The role of nutrients in drought-induced tree mortality and recovery

New Phytologist

Volumn 214, Issue 2, 2017, Pages 513-520

  Gessler, Arthur ^a   Schaub, Marcus ^a   McDowell, Nate G ^b  

^a SWISS FEDERAL RESEARCH INSTITUTE WSL   (Switzerland)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

Birch effect; carbon starvation; feedbacks; hydraulic failure; nitrogen; predisposition; tree height

Indexed keywords

BIOMASS ALLOCATION; CARBON BALANCE; DROUGHT; ECOSYSTEM RESPONSE; FEEDBACK MECHANISM; FOREST ECOSYSTEM; HEIGHT; MICROBIAL ACTIVITY; MORTALITY; NITROGEN; NUTRIENT AVAILABILITY; NUTRIENT BUDGET; PHOTOSYNTHESIS; PHYSIOLOGY; TREE; WATER USE EFFICIENCY;

CARBON; NITROGEN; PHOSPHORUS; WATER;

DROUGHT; METABOLISM; PHYSIOLOGY; TREE;

CARBON; DROUGHTS; NITROGEN; PHOSPHORUS; TREES; WATER;

EID: 85006307263     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14340     Document Type: Review

References (70)

1. Allen CD, Breshears DD, McDowell NG. 2015. On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6: 129.
2. Anderegg WRL, Flint A, C-y Huang, Flint L, Berry JA, Davis FW, Sperry JS, Field CB. 2015. Tree mortality predicted from drought-induced vascular damage. Nature Geoscience 8: 367–371.
3. Arquero O, Barranco D, Benlloch M. 2006. Potassium starvation increases stomatal conductance in olive trees. HortScience 41: 433–436.
4. Ashraf M, Foolad MR. 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59: 206–216.
5. Badri DV, Vivanco JM. 2009. Regulation and function of root exudates. Plant, Cell & Environment 32: 666–681.
6. Bigler C, Bräker OU, Bugmann H, Dobbertin M, Rigling A. 2006. Drought as an Inciting mortality factor in Scots pine stands of the Valais, Switzerland. Ecosystems 9: 330–343.
7. Birch HF. 1964. Mineralisation of plant nitrogen following alternate wet and dry conditions. Plant and Soil 20: 43–49.
8. Borken W, Matzner E. 2009. Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Global Change Biology 15: 808–824.
9. Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752–755.
10. Coomes DA, Jenkins KL, Cole LES. 2007. Scaling of tree vascular transport systems along gradients of nutrient supply and altitude. Biology Letters 3: 87–90.
11. 2 and nitrogen in transgenic cotton plants. Journal of Experimental Botany 53: 323–331.
12. Craine JM, Engelbrecht BMJ, Lusk CH, McDowell NG, Poorter H. 2012. Resource limitation, tolerance, and the future of ecological plant classification. Frontiers in Plant Science 3: 246.
13. Cregger MA, McDowell NG, Pangle RE, Pockman WT, Classen AT. 2014. The impact of precipitation change on nitrogen cycling in a semi-arid ecosystem. Functional Ecology 28: 1534–1544.
14. Demchik MC, Sharpe WE. 2000. The effect of soil nutrition, soil acidity and drought on northern red oak (Quercus rubra L.) growth and nutrition on Pennsylvania sites with high and low red oak mortality. Forest Ecology and Management 136: 199–207.
15. 2O emissions from Ugandan agroforest soils. Phyton 41: 73–80.
16. Dietze MC, Moorcroft PR. 2011. Tree mortality in the eastern and central United States: patterns and drivers. Global Change Biology 17: 3312–3326.
17. Dziedek C, von Oheimb G, Calvo L, Fichtner A, Kriebitzsch WU, Marcos E, Pitz WT, Hardtle W. 2016. Does excess nitrogen supply increase the drought sensitivity of European beech (Fagus sylvatica L.) seedlings? Plant Ecology 217: 393–405.
18. Egilla JN, Davies FT, Boutton TW. 2005. Drought stress influences leaf water content, photosynthesis, and water-use efficiency of Hibiscus rosa-sinensis at three potassium concentrations. Photosynthetica 43: 135–140.
19. Ewers BE, Oren R, Sperry JS. 2000. Influence of nutrient versus water supply on hydraulic architecture and water balance in Pinus taeda. Plant, Cell & Environment 23: 1055–1066.
20. Fangmeier A, Hadwiger-Fangmeier A, Van der Eerden L, Jäger H-J. 1994. Effects of atmospheric ammonia on vegetation – a review. Environmental Pollution 86: 43–82.
21. Fisher JB, Badgley G, Blyth E. 2012. Global nutrient limitation in terrestrial vegetation. Global Biogeochemical Cycles 26: GB3007.
22. 15N uptake and partitioning, responses of amino acids and other N compounds. Plant Biology 4: 311–320.
