Plant and Soil

, Volume 401, Issue 1–2, pp 409–426 | Cite as

Unexpected phenology and lifespan of shallow and deep fine roots of walnut trees grown in a silvoarable Mediterranean agroforestry system

  • Amandine Germon
  • Rémi Cardinael
  • Iván Prieto
  • Zhun Mao
  • John Kim
  • Alexia Stokes
  • Christian Dupraz
  • Jean-Paul Laclau
  • Christophe Jourdan
Regular Article

Abstract

Background and Aims

Fine roots play a major role in the global carbon cycle through respiration, exudation and decomposition processes, but their dynamics are poorly understood. Current estimates of root dynamics have principally been observed in shallow soil horizons (<1 m), and mainly in forest systems. We studied walnut (Juglans regia × nigra L.) fine root dynamics in an agroforestry system in a Mediterranean climate, with a focus on deep soils (down to 5 m), and root dynamics throughout the year.

Methods

Sixteen minirhizotron tubes were installed in a soil pit, at depths of 0.0–0.7, 1.0–1.7, 2.5–3.2 and 4.0–4.7 m and at two distances from the nearest trees (2 and 5 m). Fine root (diameter ≤ 2 mm) dynamics were recorded across three diameter classes every 3 weeks for 1 year to determine their phenology and turnover in relation to soil depth, root diameter and distance from the tree row.

Results

Deep (>2.5 m) root growth occurred at two distinct periods, at bud break in spring and throughout the winter i.e., after leaf fall. In contrast, shallow roots grew mainly during the spring-summer period. Maximum root elongation rates ranged from 1 to 2 cm day−1 depending on soil depth. Most root mortality occurred in upper soil layers whereas only 10 % of fine roots below 4 m died over the study period. Fine root lifespan was longer in thicker and in deeper roots with the lifespan of the thinnest roots (0.0–0.5 mm) increasing from 129 days in the topsoil to 190 at depths > 2.5 m.

Conclusions

The unexpected growth of very deep fine roots during the winter months, which is unusual for a deciduous tree species, suggests that deep and shallow roots share different physiological strategies and that current estimates based on the shortest root growth periods (i.e., during spring and summer) may be underestimating root production. Although high fine root turnover rates might partially result from the minirhizotron approach used, our results help gain insight into some of the factors driving soil organic carbon content.

Keywords

Alley cropping Juglans Deep root growth Root elongation rate Root mortality Root turnover 

Notes

Acknowledgments

This study was financed by the French ANR funded project ECOSFIX (Ecosystem Services of Roots - Hydraulic Redistribution, Carbon Sequestration and Soil Fixation, ANR-2010-STRA-003-01), by the ADEME funded project AGRIPSOL (Agroforestry for soil protection) and by la Fondation de France. We thank the farmers Mr. Henri and Alain Breton, for their authorization to open the deep pit. We are very grateful to our INRA colleagues Jean-François Bourdoncle, Lydie Dufour, Alain Sellier and Didier Arnal for their help with field and laboratory work and logistics. The Restinclières farm is the property of the Conseil Départemental de l’Hérault, which provides financial support to INRA since 1995 for the monitoring of agroforestry systems, and their support is warmly appreciated.

Supplementary material

11104_2015_2753_MOESM1_ESM.docx (28 kb)
ESM 1 (DOCX 28 kb)
11104_2015_2753_Fig8_ESM.jpg (2.7 mb)
Figure S1

Ombrothermic diagram of the study period; monthly mean air temperature (°C) and monthly rainfall (mm). (JPG 2.72 mb)

11104_2015_2753_Fig9_ESM.jpg (2.8 mb)
Figure S2

Mean daily root elongation rate (RER, cm day-1) at a depth of 0.0-0.7 m in the pit and in the plot over time. Vertical bars represent standard deviations (not shown when smaller than the symbol size). (JPG 2.75 mb)

