Fine root biomass and dynamics in beech forests across a precipitation gradient - Is optimal resource partitioning theory applicable to water-limited mature trees?

Journal of Ecology

Volumn 101, Issue 5, 2013, Pages 1183-1200

  Hertel, Dietrich ^a   Strecker, Tanja ^a,b   Müller Haubold, Hilmar ^a   Leuschner, Christoph ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Carbon allocation; Fagus sylvatica; Fine root production; Fine root turnover; Plant climate interactions; Precipitation reduction; Root : shoot ratio; Root area index; Root morphology; Sandy soils; Soil water storage capacity

Indexed keywords

BIOMASS ALLOCATION; CARBON CYCLE; DECIDUOUS FOREST; FINE ROOT; HERB; NICHE PARTITIONING; PRECIPITATION (CLIMATOLOGY); ROOT ARCHITECTURE; SANDY SOIL; SOIL WATER; TURNOVER; WATER AVAILABILITY; WATER STORAGE;

FAGUS; FAGUS SYLVATICA;

EID: 84883293650     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12124     Document Type: Article

References (113)

1. Aber, J.D., Melillo, J.M., Nadelhoffer, K.J., McClaugherty, C.A. & Pastor, J. (1985) Fine root turnover in forest ecosystems in relation to quantity and form of nitrogen availability: a comparison of two methods. Oecologia, 66, 317-321.
2. Aerts, R., Bakker, C. & De Caluwe, H. (1992) Root turnover as determinant of the cycling of C, N, and P in a dry heathland ecosystem. Biogeochemistry, 15, 175-190.
3. Allen, G.D., Macalady, A.K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier, M. 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.
4. Backes, K. & Leuschner, C. (2000) Leaf water relations of competitive Fagus sylvatica and Quercus petraea trees during 4 years differing in soil drought. Canadian Journal of Forest Research, 30, 335-346.
5. Bakker, M.R., Augusto, L. & Achat, D.L. (2006) Fine root distribution of trees and understory in mature stands of maritime pine (Pinus pinaster) on dry and humid sites. Plant and Soil, 286, 37-51.
6. Bauhus, J. & Bartsch, N. (1996) Fine-root growth in beech (Fagus sylvatica) forest gaps. Canadian Journal of Forest Research, 26, 2153-2159.
7. Bloom, A.J., Chapin, F.S. III & Mooney, H.A. (1985) Resource limitation in plants - an economic analogy. Annual Review of Ecology and Systematics, 16, 363-392.
8. 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 longterm consequences. Annals of Forest Science, 63, 625-644.
9. Bryla, D.R., Bouma, T.J. & Eissenstat, D.M. (1997) Root respiration in citrus acclimates to temperature and slows during drought. Plant, Cell & Environment, 20, 1411-1420.
10. Burton, A.J., Pregitzer, K.S. & Hendrick, R.L. (2000) Relationships between fine root dynamics and nitrogen availability in Michigan northern hardwood forests. Oecologia, 125, 389-399.
11. Cochard, H., Lemoine, D., Ameglio, T. & Granier, A. (2001) Mechanisms of xylem recovery from winter embolism in Fagus sylvatica. Tree Physiology, 21, 27-33.
12. Coleman, J.S., McConnaughay, K.D.M. & Ackerly, D.D. (1994) Interpreting phenotypic variation in plants. Trends in Ecology and Evolution, 9, 187-191.
13. Comeau, P.G. & Kimmins, J.P. (1989) Above- and below-ground biomass and production of lodgepole pine on sites with differing soil moisture regimes. Canadian Journal of Forest Research, 19, 447-454.
14. Coomes, D.A. & Grubb, P.J. (2000) Impacts of root competition in forests and woodlands: A theoretical framework and review of experiments. Ecological Monographs, 70, 171-207.
15. Cordell, S., Goldstein, G., Mueller-Dombois, D., Webb, D. & Vitousek, P.M. (1998) Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity. Oecologia, 113, 188-196.
16. Cuevas, E. (1995) Biology of the belowground system of tropical dry forests. Seasonally dry Tropical Forests (eds S.H. Bullock, H.A. Mooney & E. Medina). pp. 362-383. Cambridge University Press, Cambridge, UK.
