How to study deep roots-and why it matters

Frontiers in Plant Science

Volumn 4, Issue AUG, 2013, Pages

  Maeght, Jean Luc ^a   Rewald, Bon's ^b   Pierret, Alain ^a  

^a IRD   (Laos)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

Biogeochemical and ecological functions; Deep roots; Root measure

Indexed keywords

EID: 84893556134     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00299     Document Type: Review

References (168)

1. Abbott, M. L., and Fraley, L. (1991). A review: radiotracer methods to determine root distribution. Environ. Exp. Bot. 31, 1-10.
2. Abiven, S., Recous, S., Reyes, V., and Oliver, R. (2005). Mineralisation of C and N from root, stem and leaf residues in soil and role of their biochemical quality. Biol. Fertil. Soils 42, 119-128. doi: 10.1007/s00374-005-0006-0
3. Andrews, R. E., and Newman, E. I. (1970). Root density and competition for nutrients. Oecol. Plant 5, 319-334.
4. Baitulin, I. O. (1979). Kornevaja Sistema Rastenij Aridnoj Zony Kazakhstana. [Root Systems of Plants of the Arid Zone of Kazakhstan]. Alma-Ata: Nauka.
5. Bates, G. H. (1937). A device for the observation of root growth in the soil. Nature 139, 966-967.
6. Bengough, A. G. (2012). Water dynamics of the root zone: rhizosphere biophysics and its control on soil hydrology. Vadose Zone J. 11. doi: 10.2136/vzj2011.0111
7. Bengough, A. G., Castrignano, A., Pagès, L., and van Noordwijk, M. (2000). "Sampling strategies, scaling, and statistics," in Root Methods, eds A. L. Smit, A. G. Bengough, C. Engels, M. van Noordwijk, S. Pellerin, and S. C. van de Geijn (Berlin; Heidelberg: Springer), 147-173. doi: 10.1007/978-3-662-04188-8_533
8. Bleby, T. M., McElrone, A. J., and Jackson, R. B. (2010). Water uptake and hydraulic redistribution across large woody root systems to 20m depth. Plant Cell Environ. 33, 2132-2148. doi: 10.1111/j.1365-3040.2010.02212.x
9. Blossfeld, S., Gansert, D., Thiele, B., Kuhn, A. J., and Lösch, R. (2011). The dynamics of oxygen concentration, pH value, and organic acids in the rhizosphere of Juncus spp. Soil Biol. Biochem. 43, 1186-1197. doi: 10.1016/j.soilbio.2011.02.007
10. Böhm W. (1979). Methods of Studying Root Systems. Berlin: Springer.
11. Breazeale, J. F. (1930). Maintenance of moisture-equilibrium and nutrition of plants at and below the wilting percentage. in Ariz. Agric. Exp. Stn. Tech. Bull. 29, 137-177.
12. Brown, D. A., and Upchurch, D. R. (1987). Minirhizotron observation tubes: methods and applications for measuring rhizosphere dynamics. ASA Spec. Publ. 50, 15-30.
13. Bruijnzeel, L. A. (2004). Hydrological functions of tropical forests: not seeing the soil for the trees. Agric. Ecosyst. Environ. 104, 185-228. doi: 10.1016/j.agee.2004.01.015.
14. Burgess, S. S. O. (2010). Can hydraulic redistribution put bread on our table. Plant Soil 341, 25-29. doi: 10.1007/s11104-010-0638-1
15. Burgess, S. S. O. (2000). Seasonal water acquisition and redistribution in the Australian woody phreatophyte, Banksia pri-onotes. Ann. Bot. 85, 215-224. doi: 10.1006/anbo.1999.1019
16. Burgess, S. S. O., Adams, M. A., Turner, N. C., and Ong, C. K. (1998). The redistribution of soil water by tree root systems. Oecologia 115, 306-311. doi: 10.1007/s004420050521
17. Buss, H. L., Bruns, M. A., Schultz, M. J., Moore, J., Mathur, C. F., Brantley, S. L., et al. (2005). The coupling of biological iron cycling and mineral weathering during saprolite formation, Luquillo Mountains, Puerto Rico. Geobiology 3, 247-260.
18. Cahoon, D. R., Lynch, J. C., and Knaus, R. M. (1996). Improved cryogenic coring device for sampling wetland soils. J. Sedement. Res. 66, 1025-1027.
19. Calder, I. R., Rosier, P. T. W., Prasanna, K. T., and Parameswarappa, S. (1997). Eucalyptus water use greater than rainfall input - possible explanation from southern India. Hydrol. Earth Syst. Sci. 2, 249-255.
20. Caldwell, M. M., and Richards, J. H. (1998). Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113, 151-161.
21. Cameron, R. (1963). A study of the rooting habits of rimu and tawa in pumice soils. N.Z. J. For. 8, 771-785.
22. Canadell, J., Djema, A., Lopez, B., Lioret, F., Sabaté, S., Siscart, D., et al. (1999). Structure and dynamics of the root system. Ecol. Stud. 137, 47-59.