References

  1. Anderson LJ, Comas LH, Lakso AN, Eissenstat DM (2003) Multiple risk factors in root survivorship: a 4-year study in Concord grape. New Phytol 158:489–501CrossRefGoogle Scholar
  2. Andrianarisoa KS, Dufour L, Bienaime S, Zeller B, Dupraz C (2015) The introduction of hybrid walnut trees (Juglans nigra x regia cv. NG23) into cropland reduces soil mineral N content in autumn in southern France. Agrofor Syst, in pressGoogle Scholar
  3. Baddeley JA, Watson CA (2005) Influences of root diameter, tree age, soil depth and season on fine root survivorship in Prunus avium. Plant Soil 276:15–22CrossRefGoogle Scholar
  4. Balandier P, Dupraz C (1999) Growth of widely spaced trees. A case study from young agroforestry plantations in France. Agrofor Syst 99:151–167Google Scholar
  5. Balesdent J, Balabane M (1996) Major contribution of roots to soil carbon storage inferred from maize cultivated soils. Soil Biol Biochem 28:1261–1263CrossRefGoogle Scholar
  6. Berg B, McClaugherty C (2008) Plant litter: decomposition, humus formation, carbon sequestration, 2nd ed, 340p. Springer Verlag Berlin Heidelberg, BerlinCrossRefGoogle Scholar
  7. Bergeron M, Lacombe S, Bradley RL, Whalen J, Cogliastro A, Jutras MF, Arp P (2011) Reduced soil nutrient leaching following the establishment of tree-based intercropping systems in eastern Canada. Agrofor Syst 83:321–330CrossRefGoogle Scholar
  8. Beyer F, Hertel D, Jung K, Fender AC, Leuschner C (2013) Competition effects on fine root survival of Fagus sylvatica and Fraxinus excelsior. For Ecol Manag 302:14–22CrossRefGoogle Scholar
  9. Binkley D (2015) Ecosystems in four dimensions. New Phytol 206:883–885CrossRefPubMedGoogle Scholar
  10. Brunner I, Bakker MR, Björk RG, Hirano Y, Lukac M, Aranda X, Børja I, Eldhuset TD, Helmisaari HS, Jourdan C, Konôpka B, López BC, Pérez CM, Persson H, Ostonen I (2013) Fine-root turnover rates of European forests revisited: an analysis of data from sequential coring and ingrowth cores. Plant Soil 362:357–372CrossRefGoogle Scholar
  11. Burgess PJ, Incoll LD, Corry DT, Beaton A, Hart BJ (2004) Poplar (Populus spp) growth and crop yields in a silvoarable experiment at three lowland sites in England. Agrofor Syst 63:157–169CrossRefGoogle Scholar
  12. Burke MK, Raynal DJ (1994) Fine root growth phenology, production, and turnover in a northern hardwood forest ecosystem. Plant Soil 162:135–146CrossRefGoogle Scholar
  13. Cardinael R, Mao Z, Prieto I, Stokes A, Dupraz C, Kim JH, Jourdan C (2015a) Competition with winter crops induces deeper rooting of walnut trees in a Mediterranean alley cropping agroforestry system. Plant Soil 391:219–235CrossRefGoogle Scholar
  14. Cardinael R, Chevallier T, Barthès BG, Saby NPA, Parent T, Dupraz C, Bernoux M, Chenu C (2015b) Impact of agroforestry on stocks, forms and spatial distribution of soil organic carbon - A case study in a Mediterranean context. Geoderma 259–260:288–299CrossRefGoogle Scholar
  15. Chantereau J, Goislot K, Albaric L, Thellier T, Fabre D (2012) Synchronism between adventitious root and leaf development in hydroponic sorghum. J SAT Agric Res 10:1–5Google Scholar
  16. Chaudhry AK, Khan GS, Siddiqui MT, Akhtar M, Aslam Z (2003) Effect of arable crops on the growth of poplar (Populus deltoides) tree in agroforestry system. Pak J Agric Sci 40:82–85Google Scholar
  17. Cheng W, Coleman DC, Box JE Jr (1991) Measuring root turnover using the minirhizotron technique. Agric Ecosyst Environ 34:261–267CrossRefGoogle Scholar
  18. Clough Y, Barkmann J, Juhrbandt J, Kessler M, Wanger TC, Anshary A, Buchori D, Cicuzza D, Darras K, Putra DD, Erasmi S, Pitopang R, Schmidt C, Schulze CH, Seidel D, Steffan-Dewenter I, Stenchly K, Vidal S, Weist M, Wielgoss AC, Tscharntke T (2011) Combining high biodiversity with high yields in tropical agroforests. PNAS 108:8311–8316CrossRefPubMedPubMedCentralGoogle Scholar