17. Davidson, A.R., Ashmore, M.R. & Garretty, C. (1992) Effects of ozone and water deficit on the growth and physiology of Fagus sylvatica. Forest Ecology and Management, 51, 187-197.
18. DeVisser, P.H., Beier, B.C., Rasmussen, L., Kreutzer, K., Steinber, N., Bredemeier, M., Blanck, K., Farrell, E.P. & Cummins, T. (1994) Biological response of 5 forest ecosystems in the EXMAN project to input changes of water, nutrients and atmospheric loads. Forest Ecology and Management, 68, 15-29.
19. Eissenstat, D.M. (1991) On the relationship between specific root length and the rate of root proliferation: a field study using citrus rootstocks. New Phytologist, 118, 63-68.
20. Eissenstat, D.M. (1992) Costs and benefits of constructing roots of small diameter. Journal of Plant Nutrition, 15, 763-782.
21. Eissenstat, D.M. & Yanai, R.D. (1997) The ecology of root life span. Advances in Ecological Research, 27, 1-62.
22. Eissenstat, D.M. & Yanai, R.D. (2002) Root life span, efficiency, and turnover. Plant Roots: The Hidden Half (eds Y. Waisel, A. Eshel & U. Kafkafi), pp. 221-238. Dekker, New York.
23. Eissenstat, D.M., Wells, C.E., Yanai, R.D. & Whitbeck, J.L. (2000) Building roots in changing environment: implications for root longevity. New Phytologist, 147, 33-42.
24. Ellenberg, H. & Leuschner, C. (2010) Vegetation Mitteleuropas mit den Alpen. Ulmer, Stuttgart.
25. Enstone, D.E., Peterson, C.A. & Ma, F.S. (2002) Root endodermis and exodermis: structure, function, and responses to the environment. Journal of Plant Growth Regulation, 21, 335-351.
26. Espeleta, J.F., Eissenstat, D.M. & Graham, J.H. (1999) Citrus root responses to localized drying soil: a new approach to studying mycorrhizal effects on the roots of mature trees. Plant and Soil, 206, 1-10.
27. Espeleta, J.F., West, J.B. & Donovan, L.A. (2009) Tree species fine-root demography parallels habitat specialization across a sandhill soil resource gradient. Ecology, 90, 1773-1787.
28. Finér, L., Helmisaari, H.S., Lõhmus, K., Majdi, H., Brunner, I., Børja, I. et al. (2007) Variation in fine root biomass of three European tree species: Beech (Fagus sylvatica L.), Norway spruce (Picea abies L. Karst.) and Scots pine (Pinus sylvestris L.). Plant Biosystems, 141, 394-405.
29. Finér, L., Ohashi, M., Noguchi, K. & Hirano, Y. (2011a) Factors causing variation in fine root biomass in forest ecosystems. Forest Ecology and Management, 261, 265-277.
30. Finér, L., Ohashi, M., Noguchi, K. & Hirano, Y. (2011b) Fine root production and turnover in forest ecosystems in relation to stand and environmental characteristics. Forest Ecology and Management, 262, 2008-2023.
31. Fitter, A.H. (1986) The topology and geometry of plant root systems: influence of watering rate on root system topology in Trifolium pratense. Annals of Botany, 58, 91-101.
32. Fogel, R. (1985) Roots as primary producers in below-ground ecosystems. Ecological Interactions in Soil: Plants Microbes and Animals, Special Publication No. 4 of the British Ecological Society (eds A.H. Fitter, D. Atkinson, D.J. Read & M.B. Usher), pp. 23-36, Blackwell Scientific Publications, Oxford, UK.
33. Fogel, R. & Hunt, G. (1983) Contribution of mycorrhizae and soil fungi to nutrient cycling in a Douglas-fir ecosystem. Canadian Journal of Forest Research, 13, 219-232.
34. 15N-uptake, N balance and biomass of European beech seedlings. Trees, 18, 157-166.
35. Gaul, D., Hertel, D., Borken, W., Matzner, E. & Leuschner, C. (2008) Effects of experimental drought on the fine root system of mature Norway spruce. Forest Ecology and Management, 256, 1151-1159.
