Responses of sapwood ray parenchyma and non-structural carbohydrates of Pinus sylvestris to drought and long-term irrigation

Functional Ecology

Volumn 31, Issue 7, 2017, Pages 1371-1382

  von Arx, Georg ^a,b   Arzac, Alberto ^c,d   Fonti, Patrick ^a,b   Frank, David ^a,b,e   Zweifel, Roman ^a,b   Rigling, Andreas ^a,b   Galiano, Lucia ^a   Gessler, Arthur ^a,b   Olano, José Miguel ^f  

^a SWISS FEDERAL RESEARCH INSTITUTE WSL   (Switzerland)

^b Swiss National Research Institute for Forest Snow and Landscape   (Switzerland)

^c SIBERIAN FEDERAL UNIVERSITY   (Russian Federation)

^d UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^e UNIVERSITY OF ARIZONA   (United States)

^f UNIVERSITY OF VALLADOLID   (Spain)

Author keywords

carbon allocation; drought stress; growth vs. storage; ring width autocorrelation; structure function relationships; tree ring anatomy; xylem anatomy; xylem rays

Indexed keywords

ANATOMY; AUTOCORRELATION; BIOMASS ALLOCATION; CARBOHYDRATE; CELLS AND CELL COMPONENTS; CONIFEROUS TREE; DROUGHT STRESS; ECOSYSTEM RESILIENCE; GROWTH; IRRIGATION; PHYSIOLOGICAL RESPONSE; STEM; SURVIVAL; TREE RING; WATER AVAILABILITY;

SWITZERLAND;

PINUS SYLVESTRIS;

EID: 85017415723     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12860     Document Type: Article

References (100)