  19. Cox DR (1972) Regression models and life-tables. J Roy Stat Soc B 34:187–220Google Scholar
  20. Crawley MJ (2012) The R Book, Second Edition. 27. Survival analysis. Wiley, 1218 p.Google Scholar
  21. Desrochers A, Landhäusser SM, Lieffers VJ (2002) Coarse and fine root respiration in aspen (Populus tremuloides). Tree Physiol 22:725–732CrossRefPubMedGoogle Scholar
  22. Dufour L, Metay A, Talbot G, Dupraz C (2013) Assessing light competition for cereal production in temperate agroforestry systems using experimentation and crop modelling. J Agron Crop Sci 199:217–227CrossRefGoogle Scholar
  23. Dupraz C, Fournier C, Balvay Y, Dauzat M, Pesteur S, Simorte V (1999) Influence de quatre années de culture intercalaire de blé et de colza sur la croissance de noyers hybrides en agroforesterie. Bois et Fôrets des Agriculteurs Actes du colloque de Clermont-Ferrand 20:95–114Google Scholar
  24. Dupraz C, Liagre F (2008) Agroforesterie, des arbres et des cultures. Editions France-Agricole, Paris, p 413Google Scholar
  25. Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782CrossRefGoogle Scholar
  26. Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60CrossRefGoogle Scholar
  27. Espeleta JF, West JB, Donovan LA (2009) Tree species fine-root demography parallels habitat specialization across a sandhill soil resource gradient. Ecology 90:1773–1787CrossRefPubMedGoogle Scholar
  28. Fornara DA, Tilman D, Hobbie SE (2009) Linkages between plant functional composition, fine root processes and potential soil N mineralization rates. J Ecol 97:48–56CrossRefGoogle Scholar
  29. Gavaland A, Burnel L (2005) Croissance et biomasse aérienne de noyers noirs. Chambres d’agriculture 945:20–21Google Scholar
  30. Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31CrossRefGoogle Scholar
  31. Goel MK, Khanna P, Kishore J (2010) Understanding survival analysis: Kaplan-Meier estimate. Int J Ayurveda Res 1:274–278CrossRefPubMedPubMedCentralGoogle Scholar
  32. Graefe S, Hertel D, Leuschner C (2008) Estimating fine root turnover in tropical forests along an elevational transect using minirhizotrons. Biotropica 40(536):542Google Scholar
  33. Guo D, Li H, Mitchell RJ, Han W, Hendricks JJ, Fahey TJ, Hendrick RL (2008a) Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytol 177:443–456PubMedGoogle Scholar
  34. Guo D, Mitchell RJ, Withington JM, Fan PP, Hendricks JJ (2008b) Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. J Ecol 96:737–745CrossRefGoogle Scholar
  35. Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia 140:450–457CrossRefPubMedGoogle Scholar
  36. Hendrick RL, Pregitzer KS (1993) Patterns of fine root mortality in two sugar maple forests. Nature 361:59–61CrossRefGoogle Scholar
  37. Hendrick RL, Pregitzer KS (1996) Temporal and depth-related patterns of fine root dynamics in northern hardwood forests. J Ecol 84:167–176CrossRefGoogle Scholar
  38. Hendricks JJ, Hendrick RL, Wilson CA, Mitchell RJ, Pecot SD, Guo D (2006) Assessing the patterns and controls of fine root dynamics: an empirical test and methodological review. J Ecol 94:40–57CrossRefGoogle Scholar
  39. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195CrossRefGoogle Scholar
  40. IUSS Working Group WRB (2007) World Reference Base for Soil Resources 2006, first update 2007. World Soil Resources Reports No. 103. FAO, RomeGoogle Scholar
  41. Joslin JD, Henderson GS (1987) Organic matter and nutrients associated with fine root turnover in a white oak stand. For Sci 33:330–346Google Scholar