36. Gill, R.A. & Jackson, R.B. (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytologist, 147, 13-31.
37. Granier, A., Reichstein, M., Bréda, N., Janssens, I.A., Falge, E., Ciais, P. et al. (2007) Evidence for soil water control on carbon and water dynamics in European forests during the extremely dry year: 2003. Agricultural and Forest Meteorology, 143, 123-145.
38. Guo, D.L., Mitchell, R.J., Withington, J.M., Fan, P.P. & Hendricks, J.J. (2008) Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. Journal of Ecology, 96, 737-745.
39. Hendricks, J.J., Hendrick, R.L., Wilson, C.A., Mitchell, R.J., Pecot, S.D. & Guo, D. (2006) Assessing the patterns and controls of fine root dynamics: an empirical test and methodological review. Journal of Ecology, 94, 40-57.
40. Hertel, D. (1999) Das Feinwurzelsystem von Rein- und Mischbeständen der Rotbuche: Struktur, Dynamik und interspezifische Konkurrenz. Dissertationes Botanicae, 317. Gebrüder Bornträger, Stuttgart.
41. Hertel, D. & Leuschner, C. (2002) A comparison of four different fine root production estimates with ecosystem carbon balance data in a Fagus-Quercus mixed forest. Plant and Soil, 239, 237-251.
42. Hertel, D., Therburg, A. & Villalba, R. (2008) Above- and below-ground response of Nothofagus pumilio to growth conditions of the transition from the steppe-forest boundary to the alpine treeline in S Patagonia (Argentina). Plant Ecology and Diversity, 1, 21-33.
43. Hertel, D. & Wesche, K. (2008) Tropical-moist Polylepis stands at the treeline in E-Bolivia: the effect of elevation on above- and below-ground structure, and regeneration. Trees, 22, 303-315.
44. Intergovernmental Panel on Climate Change (IPCC) (2007) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds S. Solomon et al.), p. 996. Cambridge University Press, New York.
45. Jackson, R.B., Mooney, H.A. & Schulze, E.D. (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proceedings of the National Academy of Sciences United States of America, 94, 7362-7366.
46. Jump, A.S., Hunt, J.M. & Penuelas, J. (2006) Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Global Change Biology, 12, 2163-2174.
47. Kalisz, P.J., Zimmerman, R.W. & Muller, R.N. (1987) Root density, abundance, and distribution in mixed mesophytic forest of eastern Kentucky. Soil Science Society of America Journal, 51, 220-225.
48. Köcher, P., Gebauer, T., Horna, V. & Leuschner, C. (2009) Leaf water status and stem xylem flux in relation to soil drought in five temperate broad-leaved tree species with contrasting water use strategies. Annals of Forest Sciences, 66, article 101.
49. Konôpka, B., Yuste, J.C., Janssens, I.A. & Ceulemans, R. (2005) Comparison of fine root dynamics in Scots pine and Pedunculate oak in sandy soil. Plant and Soil, 276, 33-45.
50. Kreutzwieser, J. & Gessler, A. (2010) Global climate change and tree nutrition: influence of water availability. Tree Physiology, 30, 1221-1234.
51. Lauenroth, W.K. & Gill, R. (2003) Turnover of root systems. Root Ecology. Ecological Studies 168 (eds H. de Kroon & E.J.W. Visser), pp. 61-90. Springer, Berlin.
52. Leuschner, C. & Hertel, D. (2003) Fine root biomass of temperate forests in relation to soil acidity and fertility, climate, age and species. Progress in Botany, 64, 405-438.
53. Leuschner, C., Meier, I.C. & Hertel, D. (2006) On the niche breadth of Fagus sylvatica: soil nutrient status in 50 Central European beech stands on a broad range of bedrock types. Annals of Forest Science, 63, 355-368.
54. Leuschner, C., Backes, K., Hertel, D., Schipka, F., Schmitt, U., Terborg, O. & Runge, M. (2001a) Drought responses at leaf, stem and fine root levels of competitive Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. trees in dry and wet years. Forest Ecology and Management, 149, 33-46.
55. Leuschner, C., Hertel, D., Coners, H. & Büttner, V. (2001b) Root competition between beech and oak: a hypothesis. Oecologia, 126, 276-284.