23. Canadell, J., Jackson, R. B., Ehleringer, J. B., Mooney, H. A., Sala, O. E., and Schulze, E.-D. (1996). Maximum rooting depth of vegetation types at the global scale. Oecologia 108, 583-595. doi: 10.1007/BF00329030
24. Cannon, W. A. (1949). A tentative classification of root systems. Ecology 30, 542.
25. Cannon, H. L. (1960). The development of botanical methods of prospecting for uranium on the Colorado Plateau. U.S. Geol. Surv. Bull. 1085-A, 1-50.
26. Carbon, B. A., Bartle, G. A., Murray, A. M., and Macpherson, D. K. (1980). The distribution of root length, and the limits to flow of soil water to roots in a dry sclerophyll forest. For. Sci. 26, 656-664.
27. Cardon, Z. G., and Whitbeck, J. L. (2007). The Rhizosphere: An Ecological Perspective. London: Elsevier.
28. Chloupek, O., Forster, B. P., and Thomas, W. T. B. (2006). The effect of semi-dwarf genes on root system size in field-grown barley. Theor. Appl. Genet. 112, 779-786. doi: 10.1007/s00122-005-0147-4
29. Christina, M., Laclau, J.-P., Gonçalves, J. L. M., Jourdan, C., Nouvellon, Y., and Bouillet, J.-P. (2011). Almost symmetrical vertical growth rates above and below ground in one of the world's most productive forests. Ecosphere 2, 1-10. doi: 10.1890/ES10-00158.1
30. Clemmensen, K. E., Bahr, A., Ovaskainen, O., Dahlberg, A., Ekblad, A., Wallander, H., et al. (2013). Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615-1618. doi: 10.1126/science.1231923
31. Culver, D. C., and Pipan, T. (2009). The Biology of Caves and Other Subterranean Habitats. Oxford, New York: University Press.
32. Dalpé, Y., Diop, T., Plenchette, C., and Gueye, M. (2000). Glomales species associated with surface and deep rhizosphere of Faidherbia albida in Senegal. Mycorrhiza 10, 125-129. doi: 10.1007/s005720000069
33. Da Silva, E. V., Bouillet, J.-P., De Moraes Gonçalves, J. L., Junior, C. H. A., Trivelin, P. C. O., Hinsinger, P., et al. (2011). Functional specialization of Eucalyptus fine roots: contrasting potential uptake rates for nitrogen, potassium and calcium tracers at varying soil depths. Funct. Ecol. 25, 996-1006. doi: 10.1007/s10531-011-0057-5
34. Dauer, J. M., Withington, J. M., Oleksyn, J., Chorover, J., Chadwick, O. A., Reich, P. B., et al. (2009). A scanner-based approach to soil profile-wall mapping of root distribution. Dendrobiology 62, 35-40.
35. Davidson, E., Lefebvre, P., and Brando, P. (2011). Carbon inputs and water uptake in deep soils of an eastern Amazon forest. For. Sci. 57, 51-58.
36. Dawson, T., and Ehleringer, J. (1991). Streamside trees that do not use stream water. Nature 350, 335-337.
37. De Azevedo, M. C. B., Chopart, J. L., and de Medina, C. C. (2011). Sugarcane root length density and distribution from root intersection counting on a trench-profile. Sci. Agric.1, 94-101. doi: 10.1590/S0103-90162011000100014.
38. Dodds, W., Banks, M., and Clenan, C. (1996). Biological properties of soil and subsurface sediments under abandoned pasture and cropland. Soil Biol. Biochem. 28, 837-846. doi: 10.1016/0038-071700057-0
39. Doody, T. M., and Benyon, R. G. (2011). Direct measurement of groundwater uptake through tree roots in a cave. Ecohydrology 4, 644-649. doi: 10.1002/eco.152
40. Dunin, F., Smith, C., Zegelin, S., and Leuning, R. (2001). Water balance changes in a crop sequence with lucerne. Aust. J. Agric. Res. 52, 247-261. doi: 10.1071/ AR00089
41. Eamus, D., Chen, X., Kelley, G., and Hutley, L. (2002). Root biomass and root fractal analyses of an open Eucalyptus forest in a savanna of north Australia. Aust. J. Bot. 50, 31-41. doi: 10.1071/breakBT01054
42. Eberbach, P. L., Hoffmann, J., Moroni, S. J., Wade, L. J., and Weston, L. A. (2013). Rhizo-lysimetry: facilities for the simultaneous study of root behaviour and resource use by agricultural crop and pasture systems. Plant Methods 9:3. doi: 10.1186/1746-4811-9-3
43. Eilers, K. G., Debenport, S., Anderson, S., and Fierer, N. (2012). Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Biol. Chem. 50, 58-65. doi: 10.1016/j.soilbio.2012.03.011
44. Elliott, S., Baker, P., and Borchert, R. (2006). Leaf flushing during the dry season: the paradox of Asian monsoon forests. Global Ecol. Biogeogr. 15, 1-10. doi: 10.1016/j.soilbio.2012.03.011
45. Fang, S., Clark, R., and Liao, H. (2012). "3D quantification of plant root architecture in situ," in Measuring Roots - An Updated Approach, ed S. Mancuso (Berlin: Springer), 135-148.
