.
64. Willaume M, Pagès L (2011) Correlated responses of root growth and sugar concentrations to various defoliation treatments and rhythmic shoot growth in oak tree seedlings (Quercus pubescens). Ann Bot 107:653-662.
65. Würth MKR, Peláez-Riedl S, Wright SJ, Körner C (2005) Non-structural carbohydrate pools in a tropical forest. Oecologia 143:11-24.
66. Yang L, Conway S, Poethig RS (2011) Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156. Development 138:245-249.
67. Yang L, Xu M, Koo Y, He J, Poethig RS (2013) Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. eLife 2:e00260.
68. Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum MR, de Lucia EH (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proc Natl Acad Sci USA 99:1088-1091.