56. Leuschner, C., Coners, H., Icke, R., Hartmann, K., Effinger, N.D. & Schreiber, L. (2003) Chemical composition of the periderm in relation to in situ water absorption rates of oak, beech and spruce fine roots. Annals of Forest Science, 60, 763-772.
57. Leuschner, C., Hertel, D., Schmid, I., Koch, O., Muhs, A. & Hölscher, D. (2004) Stand fine root biomass and fine root morphology in old-growth beech forests as a function of precipitation and soil fertility. Plant and Soil, 258, 43-56.
58. Leuzinger, S., Zotz, G., Asshoff, R. & Körner, C. (2005) Responses of deciduous forest trees to severe drought in Central Europe. Tree Physiology, 25, 641-650.
59. Lõhmus, K., Oja, T. & Lasn, E. (1989) Specific root area: a soil characteristic. Plant and Soil, 119, 245-249.
60. López, B., Sabaté, S. & Gracia, C. (1998) Fine roots dynamics in a Mediterranean forest: effects of drought and stem density. Tree Physiology, 18, 601-606.
61. Magnani, F. & Borghetti, M. (1995) Interpretation of seasonal changes of xylem embolism and plant hydraulic resistance in Fagus sylvatica. Plant, Cell & Environment, 18, 689-696.
62. Mainiero, R. & Kazda, M. (2006) Depth-related fine root dynamics of Fagus sylvatica during exceptional drought. Forest Ecology and Management, 237, 135-142.
63. Majdi, H. (1996) Root sampling methods - applications and limitations of the minirhizotron technique. Plant and Soil, 185, 255-258.
64. Matamala, R., Gonzalez-Meler, M.A., Jastrow, J.D., Norby, R.J. & Schlesinger, W.H. (2003) Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science, 302, 1385-1387.
65. McConnaughay, K.D.M. & Coleman, J.S. (1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology, 80, 2581-2593.
66. Meier, I.C. & Leuschner, C. (2008a) The belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Global Change Biology, 14, 2081-2095.
67. Meier, I.C. & Leuschner, C. (2008b) Genotypic variation and phenotypic plasticity in the drought response of fine roots of European beech. Tree Physiology, 28, 297-309.
68. Metcalfe, D.B., Meir, P., Aragão, L.E.O.C., da Costa, A.C.L., Braga, A.P., Goncalvez, P.H.L., de Silva, J.A., de Almeidea, S.S., Dawson, L.A., Malhi, Y. & Williams, M. (2008) The effects of water availability on root growth and morphology in an Amazon rainforest. Plant and Soil, 311, 189-199.
69. Nadelhoffer, K.J. & Raich, J.W. (1992) Fine root production estimates and below-ground carbon allocation in forest ecosystems. Ecology, 73, 1139-1147.
70. Norby, R.J. & Jackson, R.B. (2000) Root dynamics and global change: seeking an ecosystem perspective. New Phytologist, 147, 3-12.
71. Ostonen, I., Lõhmus, K., Helmisaari, H.S., Truu, J. & Meel, S. (2007) Fine root morphological adaptations in Scots pine, Norway spruce and silver birch along a latitudinal gradient in boreal forests. Tree Physiology, 27, 1627-1634.
72. Ostonen, I., Helmisaari, H.S., Borken, W., Tedersoo, L., Kukumägi, M., Bahram, M., Lindroos, A.-J., Nöjd, P., Uri, V., Merilä, P., Asi, E. & Lõhmus, K. (2011) Fine root foraging strategies in Norway spruce forests across European climate gradient. Global Change Biology, 17, 3620-3632.
73. Parker, M.M. & Van Lear, D.H. (1996) Soil heterogeneity and root distribution of mature loblolly pine stands in Piedmont soils. Soil Science Society of America Journal, 60, 1920-1925.
74. Paula, S. & Pausas, J.G. (2011) Root traits explain different foraging strategies between resprouting life histories. Oecologia, 165, 321-331.
75. Persson, H. (1978) Root dynamics in a young Scots pine stand in Central Sweden. Oikos, 30, 508-519.
76. Persson, H. (1980) Fine-root dynamics in a Scots pine stand with and without near optimum nutrient and water regimes. Acta Phytogeographica Suecica, 68, 101-110.