  42. Joslin JD, Gaudinski JB, Torn MS, Riley WJ, Hanson PJ (2006) Fine-root turnover patterns and their relationship to root diameter and soil depth in a 14C-labeled hardwood forest. New Phytol 172:523–535CrossRefPubMedGoogle Scholar
  43. Jourdan C, Silva EV, Gonçalves JLM, Ranger J, Moreira RM, Laclau J-P (2008) Fine root production and turnover in Brazilian Eucalyptus plantations under contrasting nitrogen fertilization regimes. For Ecol Manag 256:396–404CrossRefGoogle Scholar
  44. Keel SG, Campbell CD, Högberg MN, Richter A, Wild B, Zhou X, Hurry V, Linder S, Näsholm T, Högberg P (2012) Allocation of carbon to fine root compounds and their residence times in a boreal forest depend on root size class and season. New Phytol 194:972–981CrossRefPubMedGoogle Scholar
  45. Kell DB (2012) Large-scale sequestration of atmospheric carbon via plant roots in natural and agricultural ecosystems: why and how. Philos Trans R Soc Lond 367:1589–1597CrossRefGoogle Scholar
  46. Khan GS, Chaudhry AK (2007) Effect of spacing and plant density on the growth of poplar (Populus deltoides) trees under agro-forestry system. Pak J Agric Sci 44:321–327Google Scholar
  47. Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review. J Plant Nutr Soil Sci 163:421–431CrossRefGoogle Scholar
  48. Leshem B (1965) The annual activity of intermediary roots of the aleppo pine. For Sci 11:291–298Google Scholar
  49. Leshem B (1970) Resting roots of Pinus halepensis: structure, function, and reaction to water stress. Bot Gaz 131:99–104CrossRefGoogle Scholar
  50. Leuschner C (1998) Water extraction by tree fine roots in the forest floor of a temperate Fagus-Quercus forest. Ann Sci For 55:141–157CrossRefGoogle Scholar
  51. Livesley SJ, Gregory PJ, Buresh RJ (2000) Competition in tree row agroforestry systems. Distribution and dynamics of fine root length and biomass. Plant Soil 227:149–161CrossRefGoogle Scholar
  52. López B, Sabaté S, Gracia C (1998) Fine roots dynamics in a Mediterranean forest: effects of drought and stem density. Tree Physiol 18:601–606CrossRefPubMedGoogle Scholar
  53. Lorenz K, Lal R (2014) Soil organic carbon sequestration in agroforestry systems. A review. Agron Sustain Dev 34:443–454CrossRefGoogle Scholar
  54. M’bou AT, Jourdan C, Deleporte P, Nouvellon Y, Saint-André L, Bouillet J-P, Mialoundama F, Mabiala A, Epron D (2008) Root elongation in tropical Eucalyptus plantations: effect of soil content. Ann For Sci 65:609–609CrossRefGoogle Scholar
  55. Maeght J-L, Rewald B, Pierret A (2013) How to study deep roots-and why it matters. Front Plant Sci 4:299. doi: 10.3389/fpls.2013.00299 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Mainiero R, Kazda M (2006) Depth-related fine root dynamics of Fagus sylvatica during exceptional drought. For Ecol Manag 237:135–142CrossRefGoogle Scholar
  57. Majdi H, Andersson P (2005) Fine root production and turnover in a norway spruce stand in northern Sweden: effects of nitrogen and water manipulation. Ecosystems 8:191–199CrossRefGoogle Scholar
  58. Majdi H, Damm E, Nylund J-E (2001) Longevity of mycorrhizal roots depends on branching order and nutrient availability. New Phytol 150:195–202CrossRefGoogle Scholar
  59. Majdi H, Pregitzer K, Morén A-S, Nylund J-E, Ågren GI (2005) Measuring fine root turnover in forest ecosystems. Plant Soil 276:1–8CrossRefGoogle Scholar
  60. Mao Z, Bonis ML, Rey H, Saint-André L, Stokes A, Jourdan C (2013a) Which processes drive fine root elongation in a natural mountain forest ecosystem? Plant Ecol Divers 6:231–243CrossRefGoogle Scholar
  61. Mao Z, Jourdan C, Bonis ML, Pailler F, Rey H, Saint-André L, Stokes A (2013b) Modelling root demography in heterogeneous mountain forests and applications for slope stability analysis. Plant Soil 363:357–382CrossRefGoogle Scholar