1. Adams, H.D., Germino, M.J., Breshears, D.D., Barron-Gafford, G.A., Guardiola-Claramonte, M., Zou, C.B. & Huxman, T.E. (2013) Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism. New Phytologist, 197, 1142–1151.
2. Allen, C.D., Macalady, A.K., Chenchouni, H. et al. (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management, 259, 660–684.
3. Anderegg, W.R.L. & Anderegg, L.D.L. (2013) Hydraulic and carbohydrate changes in experimental drought-induced mortality of saplings in two conifer species. Tree Physiology, 33, 252–260.
4. Arbellay, E., Fonti, P. & Stoffel, M. (2012) Duration and extension of anatomical changes in wood structure after cambial injury. Journal of Experimental Botany, 63, 3271–3277.
5. Arbellay, E., Stoffel, M. & Bollschweiler, M. (2010) Wood anatomical analysis of Alnus incana and Betula pendula injured by a debris-flow event. Tree Physiology, 30, 1290–1298.
6. Arbellay, E., Stoffel, M., Sutherland, E.K., Smith, K.T. & Falk, D.A. (2014) Changes in tracheid and ray traits in fire scars of North American conifers and their ecophysiological implications. Annals of Botany, 114, 223–232.
7. von Arx, G., Archer, S.R. & Hughes, M.K. (2012) Long-term functional plasticity in plant hydraulic architecture in response to supplemental moisture. Annals of Botany, 109, 1091–1100.
8. von Arx, G. & Carrer, M. (2014) ROXAS – a new tool to build centuries-long tracheid-lumen chronologies in conifers. Dendrochronologia, 32, 290–293.
9. von Arx, G. & Dietz, H. (2005) Automated image analysis of annual rings in the roots of perennial forbs. International Journal of Plant Sciences, 166, 723–732.
10. von Arx, G., Arzac, A., Olano, J.M. & Fonti, P. (2015) Assessing conifer ray parenchyma for ecological studies: pitfalls and guidelines. Frontiers in Plant Science, 6, 1016.
11. von Arx, G., Crivellaro, A., Prendin, A.L., Čufar, K. & Carrer, M. (2016) Quantitative wood anatomy—practical guidelines. Frontiers in Plant Science, 7, 781.
12. Bamber, R.K. (1976) Heartwood, its function and formation. Wood Science and Technology, 10, 1–8.
13. Barton, K. (2016) MuMIn: Multi-Model Inference. R package version 1.15.6. Available at: http://CRAN.R-project.org/package=MuMIn (accessed 13 December 2016).
14. van Bel, A.J.E. (1990) Xylem-phloem exchange via the rays: the undervalued route of transport. Journal of Experimental Botany, 41, 631–644.
15. Breda, 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. Annals of Forest Science, 63, 625–644.
16. Brodersen, C.R. & McElrone, A.J. (2013) Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Frontiers in Plant Science, 4, 108.
17. Brunner, I., Pannatier, E.G., Frey, B., Rigling, A., Landolt, W., Zimmermann, S. & Dobbertin, M. (2009) Morphological and physiological responses of Scots pine fine roots to water supply in a dry climatic region in Switzerland. Tree Physiology, 29, 541–550.
18. Burgert, I. & Eckstein, D. (2001) The tensile strength of isolated wood rays of beech (Fagus sylvatica L.) and its significance for the biomechanics of living trees. Trees-Structure and Function, 15, 168–170.
19. Carbone, M.S., Czimczik, C.I., Keenan, T.F., Murakami, P.F., Pederson, N., Schaberg, P.G., Xu, X. & Richardson, A.D. (2013) Age, allocation and availability of nonstructural carbon in mature red maple trees. New Phytologist, 200, 1145–1155.
20. Carnicer, J., Coll, M., Ninyerola, M., Pons, X., Sanchez, G. & Penuelas, J. (2011) Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proceedings of the National Academy of Sciences of the United States of America, 108, 1474–1478.
21. Cermak, J. & Nadezhdina, N. (1998) Sapwood as the scaling parameter- defining according to xylem water content or radial pattern of sap flow? Annals of Forest Science, 55, 509–521.
22. Chapin, F.S., Schulze, E.D. & Mooney, H.A. (1990) The ecology and economics of storage in plants. Annual Review of Ecology and Systematics, 21, 423–447.
23. Cook, E. & Pederson, N. (2011) Uncertainty, Emergence, and Statistics in Dendrochronology. Dendroclimatology (eds M.K. Hughes, T.W. Swetnam & H.F. Diaz), pp. 77–112. Springer, Dordrecht, the Netherlands.
24. Desoto, L., Olano, J.M. & Rozas, V. (2016) Secondary growth and carbohydrate storage patterns differ between sexes in Juniperus thurifera. Frontiers in Plant Science, 7, 723.
25. Dobbertin, M., Hug, C. & Mizoue, N. (2004) Using slides to test for changes in crown defoliation assessment methods. Part I: visual assessment of slides. Environmental Monitoring and Assessment, 98, 295–306.
26. Dobbertin, M., Eilmann, B., Bleuler, P., Giuggiola, A., Graf Pannatier, E., Landolt, W., Schleppi, P. & Rigling, A. (2010) Effect of irrigation on needle morphology, shoot and stem growth in a drought-exposed Pinus sylvestris forest. Tree Physiology, 30, 346–360.