23. Franklin JF, Shugart HH, Harmon ME. 1987. Tree death as an ecological process. BioScience 37: 550–556.
24. Gessler A, Jung K, Gasche R, Papen H, Heidenfelder A, Borner E, Metzler B, Augustin S, Hildebrand E, Rennenberg H. 2005. Climate and forest management influence nitrogen balance of European beech forests: microbial N transformations and inorganic N net uptake capacity of mycorrhizal roots. European Journal of Forest Research 124: 95–111.
25. Gessler A, Keitel C, Nahm M, Rennenberg H. 2004. Water shortage affects the water and nitrogen balance in central European beech forests. Plant Biology 6: 289–298.
26. Gessler A, Kreuzwieser J, Dopatka T, Rennenberg H. 2002. Diurnal courses of ammonium net uptake by the roots of adult beech (Fagus sylvatica) and spruce (Picea abies) trees. Plant and Soil 240: 23–32.
27. Ghashghaie J, Saugier B. 1989. Effects of nitrogen deficiency on leaf photosynthetic response of tall fescue to water deficit. Plant, Cell & Environment 12: 261–271.
28. Goldstein G, Bucci SJ, Scholz FG. 2013. Why do trees adjust water relations and hydraulic architecture in response to nutrient availability? Tree Physiology 33: 238–240.
29. Hacke UG, Plavcová L, Almeida-Rodriguez A, King-Jones S, Zhou W, Cooke JEK. 2010. Influence of nitrogen fertilization on xylem traits and aquaporin expression in stems of hybrid poplar. Tree Physiology 30: 1016–1025.
30. Hartmann H, Ziegler W, Kolle O, Trumbore S. 2013. Thirst beats hunger – declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytologist 200: 340–349.
31. Heckathorn SA, DeLucia EH, Zielinski RE. 1997. The contribution of drought-related decreases in foliar nitrogen concentration to decreases in photosynthetic capacity during and after drought in prairie grasses. Physiologia Plantarum 101: 173–182.
32. Hentschel R, Rosner S, Kayler ZE, Andreassen K, Børja I, Solberg S, Tveito OE, Priesack E, Gessler A. 2014. Norway spruce physiological and anatomical predisposition to dieback. Forest Ecology and Management 322: 27–36.
33. Hodge A, Robinson D, Fitter A. 2000. Are microorganisms more effective than plants at competing for nitrogen? Trends in Plant Science 5: 304–308.
34. Högberg P, Fan H, Quist M, Binkley DAN, Tamm CO. 2006. Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Global Change Biology 12: 489–499.
35. Hommel R, Siegwolf R, Zavadlav S, Arend M, Schaub M, Galiano L, Haeni M, Kayler ZE, Gessler A. 2016. Impact of interspecific competition and drought on the allocation of new assimilates in trees. Plant Biology 18: 785–796.
36. Jarvis P, Rey A, Petsikos C, Wingate L, Rayment M, Pereira J, Banza J, David J, Miglietta F, Borghetti M et al. 2007. Drying and wetting of Mediterranean soils stimulates decomposition and carbon dioxide emission: the “Birch effect”. Tree Physiology 27: 929–940.
37. Jonard M, Fürst A, Verstraeten A, Thimonier A, Timmermann V, Potočić N, Waldner P, Benham S, Hansen K, Merilä P et al. 2014. Tree mineral nutrition is deteriorating in Europe. Global Change Biology 21: 418–430.
38. Kozlowski T, Pallardy S. 2002. Acclimation and adaptive responses of woody plants to environmental stresses. Botanical Review 68: 270–334.
39. Kreuzwieser J, Gessler A. 2010. Global climate change and tree nutrition: influence of water availability. Tree Physiology 30: 1221–1234.
40. Lloret F, Escudero A, Iriondo JM, Martínez-Vilalta J, Valladares F. 2012. Extreme climatic events and vegetation: the role of stabilizing processes. Global Change Biology 18: 797–805.
41. Magill AH, Aber JD, Currie WS, Nadelhoffer KJ, Martin ME, McDowell WH, Melillo JM, Steudler P. 2004. Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA. Forest Ecology and Management 196: 7–28.
42. Manion PD. 1981. Tree disease concepts. Englewood Cliffs, NJ, USA: Prentice-Hall Inc.
43. Marschner H, Kirkby EA, Cakmak I. 1996. Effect of mineral nutritional status on shoot–root partitioning of photoassimilates and cycling of mineral nutrients. Journal of Experimental Botany 47: 1255–1263.
44. Martínez-Vilalta J, Piñol J, Beven K. 2002. A hydraulic model to predict drought-induced mortality in woody plants: an application to climate change in the Mediterranean. Ecological Modelling 155: 127–147.
45. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG et al. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178: 719–739.
46. McDowell NG. 2011. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology 155: 1051–1059.
47. McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M. 2011. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends in Ecology & Evolution 26: 523–532.
48. McDowell NG, Fisher RA, Xu C, Domec JC, Hölttä T, Mackay DS, Sperry JS, Boutz A, Dickman L, Gehres N et al. 2013. Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. New Phytologist 200: 304–321.
49. Millard P, Proe MF. 1992. Storage and internal cycling of nitrogen in relation to seasonal growth of Sitka spruce. Tree Physiology 10: 33–43.
50. Muhr J, Franke J, Borken W. 2010. Drying–rewetting events reduce C and N losses from a Norway spruce forest floor. Soil Biology and Biochemistry 42: 1303–1312.
51. 2-enriched atmosphere. Nature 411: 469–472.
52. Rennenberg H, Dannenmann M. 2015. Nitrogen nutrition of trees in temperate forests—the significance of nitrogen availability in the pedosphere and atmosphere. Forests 6: 2820–2835.
53. Royo AA, Knight KS. 2012. White ash (Fraxinus americana) decline and mortality: the role of site nutrition and stress history. Forest Ecology and Management 286: 8–15.
54. Sala A, Piper F, Hoch G. 2010. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytologist 186: 274–281.
55. Sardans J, Alonso R, Janssens IA, Carnicer J, Vereseglou S, Rillig MC, Fernández Martínez M, Sanders TGM, Peñuelas J. 2015. Foliar and soil concentrations and stoichiometry of nitrogen and phosphorous across European Pinus sylvestris forests: relationships with climate, N deposition and tree growth. Functional Ecology 30: 676–689.
56. Sardans J, Peñuelas J. 2013. Tree growth changes with climate and forest type are associated with relative allocation of nutrients, especially phosphorus, to leaves and wood. Global Ecology and Biogeography 22: 494–507.
57. Sardans J, Peñuelas J. 2015. Potassium: a neglected nutrient in global change. Global Ecology and Biogeography 24: 261–275.
58. Schulze ED. 1989. Air pollution and forest decline in a spruce (Picea abies) forest. Science 244: 776–783.
59. Sergent AS, Rozenberg P, Breda N. 2014. Douglas-fir is vulnerable to exceptional and recurrent drought episodes and recovers less well on less fertile sites. Annals of Forest Science 71: 697–708.
60. Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT. 2014. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell & Environment 37: 153–161.
61. Sperry JS, Love DM. 2015. What plant hydraulics can tell us about responses to climate-change droughts. New Phytologist 207: 14–27.
62. Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13: 87–115.
63. Volkmann THM, Haberer K, Gessler A, Weiler M. 2016. High-resolution isotope measurements resolve rapid ecohydrological dynamics at the soil–plant interface. New Phytologist 201: 839–849.
64. Wallander H, Nylund JE. 1992. Effects of excess nitrogen and phosphorus starvation on the extramatrical mycelium of ectomycorrhizas of Pinus sylvestris L. New Phytologist 120: 495–503.
65. Wang WF, Peng CH, Kneeshaw DD, Larocque GR, Luo ZB. 2012. Drought-induced tree mortality: ecological consequences, causes, and modeling. Environmental Reviews 20: 109–121.
66. Waring RH. 1987. Characteristics of trees predisposed to die. BioScience 37: 569–574.
67. Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE et al. 2011. Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92: 1616–1625.
68. Wu F, Bao W, Li F, Wu N. 2008. Effects of drought stress and N supply on the growth, biomass partitioning and water-use efficiency of Sophora davidii seedlings. Environmental and Experimental Botany 63: 248–255.
69. Xiong Y, D'Atri JJ, Fu S, Xia H, Seastedt TR. 2011. Rapid soil organic matter loss from forest dieback in a subalpine coniferous ecosystem. Soil Biology and Biochemistry 43: 2450–2456.
70. Zwieniecki MA, Holbrook NM. 2009. Confronting Maxwell's demon: biophysics of xylem embolism repair. Trends in Plant Science 14: 530–534.