  62. Matamala R, Gonzàlez-Meler MA, Jastrow JD, Norby RJ, Schlesinger WH (2003) Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302:1385–1387CrossRefPubMedGoogle Scholar
  63. McClaugherty CA, Aber JD (1982) The role of fine roots in the organic matter and nitrogen budgets of two forested ecosystems. Ecology 63:1481–1490CrossRefGoogle Scholar
  64. McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2014) Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology 95:2224–2235CrossRefPubMedGoogle Scholar
  65. McCormack ML, Guo D (2014) Impacts of environmental factors on fine root lifespan. Funct Plant Ecol 5:205. doi: 10.3389/fpls.2014.00205 Google Scholar
  66. McCormack ML, Gaines KP, Pastore M, Eissenstat DM (2015) Early season root production in relation to leaf production among six diverse temperate tree species. Plant Soil 398:121–129CrossRefGoogle Scholar
  67. Meier IC, Leuschner C (2008) Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Glob Chang Biol 14:2081–2095CrossRefGoogle Scholar
  68. Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095CrossRefPubMedGoogle Scholar
  69. Minchin PEH, Lacointe A (2005) New understanding on phloem physiology and possible consequences for modelling long-distance carbon transport. New Phytol 166:771–779CrossRefPubMedGoogle Scholar
  70. Misson L, Gershenson A, Tang J, McKay M, Cheng W, Goldstein A (2006) Influences of canopy photosynthesis and summer rain pulses on root dynamics and soil respiration in a young ponderosa pine forest. Tree Physiol 26:833–844CrossRefPubMedGoogle Scholar
  71. Mulia R, 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 281:71–85CrossRefGoogle Scholar
  72. Mulia R, Dupraz C, Van Noordwijk M (2010) Reconciling root plasticity and architectural ground rules in tree root growth models with voxel automata. Plant Soil 337:77–92CrossRefGoogle Scholar
  73. Muñoz F, Beer J (2001) Fine root dynamics of shaded cacao plantations in Costa Rica. Agrofor Syst 51:119–130CrossRefGoogle Scholar
  74. Oelbermann M, Paul Voroney R, Gordon AM (2004) Carbon sequestration in tropical and temperate agroforestry systems: a review with examples from Costa Rica and southern Canada. Agric Ecosyst Environ 104:359–377CrossRefGoogle Scholar
  75. Padilla FM, Pugnaire FI (2007) Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Funct Ecol 21:489–495CrossRefGoogle Scholar
  76. Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR (1998) Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiol 18:665–670CrossRefPubMedGoogle Scholar
  77. Pregitzer K, King J, Burton A, Brown S (2000) Responses of tree fine roots to temperature. New Phytol 147:105–115CrossRefGoogle Scholar
  78. Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine North American trees. Ecol Monogr 72:293–309CrossRefGoogle Scholar
  79. Prieto I, Roumet C, Cardinael R, Dupraz C, Jourdan C, Kim JH, Maeght JL, Mao Z, Pierret A, Portillo N, Roupsard O, Thammahacksa C, Stokes A (2015) Root functional parameters along a land-use gradient: evidence of a community-level economics spectrum. J Ecol 103:361–373CrossRefGoogle Scholar
  80. Radin JW, Parker LL, Sell CR (1978) Partitioning of sugar between growth and nitrate reduction in cotton roots. Plant Physiol 62:550–553CrossRefPubMedPubMedCentralGoogle Scholar
  81. Rasse DP, Rumpel C, Dignac MF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356CrossRefGoogle Scholar
  82. Richter DB, Billings SA (2015) ‘One physical system’: Tansley’s ecosystem as Earth’s critical zone. New Phytol 206:900–912CrossRefPubMedGoogle Scholar
  83. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  84. Satomura T, Fukuzawa K, Horikoshi T (2007) Considerations in the study of tree fine-root turnover with minirhizotrons. Plant Root 1:34–45CrossRefGoogle Scholar