46. Filella, I., and Peñuelas, J. (2003). Indications of hydraulic lift by Pinus halepensis and its effects on the water relations of neighbour shrubs. Biol. Plantarum 47, 209-214. doi: 10.1023/B:BIOP. 0000022253.08474.fd
47. Fitter, A., Hodge, A., and Robinson, D. (2000). "Plant response to patchy soils," in The Ecological Consequences of Environ-Mental Heterogeneity, eds M. J. Hutchings, E. A. John, and A. J. A. Stewart (Oxford: Blackwell Science), 71-90.
48. Freckman, D. W., and Virginia, R. A. (1989). Plant-feeding nematodes in deep-rooting desert ecosystems. Ecology 70, 1665-1678. doi: 10.2307/1938101
49. Goldstein, G., Meinzer, F. C., Bucci, S. J., Scholz, F. G., Franco, A. C., and Hoffmann, W. A. (2008). Water economy of Neotropical savanna trees: six paradigms revisited. Tree Physiol. 28, 395-404. doi: 10.1093/treephys/28.3.395
50. Gonkhamdee, S., Maeght, J. L., Do, F., and Pierret, A. (2009). Growth dynamics of line Heavea brasiliensis roots along a 4.5-m soil profile. Khon Kaen Agric. J. 37, 265-276.
51. Göransson, H., Fransson, A.-M., and Jönsson-Belyazid, U. (2007). Do oaks have different strategies for uptake of N, K and P depending on soil depth. Plant Soil 297, 119-125. doi: 10.1007/s11104-0 07-9325-2
52. Göransson, H., Ingerslev, M., and Wallander, H. (2008). The vertical distribution of N and K uptake in relation to root distribution and root uptake capacity in mature Quercus robur, Fagus sylvatica and Picea abies stands. Plant Soil 306, 129-137. doi: 10.1007/s11104-007-9524-x
53. Göransson, H., Wallander, H., Ingerslev, M., and Rosengen, U. (2006). Estimating the relative nutrient uptake from different soil depth of Quercus robur, Fagus sylvatica and Picea abies (L.) Karst. Plant Soil 286, 87-97. doi: 10.1007/s11104-0 06-9028-0
54. Guo, D., Li, H., Mitchell, R. J., Han, W., Hendricks, J. J., Fahey, T. J., et al. (2008). Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytol. 177, 443-456. doi: 10.1111/j.1469-8137.2007.02242.x
55. Harper, R. J., and Tibbett, M. (2013). The hidden organic carbon in deep mineral soils. Plant Soil 368, 641-648. doi: 10.1007/s11104-013-1600-9
56. Harper, J. L., Jones, M., and Sackville Hamilton, N. R. (1991). "The evolution of roots and the problems of analyzing their behaviour," in Plant Root Growth: An Ecological Perspective, ed D. Atkinso (Oxford: Blackwell Scientific Publications), 3-22.
57. Harrison, R., Footen, P., and Strahm, B. (2011). Deep soil horizons: contribution and importance to soil carbon pools and in assessing whole-ecosystem response to management and global change. For. Sci. 57, 67-76.
58. He, H., Bleby, T. M., Veneklaas, E. J., and Lambers, H. (2012). Arid-zone Acacia species can access poorly soluble iron phosphate but show limited growth response. Plant Soil 358, 119-130. doi: 10.1007/s11104-011-1103-5
59. Herrera, J., Verhulst, N., and Govaerts, B. (2012). "Strategies to identify genetic diversity in root traits," in Physiological Breeding I: Interdisciplinary Approaches to Improve Crop Adaptation, eds M. P. Reynolds, A. J. D. Pask, and D. Mullan (Mexico, DF: CIMMYT), 97-108.
60. Hinsinger, P. (1998). How do plant roots acquire mineral nutrients. Chemical processes involved in the rhizosphere. Adv. Agron. 64, 225-265.
61. Hinsinger, P., Brauman, A., Devau, N., Gérard, F., Jourdan, C., Laclau, J.-P., et al. (2011). Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil 348, 29-61. doi: 10.1007/s11104-011-0903-y
62. Hinsinger, P., Cloutier-Hurteau, B., Jourdan, C., and Laclau, J. P. (2012). "The roots of our soils," in Roots to The Future 8th Symposium of the International Society of Root Research (Dundee).