27. Eilmann, B., Dobbertin, M. & Rigling, A. (2013) Growth response of Scots pine with different crown transparency status to drought release. Annals of Forest Science, 70, 685–693.
28. Eilmann, B., Zweifel, R., Buchmann, N., Fonti, P. & Rigling, A. (2009) Drought-induced adaptation of the xylem in Scots pine and pubescent oak. Tree Physiology, 29, 1011–1020.
29. Eilmann, B., Zweifel, R., Buchmann, N., Graf Pannatier, E. & Rigling, A. (2011) Drought alters timing, quantity, and quality of wood formation in Scots pine. Journal of Experimental Botany, 62, 2763–2771.
30. Esteban, L., Martín, J., de Palacios, P. & Fernández, F. (2012) Influence of region of provenance and climate factors on wood anatomical traits of Pinus nigra Arn. subsp. salzmannii. European Journal of Forest Research, 131, 633–645.
31. Feichtinger, L.M., Eilmann, B., Buchmann, N. & Rigling, A. (2015) Trait-specific responses of Scots pine to irrigation on a short vs long time scale. Tree Physiology, 35, 160–171.
32. Fichot, R., Laurans, F., Monclus, R., Moreau, A., Pilate, G. & Brignolas, F. (2009) Xylem anatomy correlates with gas exchange, water-use efficiency and growth performance under contrasting water regimes: evidence from Populus deltoides x Populus nigra hybrids. Tree Physiology, 29, 1537–1549.
33. Fischer, C. & Höll, W. (1992) Food reserves of scots pine (Pinus sylvestris L.). Trees, 6, 147–155.
34. Fonti, P. & Frey, B. (2002) Is the ray volume a possible factor influencing ring shake occurrence in chestnut wood? Trees, 16, 519–522.
35. Fonti, P., Treydte, K., Osenstetter, S., Frank, D. & Esper, J. (2009) Frequency-dependent signals in multi-centennial oak vessel data. Palaeogeography, Palaeoclimatology, Palaeoecology, 275, 92–99.
36. Fonti, P., Tabakova, M., Kirdyanov, A., Bryukhanova, M. & von Arx, G. (2015) Variability of ray anatomy of Larix gmelinii along a forest productivity gradient in Siberia. Trees, 29, 1165–1175.
37. 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 Phytologist, 190, 750–759.
38. Gartner, B.L., Baker, D.C. & Spicer, R. (2000) Distribution and vitality of xylem rays in relation to tree leaf area in Douglas-fir. IAWA Journal, 21, 389–401.
39. Gärtner, H., Lucchinetti, S. & Schweingruber, F.H. (2015) A new sledge microtome to combine wood anatomy and tree-ring ecology. IAWA Journal, 36, 452-459.
40. Gärtner, H. & Schweingruber, F.H. (2013) Microscopic Preparation Techniques for Plant Stem Analysis. Kessel Publishing House, Remagenm, Germany.
41. Gonzalez, P., Neilson, R.P., Lenihan, J.M. & Drapek, R.J. (2010) Global patterns in the vulnerability of ecosystems to vegetation shifts due to climate change. Global Ecology and Biogeography, 19, 755–768.
42. Gricar, J., Prislan, P., De Luis, M., Gryc, V., Hacurova, J., Vavrcik, H. & Cufar, K. (2015) Plasticity in variation of xylem and phloem cell characteristics of Norway spruce under different local conditions. Frontiers in Plant Science, 6, 730.
43. Grissino-Mayer, H. (2001) Evaluating crossdating acuracy: a manual and tutorial for the computer program COFECHA. Tree-Ring Research, 57, 205–221.
44. Gruber, A., Pirkebner, D. & Oberhuber, W. (2013) Seasonal dynamics of mobile carbohydrate pools in phloem and xylem of two alpine timberline conifers. Tree Physiology, 33, 1076–1083.
45. Hanewinkel, M., Cullmann, D.A., Schelhaas, M.-J., Nabuurs, G.-J. & Zimmermann, N.E. (2013) Climate change may cause severe loss in the economic value of European forest land. Nature Climate Change, 3, 203–207.
46. Hartmann, H. (2015) Carbon starvation during drought-induced tree mortality–are we chasing a myth? Journal of Plant Hydraulics, 2, e005.
47. Hartmann, H. & Trumbore, S. (2016) Understanding the roles of nonstructural carbohydrates in forest trees – from what we can measure to what we want to know. New Phytologist, 211, 386–403.
48. Herzog, C., Steffen, J., Graf Pannatier, E., Hajdas, I. & Brunner, I. (2014) Nine years of irrigation cause vegetation and fine root shifts in a water-limited pine forest. PLoS ONE, 9, e96321.
49. Hoch, G., Richter, A. & Körner, C. (2003) Non-structural carbon compounds in temperate forest trees. Plant, Cell & Environment, 26, 1067–1081.
50. Hölttä, T., Mencuccini, M. & Nikinmaa, E. (2009) Linking phloem function to structure: analysis with a coupled xylem–phloem transport model. Journal of Theoretical Biology, 259, 325–337.
51. Hsiao, T.C. & Acevedo, E. (1974) Plant responses to water deficits, water-use efficiency, and drought resistance. Agricultural Meteorology, 14, 59–84.