77. Polverigiani, S., McCormack, M.L., Mueller, C.W. & Eissenstat, D.M. (2011) Growth and physiology of olive pioneer and fibrous roots exposed to soil moisture deficits. Tree Physiology, 31, 1228-1237.
78. 2, nutrients and water: a quantitative review. Australian Journal of Plant Physiology, 27, 595-607.
79. Powell, S.W. & Day, F.P. (1991) Root production in four communities in the Great Dismal Swamp. American Journal of Botany, 78, 288-297.
80. Pregitzer, K.S., Hendrick, R.L. & Fogel, R. (1993) The demography of fine roots in response to patches of water and nitrogen. New Phytologist, 125, 575-580.
81. Pregitzer, K.S., DeForest, J.L., Burton, A.J., Allen, M.F., Ruess, R.W. & Hendrick, R.L. (2002) Fine root architecture of nine North American trees. Ecological Monographs, 72, 293-309.
82. Reich, P.B. (2002) Root-Shoot Relations: Optimality in Acclimation and Adaptation or the "Emperor's New Clothes"? Plant Roots: The Hidden Half (eds Y. Waisel, A. Eshel & U. Kafkafi), pp. 205-220, Dekker, New York.
83. Rennenberg, H., Loreto, F., Polle, A., Brilli, F., Fares, S., Beniwal, R.S. & Gessler, A. (2006) Physiological responses of forest trees to heat and drought. Plant Biology, 8, 556-571.
84. Rewald, B., Michopoulos, P., Dalsgaard, L., Jones, D.L. & Godbold, D.L. (2011) Hydrological effects on below ground processes in temperate and mediterranean forests. Forest Management and the Water Cycle: An Ecosystem-Based Approach (eds M. Bredemeier, S. Cohen, D.L. Godbold, E. Lode, V. Pichler & P. Schleppi), Ecological Studies 212, pp. 5-29, Springer, Heidelberg, New York.
85. Rice, S.A. & Bazzaz, F.A. (1989) Quantification of plasticity of plant traits in response to light intensity: comparing phenotypes at a common weight. Oecologia, 78, 502-507.
86. Rose, L., Leuschner, C., Köckemann, B. & Buschmann, H. (2009) Are marginal beech (Fagus sylvatica L.) provenances a source for drought tolerant ecotypes? European Journal of Forest Research, 128, 335-343.
87. Rowell, D.P. & Jones, R.G. (2006) Causes and uncertainty of future summer drying over Europe. Climate Dynamics, 27, 281-299.
88. Ruess, R.W., van Cleve, K., Yarie, J. & Viereck, L.A. (1996) Contributions of fine root production and turnover to the carbon and nitrogen cycling in taiga forests of the Alaskan interior. Canadian Journal of Forest Research, 26, 1326-1336.
89. Rühr, N., Offermann, C., Gessler, A., Winkler, J.B., Ferrio, J.P., Buchmann, N. & Barnard, R.L. (2009) Effects of drought on allocation of recent carbon: from beech leaves to soil respiration. New Phytologist, 184, 950-961.
90. Santantonio, D. & Hermann, R.K. (1985) Standing crop, production, and turnover of fine roots on dry, moderate, and wet sites of mature Douglas fir in Western Oregon. Annales des Sciences Forestières, 42, 113-142.
91. Schär, C., Vidale, P.L., Lüthi, D., Frei, C., Häberli, C., Liniger, M. & Appenzeller, C. (2004) The role of increasing temperature variability- in European summer heatwaves. Nature, 427, 332-336.
92. Schenk, H.J. (2005) Vertical vegetation structure below ground: scaling from root to globe. Progress in Botany, 66, 341-373.
93. Schenk, H.J. & Jackson, R.B. (2002) Rooting depths, lateral root spreads and belowground/aboveground allometries of plants in water-limited ecosystems. Journal of Ecology, 90, 480-494.
94. Scholze, M., Knorr, W., Arnell, N.W. & Prentice, I. (2006) A climate-change risk analysis for world ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 103, 13116-13120.
95. Schreiber, L. & Franke, R.B. (2011) Endodermis and Exodermis in Roots. eLS (Encyclopedia of Life Sciences). John Wiley & Sons, Ltd, Chichester. DOI: 10.1002/9780470015902.a0002086.pub2.