63. Hodge, A. (2006). Plastic plants and patchy soils. J. Exp. Bot. 57, 401-411. doi: 10.1093/jxb/eri280
64. Hodge, A., Berta, G., Doussan, C., Merchan, F., and Crespi, M. (2009). Plant root growth, architecture and function. Plant Soil 321, 153-187. doi: 10.1007/s11104-009-9929-9
65. Horton, J. L., and Hart, S. C. (1998). Hydraulic lift: a potentially important ecosystem process. Tre n ds Ecol. Evol. 13, 232-235. doi: 10.1016/S0169-534701328-7
66. Howarth, F. G. (1983). Ecology of cave arthropods. Annu. Rev. Entomol. 28, 365-389. doi: 10.1146/annurev. en.28.010183.002053
67. Howarth, F. G., James, S. A., McDowell, W., Preston, D. J., and Imada, C. T. (2007). Identification of roots in lava tube caves using molecular techniques: implications for conservation of cave arthropod faunas. J. Insect. Conserv. 11, 251-261. doi: 10.1007/s10841-006-9040-y
68. Hummel, J. W., Levan, M. A., and Sudduth, K. A. (1989). Mini-rhizotron installation in heavy soils. Trans. ASAE 32, 770-776.
69. Iversen, C. M., Murphy, M. T., Allen, M. F., Childs, J., Eissenstat, D. M., Lilleskov, E. A., et al. (2011). Advancing the use of minirhi-zotrons in wetlands. Plant Soil 352, 23-39. doi: 10.1007/s11104-011-0953-1
70. Jackson, R. B., Moore, L. A., Hoffmann, W. A., Pockman, W. T., and Linder, C. R. (1999). Ecosystem rooting depth determined with caves and DNA. Proc. Natl. Acad. Sci. U.S.A. 96, 11387-11392. doi: 10.1073/pnas.96. 20.11387
71. Jennings, C. M. J. (1974). The hydro-geology of Botswana. PhD thesis, University of Natal, South Africa, p. 873.
72. Johnson, M. G., Tingey, D. T., Phillips, D. L., and Storm, M. J. (2001). Advancing fine root research with minirhizotrons. Environ. Exp. Bot. 45, 263-289. doi: 10.1016/S0098-847200077-6
73. Justin, S. H. F. W., and Armstrong, W. (1987). The anatomical characteristics of roots and plant response to soil flooding. New Phytol. 106, 465-495. doi: 10.1111/j.1469-8137.1987.tb00153.x
74. Kage, H., Kochler, M., and Stutzel, H. (2000). Root growth of cauliflower (Brassica oleracea L. botrytis) under unstressed conditions: measurement and modelling. Plant Soil 223, 131-145. doi: 10.1023/A:3A1004866823128
75. Kato, Y., Abe, J., Kamoshita, A., and Yamagishi, J. (2006). Genotypic variation in root growth angle in rice (Oryza sativa L.) and its association with deep root development in upland fields with different water regimes. Plant Soil 287, 117-129. doi: 10.1007/s11104-006-9008-4
76. Kell, D. B. (2011). Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration. Ann. Bot. 108, 407-418. doi: 10.1093/aob/mcr175
77. Kleidon, A., and Heimann, M. (2000). Assessing the role of deep rooted vegetation in the climate system with model simulations: mechanism, comparison to observations and implications for Amazonian deforestation. Clim. Dynam. 16, 183-199. doi: 10.1007/s003820050012
78. Kloeppel, B. D., and Gower, S. T. (1995). Construction and installation of acrylic minirhizotron tubes in forest ecosystems. Soil Sci. Soc. Am. J. 59, 241-243.
79. Koarashi, J., Hockaday, W. C., Masiello, C. A., and Trumbore, S. E. (2012). Dynamics of decadally cycling carbon in subsurface soils. J. Geophys. 117, G03033. doi: 10.1029/2012JG002034
80. Kornecki, T. S., Prior, S. A., Runion, G. B., Rogers, H. H., and Erbach, D. C. (2008). Hydraulic core extraction: cutting device for soil-root studies. Commun. Soil Sci. Plant 39, 1080-1089. doi: 10.1080/00103620801925588
81. Kristensen, H. L., and Thorup-Kristensen, K. (2004). Uptake of 15N labeled nitrate by root systems of sweet corn, carrot and white cabbage from 0.2-2.5 meters depth. Plant Soil 265, 93-100. doi: 10.1007/s11104-005-0696-y
82. Kristensen, H. L., and Thorup-Kristensen, K. (2007). Effects of vertical distribution of soil inorganic nitrogen on root growth and subsequent nitrogen uptake by field vegetable crops. Soil Use Manage. 23, 338-347. doi: 10.1111/j.1473-2743.2007.00105.x
83. Kutschera, L., and Lichtenegger, E. (1997). Bewurzelung Von Pflanzen in Vers c h ie de ne n Le be n s rä um e n. Linz: Landesmuseum.