52. Hudgins, J.W., Ralph, S., Franceschi, V. & Bohlmann, J. (2006) Ethylene in induced conifer defense: cDNA cloning, protein expression, and cellular and subcellular localization of 1-aminocyclopropane-1-carboxylate oxidase in resin duct and phenolic parenchyma cells. Planta, 224, 865–877.
53. IPCC. (2013) Summary for policymakers. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds T.F. Stocker, D. Qin, G.K. Plattner et al.). Cambridge University Press, Cambridge, UK & New York, NY, USA.
54. Irvine, J., Perks, M.P., Magnani, F. & Grace, J. (1998) The response of Pinus sylvestris to drought: stomatal control of transpiration and hydraulic conductance. Tree Physiology, 18, 393–402.
55. Jacquet, J.-S., Bosc, A., O’’Grady, A. & Jactel, H. (2014) Combined effects of defoliation and water stress on pine growth and non-structural carbohydrates. Tree Physiology, 34, 367–376.
56. Johnson, D.M., McCulloh, K.A., Woodruff, D.R. & Meinzer, F.C. (2012) Hydraulic safety margins and embolism reversal in stems and leaves: why are conifers and angiosperms so different? Plant Science, 195, 48–53.
57. Lloret, F., Martinez-Vilalta, J., Serra-Diaz, J.M. & Ninyerola, M. (2013) Relationship between projected changes in future climatic suitability and demographic and functional traits of forest tree species in Spain. Climatic Change, 120, 449–462.
58. Mantyka-Pringle, C.S., Visconti, P., Di Marco, M., Martin, T.G., Rondinini, C. & Rhodes, J.R. (2015) Climate change modifies risk of global biodiversity loss due to land-cover change. Biological Conservation, 187, 103–111.
59. McDowell, N., Pockman, W.T., Allen, C.D. 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.
60. McDowell, N.G., Beerling, D.J., Breshears, D.D., Fisher, R.A., Raffa, K.F. & Stitt, M. (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends in Ecology & Evolution, 26, 523–532.
61. Mencuccini, M. (2014) Temporal scales for the coordination of tree carbon and water economies during droughts. Tree Physiology, 34, 439–442.
62. Muller, B., Pantin, F., Génard, M., Turc, O., Freixes, S., Piques, M. & Gibon, Y. (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. Journal of Experimental Botany, 62, 1715–1729.
63. Myer, J.E. (1922) Ray volumes of the commercial woods of the United States and their significance. Journal of Forestry, 20, 337–351.
64. Oberhuber, W., Swidrak, I., Pirkebner, D. & Gruber, A. (2011) Temporal dynamics of nonstructural carbohydrates and xylem growth in Pinus sylvestris exposed to drought. Canadian Journal of Forest Research, 41, 1590–1597.
65. Olano, J.M., Menges, E.S. & Martinez, E. (2006) Carbohydrate storage in five resprouting Florida scrub plants across a fire chronosequence. New Phytologist, 170, 99–105.
66. Olano, J.M., Eugenio, M., Garcia-Cervigon, A.I., Folch, M. & Rozas, V. (2012) Quantitative tracheid anatomy reveals a complex environmental control of wood structure in continental Mediterranean climate. International Journal of Plant Sciences, 173, 137–149.
67. Olano, J.M., Arzac, A., García-Cervigón, A.I., von Arx, G. & Rozas, V. (2013) New star on the stage: amount of ray parenchyma in tree rings shows a link to climate. New Phytologist, 198, 486–495.
68. Palacio, S., Milla, R., Albuixech, J., Pérez-Rontomé, C., Camarero, J.J., Maestro, M. & Montserrat-Martí, G. (2008) Seasonal variability of dry matter content and its relationship with shoot growth and nonstructural carbohydrates. New Phytologist, 180, 133–142.
69. Palacio, S., Hoch, G., Sala, A., Körner, C. & Millard, P. (2013) Does carbon storage limit tree growth? New Phytologist, 201, 1096–1100.
70. Pfautsch, S., Hölttä, T. & Mencuccini, M. (2015) Hydraulic functioning of tree stems—fusing ray anatomy, radial transfer and capacitance. Tree Physiology, 35, 706–722.
71. Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D. & R Core Team (2016) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-127. Available at: http://CRAN.R-project.org/package=nlme (accessed 13 December 2016).
72. Plavcová, L. & Jansen, S. (2015) The Role of Xylem Parenchyma in the Storage and Utilization of Nonstructural Carbohydrates. Functional and Ecological Xylem Anatomy (ed. U. Hacke), pp. 209–234. Springer, Cham, Switzerland.
73. Popp, M., Lied, W., Meyer, A.J., Richter, A., Schiller, P. & Schwitte, H. (1996) Sample preservation for determination of organic compounds: microwave versus freeze-drying. Journal of Experimental Botany, 47, 1469–1473.
74. Poyatos, R., Aguadé, D., Galiano, L., Mencuccini, M. & Martínez-Vilalta, J. (2013) Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine. New Phytologist, 200, 388–401.