96. Silver, W.L., Thompson, A.W., McGroddy, M.E., Varner, R.K., Dias, J.D., Silva, H., Crill, P.M. & Kellers, M. (2005) Fine root dynamics and trace gas fluxes in two lowland tropical forest soils. Global Change Biology, 11, 290-360.
97. Steele, S.J., Gower, S.T., Vogel, J.G. & Norman, J.M. (1997) Root mass, net primary production and turnover in aspen, Jack pine and black spruce forests in Saskatchewan and Manitoba, Canada. Tree Physiology, 17, 577-587.
98. Stout, D.L. & Sala, A. (2003) Xylem vulnerability to cavitation in Pseudotsuga menziesii and Pinus ponderosa from contrasting habitats. Tree Physiology, 23, 43-50.
99. Sun, Y., Gu, J., Zhuang, H., Guo, D. & Wang, Z. (2011) Lower order roots more palatable to herbivores: a case study with two temperate tree species. Plant and Soil, 347, 351-361.
100. Teskey, R.O. & Hinckley, T.M. (1981) Influence of temperature and water potential on root growth of white oak. Physiologia Plantarum, 52, 363-369.
101. Tierney, G.L., Fahey, T.J., Groffman, P.M., Hardy, J.P., Fitzhughs, R.D., Driscoll, C.T. & Yavitt, J.P. (2003) Environmental control of fine root dynamics in a northern hardwood forest. Global Change Biology, 9, 670-679.
102. Tognetti, R., Johnson, J.D. & Michelozzi, M. (1995) The response of European beech (Fagus sylvatica L.) seedlings from two Italian populations to drought and recovery. Trees, 9, 348-354.
103. 2 and water stress. II. Recent photosynthate distribution and growth. New Phytologist, 140, 493-504.
104. Van Hees, A.F.M. (1997) Growth and morphology of pedunculate oak (Quercus robur L.) and beech (Fagus sylvatica L.) seedlings in relation to shading and drought. Annales des Science Forestières, 54, 9-18.
105. Van Praag, H.J., Sougenez-Remy, S., Weissen, F. & Carletti, G. (1988) Root turnover in a beech stand of the Belgian Ardennes. Plant and Soil, 105, 87-103.
106. Vogt, K.A., Vogt, D.J., Moore, E.E., Fatuga, B.A., Redlin, M.R. & Edmonds, R.L. (1987) conifer and angiosperm fine-root biomass in relation to stand age and site productivity in Douglas-fir forests. Journal of Ecology, 75, 857-870.
107. Vogt, K.A., Vogt, D.J., Palmiotto, P.A., Boon, P., O'Hara, J. & Asbjornsen, H. (1996) Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species. Plant and Soil, 187, 159-219.
108. Wagenhoff, A. & Wagenhoff, E. (1975) Verlauf und Auswirkung des Buchen-rindensterbens im Forstamt Bovenden in den Jahren 1959 bis 1965. Aus dem Walde, 24, 111-168.
109. Walter, H. & Stadelmann, E.J. (1968) The physiological prerequisites for the transition of autotrophic plants from water to terrestrial life. BioScience, 18, 694-701.
110. West, J.B., Espeleta, J.F. & Donovan, L.A. (2004) Fine root production and turnover across a complex edaphic gradient of a Pinus palustris-Aristida stricta savanna ecosystem. Forest Ecology and Management, 189, 397-406.
111. Winkler, J.B., Dannenmann, M., Simon, J., Pena, R., Offermann, C., Sternad, W. et al. (2010) Carbon and nitrogen balance in beech roots under competitive pressure of soil-borne microorganisms induced by girdling, drought and glucose application. Functional Plant Biology, 37, 879-889.
112. Withington, J.M., Reich, P.B., Oleksyn, J. & Eissenstat, D.M. (2006) Comparisons of structure and life span in roots and leaves among temperate trees. Ecological Monographs, 76, 381-397.
113. Zadworny, M. & Eissenstat, D.M. (2011) Contrasting the morphology, anatomy and fungal colonization of new pioneer and fibrous roots. New Phytologist, 190, 213-221.