84. Laclau, J.-P., Ranger, J., De Moraes Gonçalves, J. L., Maquère, V., Krusche, A. V., M'Bou, A. T., et al. (2010). Biogeochemical cycles of nutrients in tropical Eucalyptus plantations. For. Ecol. Manage. 259, 1771-1785. doi: 10.1016/j.foreco.2009.06.010
85. Laclau, J.-P., Silva, E. a. D., Rodrigues Lambais, G., Bernoux, M., Le Maire, G., Stape, J. L., et al. (2013). Dynamics of soil exploration by fine roots down to a depth of 10 m throughout the entire rotation in Eucalyptus grandis plantations. Front. Plant Sci. 4:243. doi: 10.3389/fpls.2013.00243
86. Laio, F., Tamea, S., Ridolfi, L., D'Odorico, P., and Rodriguez-Iturbe, I. (2009). Ecohydrology of groundwater-dependent ecosystems: 1. Stochastic water table dynamics. Water Resour. Res. 45, 1-13. doi: 10.1029/2008 WR007292
87. Lambers, H., Shane, M. W., Cramer, M. D., Pearse, S. J., and Veneklaas, E. J. (2006). Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann. Bot. 98, 693-713. doi: 10.1093/aob/mcl114
88. Lewis, D. C., and Burgy, R. H. (1964). The Relationship between oak tree roots and groundwater in fractured rock as determined by tritium tracing. J. Geophys. 69, 2579-2588. doi: 10.1029/JZ069i012 p02579
89. Lorenz, K., and Lal, R. (2005). The depth distribution of soil organic carbon in relation to land use and management and the potential of carbon sequestration in subsoil horizons. Adv. Agron. 88, 35-66. doi: 10.1016/S0065-211388002-2
90. Maeght, J. L., Henry des Tureaux, T., Sengtaheuanghoung, O., Stokes, A., Ribolzi, O., and Pierret, A. (2012). "Drought effect on teak tree (Tectona grandis) roots on carbon inputs and water uptake in a deep soil of northern Laos," in Roots to The Future 8th Symposium of the International Society of Root Research (Dundee).
91. Maeght, J.-L., Pierret, A., Sanwangsri, M., and Hammecker, C. (2007). "Field monitoring of rice rhizosphere dynamics in saline soils of NE Thailand," in International Conference Rhizosphere (Montpellier), 26-31.
92. Majdi, H., Pregitzer, K., Morén, A.-S., Nylund, J.-E., and Ågren, G. I. (2005). Measuring fine root turnover in forest ecosystems. Plant Soil 276, 1-8. doi: 10.1007/s11104-005-3104-8
93. Malézieux, E., Crozat, Y., Dupraz, C., Laurans, M., Makowski, D., Ozier-Lafontaine, H., et al. (2009). Mixing plant species in cropping systems: concepts, tools and models. A review. Agron. Sustain. Dev. 29, 43-62. doi: 10.1051/agro: 2007057
94. McCormack, M. L., Eissenstat, D., Prasad, A., and Smithwick, E. (2013). Regional scale patterns of fine root lifespan and turnover under current and future climate. Global Change Biol. 19, 1697-1708. doi: 10.1111/gcb.12163
95. McCulley, R. L., Jobbágy, E. G., Pockman, W. T., and Jackson, R. B. (2004). Nutrient uptake as a contributing explanation for deep rooting in arid and semi-arid ecosystems. Oecologia 141, 620-628. doi: 10.1007/s00442-004-1687-z
96. McElrone, A. J., Bichler, J., Pockman, W. T., Addington, R. N., Linder, C. R., and Jackson, R. B. (2007). Aquaporin-mediated changes in hydraulic conductivity of deep tree roots accessed via caves. Plant Cell Environ. 30, 1411-1421. doi: 10.1111/j.1365-3040.2007.01714.x
97. McElrone, A. J., Pockman, W. T., Martinez-Vilalta, J., and Jackson, R. B. (2004). Variation in xylem structure and function in stems and roots of trees to 20 m depth. New Phytol. 163, 507-517. doi: 10.1111/j.1469-8137.2004.01127.x
98. McMurtrie, R. E., Iversen, C. M., Dewar, R. C., Medlyn, B. E., Näsholm, T., Pepper, et al. (2012). Plant root distributions and nitrogen uptake predicted by a hypothesis of optimal root foraging. Ecol. Evol. 2, 1235-1250. doi: 10.1002/ece3.266
99. Meyer, B. S., and Anderson, D. B. (1939). Plant Physiology. Bridgebort, CT: Braunworth and co.
100. Michot, D. (2003). Spatial and temporal monitoring of soil water content with an irrigated corn crop cover using surface electrical resistivity tomography. Wa ter Res o ur. Res. 39, 1138. doi: 10.1029/2002WR001581
101. Misra, R. K., Dexter, A. R., and Alston, A. M. (1986). Maximum axial and radial growth pressures of plant roots. Plant Soil 95, 315-326. doi: 10.1007/BF02374612
102. Mitchell, P., and Black, J. (1968). Distribution of peach roots under pasture and cultivation. Aust. J. Exp. Agric. 8, 106-111. doi: 10.1071/EA9680106
103. Moran, C. J., Pierret, A., and Stevenson, A. W. (2000). X-ray absorption and phase contrast imaging to study the interplay between plant roots and soil structure. Plant Soil 223, 99-115. doi: 10.1023/A:1004835813094
104. Mulia, R., and Dupraz, C. (2006). Unusual fine root distributions of two deciduous tree species in southern France: what consequences for modelling of tree root dynamics. Plant Soil 281, 71-85. doi: 10.1007/s11104-005-3770-6
105. Nakaji, T., Noguchi, K., and Oguma, H. (2008). Classification of rhi-zosphere components using visible-near infrared spectral images. Plant Soil 310, 245-261. doi: 10.1007/s11104-007-9478-z.