75. Pruyn, M.L., Gartner, B.L. & Harmon, M.E. (2002) Within-stem variation of respiration in Pseudotsuga menziesii (Douglas-fir) trees. New Phytologist, 154, 359–372.
76. Pruyn, M.L., Gartner, B.L. & Harmon, M.E. (2005) Storage versus substrate limitation to bole respiratory potential in two coniferous tree species of contrasting sapwood width. Journal of Experimental Botany, 56, 2637–2649.
77. R Development Core Team. (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
78. Reichstein, M., Bahn, M., Ciais, P. et al. (2013) Climate extremes and the carbon cycle. Nature, 500, 287–295.
79. Richardson, A.D., Carbone, M.S., Keenan, T.F., Czimczik, C.I., Hollinger, D.Y., Murakami, P., Schaberg, P.G. & Xu, X. (2013) Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytologist, 197, 850–861.
80. Richardson, A.D., Carbone, M.S., Huggett, B.A., Furze, M.E., Czimczik, C.I., Walker, J.C., Xu, X., Schaberg, P.G. & Murakami, P. (2015) Distribution and mixing of old and new nonstructural carbon in two temperate trees. New Phytologist, 206, 590–597.
81. Rigling, A., Braker, O., Schneiter, G. & Schweingruber, F. (2002) Intra-annual tree-ring parameters indicating differences in drought stress of Pinus sylvestris forests within the Erico-Pinion in the Valais (Switzerland). Plant Ecology, 163, 105–121.
82. Rigling, A., Bruhlhart, H., Braker, O.U., Forster, T. & Schweingruber, F.H. (2003) Effects of irrigation on diameter growth and vertical resin duct production in Pinus sylvestris L. on dry sites in the central Alps, Switzerland. Forest Ecology and Management, 175, 285–296.
83. Ryan, M.G. (1989) Sapwood volume for 3 subalpine conifers - predictive equations and ecological implications. Canadian Journal of Forest Research, 19, 1397–1401.
84. Saffell, B.J., Meinzer, F.C., Woodruff, D.R., Shaw, D.C., Voelker, S.L., Lachenbruch, B. & Falk, K. (2014) Seasonal carbohydrate dynamics and growth in Douglas-fir trees experiencing chronic, fungal-mediated reduction in functional leaf area. Tree Physiology, 34, 218–228.
85. Sala, A. & Hoch, G. (2009) Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant, Cell & Environment, 32, 22–30.
86. Sala, A., Woodruff, D.R. & Meinzer, F.C. (2012) Carbon dynamics in trees: feast or famine? Tree Physiology, 32, 764–775.
87. Salleo, S., Trifilo, P., Esposito, S., Nardini, A. & Lo Gullo, M.A. (2009) Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Functional Plant Biology, 36, 815–825.
88. Saranpää, P. & Höll, W. (1989) Soluble carbohydrates of Pinus sylvestris L. sapwood and heartwood. Trees, 3, 138–143.
89. Schaer, C., Vidale, P.L., Lüthi, D., Frei, C., Häberli, C., Lingier, M.A. & Appenzeller, C. (2004) The role of increasing temperature variability in European summer heatwaves. Nature, 427, 332–336.
90. Sevanto, S. (2014) Phloem transport and drought. Journal of Experimental Botany, 65, 1751–1759.
91. Spicer, R. (2014) Symplasmic networks in secondary vascular tissues: parenchyma distribution and activity supporting long-distance transport. Journal of Experimental Botany, 65, 1829–1848.
92. Stearns, S.C. (1976) Life-History Tactics - Review of Ideas. Quarterly Review of Biology, 51, 3–47.
93. Wiley, E. & Helliker, B. (2012) A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytologist, 195, 285–289.
94. Würth, M.K.R., Peláez-Riedl, S., Wright, S.J. & Körner, C. (2005) Non-structural carbohydrate pools in a tropical forest. Oecologia, 143, 11–24.
95. Yan, C.-F., Gessler, A., Rigling, A., Dobbertin, M., Han, X.-G. & Li, M.-H. (2016) Effects of mistletoe removal on growth, N and C reserves, and carbon and oxygen isotope composition in Scots pine hosts. Tree Physiology, 36, 562–575.
96. Zha, T., Kellomaki, S., Wang, K.Y., Ryyppo, A. & Niinisto, S. (2004) Seasonal and annual stem respiration of Scots pine trees under boreal conditions. Annals of Botany, 94, 889–896.
97. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A. & Smith, G.M. (2009) Mixed Effects Models and Extensions in Ecology With R. Springer, New York, NY, USA.
98. Zweifel, R., Bangerter, S., Rigling, A. & Sterck, F.J. (2012) Pine and mistletoes: how to live with a leak in the water flow and storage system? Journal of Experimental Botany, 63, 2565–2578.
99. Zweifel, R., Zimmermann, L., Zeugin, F. & Newbery, D.M. (2006) Intra-annual radial growth and water relations of trees: implications towards a growth mechanism. Journal of Experimental Botany, 57, 1445–1459.
100. Zweifel, R., Steppe, K. & Sterck, F.J. (2007) Stomatal regulation by microclimate and tree water relations: interpreting ecophysiological field data with a hydraulic plant model. Journal of Experimental Botany, 58, 2113–2131.