106. Nepstad, D., de Carvalho, C., and Davidson, E. (1994). The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures. Nature 372, 666-669. doi: 10.1038/372666a0
107. Newton, M., and Zedaker, S. M. (1981). Excavating Roots With Explosives. Corvallis, OR: Oregon State University, Forest Research Laboratory.
108. Nicoullaud, B., Darthout, R., Duval, O., Le Lay, D. C., and Terrasse, B. R. B. (1995). Étude de l'enracinement du blé tendre d'hiver et du maïs dans les sols argilo-limoneux de Petite beauce. Etud. Gest. Sols 2, 183-200.
109. Novak, T., and Perc, M. (2012). Duality of terrestrial subterranean fauna. Int. J. Speleol. 41, 181-188. doi: 10.5038/1827-806X.41.2.5
110. Oliveira, R. S., Dawson, T. E., Burgess, S. S. O., and Nepstad, D. C. (2005). Hydraulic redistribution in three Amazonian trees. Oecologia 145, 354-363. doi: 10.1007/s00442-005-0108-2
111. Passioura, J. B., and Wetselaar, R. (1972). Consequences of banding nitrogen fertilizers in soil. Plant Soil 36, 461-473. doi: 10.1007/BF01373498
112. Peñuelas, J., and Filella, I. (2003). Deuterium labelling of roots provides evidence of deep water access and hydraulic lift by Pinus nigra in a Mediterranean forest of NE Spain. Environ. Exp. Bot. 49, 201-208. doi: 10.1016/S0098-847200070-9
113. Phillips, D. L., Johnson, M. G., Tingey, D. T., Biggart, C., Nowak, R. S., and Newsom, J. C. (2000). Minirhizotron installation in sandy, rocky soils with minimal soil disturbance. Soil Sci. Soc. Am. J. 64, 761. doi: 10.2136/sssaj2000.64 2761x
114. Poelman, G., van de Koppel, J., and Brouwer, G. (1996). A telescopic method for photographing within 8×8 cm minirhizotrons. Plant Soil 185, 163-167. doi: 10.1007/BF02257572
115. Poot, P., and Lambers, H. (2008). Shallow-soil endemics: adaptive advantages and constraints of a specialized root-system morphology. New Phytol. 178, 371-381. doi: 10.1111/j.1469-8137.2007.02370
116. Pregitzer, K. K. S., Laskowski, M. J. M., Burton, A. J., Lessard, C., and Zak, D. R. (1998). Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiol. 18, 665-670. doi: 10.1093/treephys/18.10.665
117. Rasse, D. P., Rumpel, C., and Dignac, M.-F. (2005). Is soil carbon mostly root carbon. Mechanisms for a specific stabilisation. Plant Soil 269, 341-356. doi: 10.1007/s11104-004-0907-y.
118. Rawitscher, F. (1948). The water economy of the vegetation of the Campos cerrados in southern Brazil. J. Ecol. 36, 237-268.
119. Reboleira, A. S., Borges, P., Gonçalves, F., Serrano, A., and Oromí, P. (2011). The subterranean fauna of a biodiversity hotspot region-Portugal: an overview and its conservation. Int. J. Speleol. 40, 23-37. doi: 10.5038/1827-806X.40.1.4
120. Rewald, B., and Ephrath, J. E. (2013). "Minirhizotron techniques," in Plant Roots: The Hidden Half, eds A. Eshel and T. Beeckman (New York, NY: CRC Press), 421-4215.
121. Rewald, B., and Leuschner, C. (2009). Does root competition asymmetry increase with water availability. Plant Ecol. Divers. 2, 255-264. doi: 10.1080/17550870903022865
122. Rewald, B., Meinen, C., Trockenbrodt, M., Ephrath, J. E., and Rachmilevitch, S. (2012). Root taxa identification in plant mixtures - current techniques and future challenges. Plant Soil 359, 165-182. doi: 10.1007/s11104-012-1164-0
123. Richards, J., and Caldwell, M. (1987). Hydraulic lift: Substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia, 486-489. doi: 10.1007/BF00379405
124. Richter, A. K., and Walthert, L. (2007). Does low soil base saturation affect fine root properties of European beech (Fagus sylvatica L.). Plant Soil 298, 60-79. doi: 10.1007/s11104-007-9338-x
125. Richter, D. D., and Markewitz, D. (1995). How deep is soil. Bioscience 45, 600-609. doi: 10.2307/1312764
126. Ritson, P., and Sochacki, S. (2003). Measurement and prediction of biomass and carbon content of Pinus pinaster trees in farm forestry plantations, south-western Australia. For. Ecol. Manage. 175, 103-117. doi: 10.1016/S0378-112700121-4
127. Rizzo, D., and Gross, R. (2000). "Distribution of Armillaria on pear root systems and comparison of excavation techniques," in The Supporting Roots of Trees and Woody Plants: Form, Function and Physiology, ed A. Stokes (Dordrecht: Kluwer Academic Publishers), 305-311.
128. Robinson, D. (1991). "Roots and resource fluxes in plants and communities," in Plant Root Growth: An Ecological Perspective, ed D. Atkinson (Oxford: Blackwell Scientific), 103-130.
129. Robinson, D., Crop, S., and Dd, D. (1996). Resource capture by localized root proliferation: why do plants bother. Ann. Bot. 77, 179-186. doi: 10.1006/anbo.1996. 0020
130. Rosling, A., Landeweert, R., Lindahl, B. D., Larsson, K.-H., Kuyper, T. W., Taylor, A. F. S., et al. (2003). Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol. 159, 775-783. doi: 10.1046/j. 1469-8137.2003.00829.x
131. Rumpel, C., and Kögel-Knabner, I. (2011). Deep soil organic matter-a key but poorly understood component of terrestrial C cycle. Plant Soil 338, 143-158. doi: 10.1007/s11104-010-0391-5.
132. Santner, A., Calderon-Villalobos, L. I. A., and Estelle, M. (2009). Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol. 5, 301-307. doi: 10.1038/nchembio.165
133. Schenk, H. J. (2008). Soil depth, plant rooting strategies and species' niches. New Phytol. 178, 223-225. doi: 10.1111/j.1469-8137.2008.02427.x
134. Schenk, H. J., and Jackson, R. B. (2002). The global biogeogra-phy of roots. Ecol. Monogr. 72, 311-328. doi: 10.1890/0012-9615072[0311:TGBOR]2.0.CO;2
135. Schwinning, S. (2010). The ecohydrol-ogy of roots in rocks. Ecohydrology 245, 238-245. doi: 10.1002/eco.134
136. Sekiya, N., Araki, H., and Yano, K. (2010). Applying hydraulic lift in an agroecosystem: forage plants with shoots removed supply water to neighboring vegetable crops. Plant Soil 341, 39-50. doi: 10.1007/s11104-010-0581-1
137. Shalyt, M. S. (1950). Podzemnaja cast' nekotorykh lugovykh, stepnykh i pustynnykh rastenyi i fitocenozov. C. I. Travjanistye i polukustarnigkovye rastenija i fitocenozy lesnoj (luga) i stepnoj zon. (Belowground parts of some meadow, steppe, and desert plants and plant communities. Part I: Herbaceous plants and subshrubs and plant communities of forest and steppe zones. In Russian). Trudy Botanicheskogo Instituta im. V.L. Komarova. Akademii nauk SSSR. Seriia III, Geobotanika 6, 205-442.
138. Shimamura, S., Yoshida, S., and Mochizuki, T. (2007). Cortical aerenchyma formation in hypocotyl and adventitious roots of Luffa cylindrica subjected to soil flooding. Ann. Bot. 100, 1431-1439. doi: 10.1093/aob/mcm239
139. Silva, J. S., and Rego, F. C. (2003). Root distribution of a Mediterranean shrubland in Portugal. Plant Soil 255, 529-540. doi: 10.1023/A:1026029031005
140. Silva, M. S., Martins, R. P., and Ferreira, R. L. (2011). Cave lithol-ogy determining the structure of the invertebrate communities in the brazilian atlantic rain forest. Biodivers. Conserv. 20, 1713-1729. doi: 10.1007/s10531-011-0057-5
141. Silva, S., Whitford, W. G., Jarrell, W. M., and Virginia, R. A. (1989). The microarthropod fauna associated with a deep rooted legume, Prosopis glandulosa, in the Chihuahuan Desert. Biol. Fert. Soils 7, 330-335. doi: 10.1007/BF00257828.
142. Smit, A. L., Bengough, A. G., Engels, C., van Noordwijk, M., Pellerin, S., van de Geijn, S. C. (2000). Root Methods: A Handbook. Berlin: Springer.
143. Snider, J., Moya, M., Garcia, M. G., Spilde, M. N., and Northup, D. E. (2009). "Identification of the micro-bial communities associated with roots in lava tubes in new mexico an Hawai," in Proceedings of the15th International Congress of Speleology, Vol. 2 (Kerrville, TX), 718-723.
144. Snyder, K. a., James, J. J., Richards, J. H., and Donovan, L. a. (2008). Does hydraulic lift or nighttime transpiration facilitate nitrogen acquisition. Plant Soil 306, 159-166. doi: 10.1007/s11104-008-9567-7
145. Stoeckeler, J. H., and Kluender, W. A. (1938). The hydraulic method of excavating the root systems of plants. Ecology 19, 355-369.
146. Stone, E. L., and Comerford, N. B. (1994). "Plant and animal activity below the solum," in Proceedings of a Symposium on Whole Regolith Pedology (Minneapolis, MN), 57-74. doi: 10.2136/sssaspecpub34.c4
147. Stone, E. L., and Kalisz, P. J. (1991). On the maximum extent of tree roots. For. Ecol. Manage. 46, 59-102. doi: 10.1016/0378-112790245-Q
148. Stone, F. D. (2010). "Bayliss lava tube and the discovery of a rich cave fauna in tropical Australia," in 14th International Symposium on Vulcanospeleology, (Undara Volcanic National Park, Queensland), 47-58.
149. Strebel, O., Duynisveld, W. H. M., and Böttcher, J. (1989). Nitrate pollution of groundwater in Western Europe. Agric. Ecosyst. Environ. 26, 189-214. doi: 10.1016/0167-880990013-3
150. Strong, D., Sale, P., and Helyar, K. (1999). The influence of the soil matrix on nitrogen mineralisation and nitrification III. Predictive utility of traditional variables and process location within the pore. Aust. J. Soil Res. 37, 137-149.
151. Sverdrup, H., Hagen-Thorn, A., Holmqvist, J., Wallman, P., Warfvinge, P., Walse, C., et al. (2002). "Biogeochemical processes and mechanisms. Developing principles and models for sustainable forestry in Sweden," in Managing Forest Ecosystems, Vol. 5, eds H. Sverdrup and I. Stjernquist (Dordrecht: Kluwer Academic Publishers), 91-196.
152. Thorup-Kristensen, K. (2001). Are differences in root growth of nitrogen catch crops important for their ability to reduce soil nitrate-N content, and how can this be measured? Plant Soil 230, 185-195.
153. Thorup-Kristensen, K., Nielsen, N. E. (1998). Modelling and measuring the effect of nitrogen catch crops on the nitrogen supply for succeeding crops. Plant Soil 203, 79-89. doi: 10.1023/A:1004398131396
154. Trachsel, S., Kaeppler, S. M., Brown, K. M., and Lynch, J. P. (2010). Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant Soil 341, 75-87. doi: 10.1007/s11104-010-0623-8
155. Trumbore, S. E., and Gaudinski, J. B. (2003). Atmospheric science. the secret lives of roots. Science 302, 1344-1345. doi: 10.1126/sci-ence.1091841
156. Vanapalli, S. K., and Oh, W. T. (2012). "Stability analysis of unsupported vertical trenches in unsaturated soils," in GeoCongress 2012, (Reston, VA: American Society of Civil Engineers), 2502-2511. doi: 10.1061/9780784412121.256
157. Van Noordwijk, M., Brouwer, G., Meijboom, F., Dorosario G Oliveira, M., and Bengough, A. (2000). "Trench profile techniques and core break methods," in Root methods, eds A. L. Smit, A. G.
158. Bengough, C. Engels, M. van Noordwijk, S. Pellerin, and B. H. Van der Geijn (Berlin: Springer), 212-233.
159. Virginia, R. A., Jenkins, M. B., and Jarrell, W. M. (1986). Depth of root symbiont occurrence in soil. Biol. Fert. Soils 2, 127-130. doi: 10.1007/ BF00257591
160. Vogt, K. A., Vogt, D. J., Palm iot to, P. A., Boon, P., and Jennifer, O. H. (1996). Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species. Plant Soil 187, 159-219. doi: 10.1007/BF 00017088
161. Vos, J., and Groenwold, J. (1983). Estimation of root densities by observation tubes and endoscope. Plant Soil 300, 295-300. doi: 10.1007/BF02143621
162. Waddington, J. (1971). Observation of plant roots in situ. Can. J. Bot. 49, 1850-1852. doi: 10.1139/ b71-261.
163. Wagner, B., Gärtner, H., Ingensand, H., and Santini, S. (2010). Incorporating 2D tree-ring data in 3D laser scans of coarse-root systems. Plant Soil 334, 175-187. doi: 10.1007/s11104-010-0370-x
164. Wardle, D. A., Bardgett, R. D., Klironomos, J. N., Heikki, S., van der Putten, W. H., and Wall, D. H. (2004). Ecological linkages between aboveground and belowground biota. Science 304, 1629-1633. doi: 10.1126/science.1094875
165. Wearver, J. E. (1915). A study of the root-systems of prairie plants of south eastern Washington. Plant Wo r l d 18, 227-248.
166. Weaver, J. E. (1919). The Ecological Relations of Roots. Publication No. 286. Washington, DC: Carnegie Institu-tion of Washington
167. Weaver, J. E., and Bruner, W. E. (1927). Root Development of Vegetable Crops. New York, NY: McGraw-Hill Book Company.
168. Zapater, M., Hossann, C., Bréda, N., Bréchet, C., Bonal, D., and Granier, A. (2011). Evidence of hydraulic lift in a young beech and oak mixed forest using 18O soil water labelling. Trees 25, 885-894. doi: 10.1007/s00468-011-0563-9