  85. Schroth G, Zech W (1995) Above- and below-ground biomass dynamics in a sole cropping and an alley cropping system with Gliricidia sepium in the semi-deciduous rainforest zone of west Africa. Agrofor Syst 31:191–198CrossRefGoogle Scholar
  86. Solomon S, Plattnerb GK, Knuttic R, Friedlingstein P (2009) Irreversible climate change due to carbon dioxide emissions. Proc Natl Acad Sci 106:1704–1709CrossRefPubMedPubMedCentralGoogle Scholar
  87. Somarriba E (1992) Revisiting the past: an essay on agroforestry definition. Agrofor Syst 19:233–240CrossRefGoogle Scholar
  88. Strand AE, Pritchard SG, McCormack ML, Davis MA, Oren R (2008) Irreconcilable differences: fine-root life spans and soil carbon persistence. Science 319:456–458CrossRefPubMedGoogle Scholar
  89. Talbot G, Roux S, Graves A, Dupraz C, Marrou H, Wery J (2014) Relative yield decomposition: a method for understanding the behaviour of complex crop models. Environ Model Softw 51:136–148CrossRefGoogle Scholar
  90. Therneau T (2014) A package for survival analysis in S. R package version 2.37-7Google Scholar
  91. Tian X, Doerner P (2013) Root resource foraging: does it matter? Front Plant Sci 4:1–4CrossRefGoogle Scholar
  92. Tierney GL, Fahey TJ (2001) Evaluating minirhizotron estimates of fine root longevity and production in the forest floor of a temperate broadleaf forest. Plant Soil 229:167–176CrossRefGoogle Scholar
  93. Torquebiau EF (2000) A renewed perspective on agroforestry concepts and classification. Comptes rendus de l’Académie des sciences. Série III. Sci de la vie 323:1009–1017Google Scholar
  94. Tully KL, Lawrence D, Scanlon MT (2012) More trees less loss: nitrogen leaching losses decrease with increasing biomass in coffee agroforests. Agric Ecosyst Environ 161:137–144CrossRefGoogle Scholar
  95. Varah A, Jones H, Smith J, Potts SG (2013) Enhanced biodiversity and pollination in UK agroforestry systems. J Sci Food Agric 93:2073–2075CrossRefPubMedGoogle Scholar
  96. Waisel T, Eshel A, Beeckman T, Kafkafi U (2002) Plant roots: the hidden half, 3rd edn. Marcel Dekker, Inc., NewYorkGoogle Scholar
  97. Wells CE, Eissenstat DM (2001) Marked differences in survivorship among apple roots of different diameters. Ecology 82:882CrossRefGoogle Scholar
  98. Wells CE, Glenn DM, Eissenstat DM (2002) Changes in the risk of fine-root mortality with age: a case study in peach, Prunus persica (Rosaceae). Am J Bot 89:79–87CrossRefPubMedGoogle Scholar
  99. Willaume M, Pagès L (2006) How periodic growth pattern and source/sink relations affect root growth in oak tree seedlings. J Exp Bot 57:815–826CrossRefPubMedGoogle Scholar
  100. Withington JM, Elkin AD, Bułaj B, Olesiński J, Tracy KN, Bouma TJ, Oleksyn J, Anderson LJ, Modrzyński J, Reich PB, Eissenstat DM (2003) The impact of material used for minirhizotron tubes for root research. New Phytol 160:533–544CrossRefGoogle Scholar
  101. Xia M, Guo D, Pregitzer KS (2010) Ephemeral root modules in Fraxinus mandshurica. New Phytol 188:1065–1074CrossRefPubMedGoogle Scholar
  102. Young A (1997) Agroforestry for Soil Management. Wallingford UK p. 320Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Amandine Germon
    • 1
    • 2
  • Rémi Cardinael
    • 1
    • 3
  • Iván Prieto
    • 4
  • Zhun Mao
    • 5
    • 6
  • John Kim
    • 7
    • 8
  • Alexia Stokes
    • 7
  • Christian Dupraz
    • 1
  • Jean-Paul Laclau
    • 9
  • Christophe Jourdan
    • 9
  1. 1.INRA, UMR 1230 SystemMontpellierFrance
  2. 2.AgroParisTech - GEEFTMontpellier Cedex 4France
  3. 3.IRD, UMR 210 Eco&SolsMontpellierFrance
  4. 4.CNRS, CEFE UMR 5175Université de Montpellier – Université Paul Valéry – EPHEMontpellier Cedex 5France
  5. 5.Unité Ecosystèmes Montagnards, Centre de GrenobleIRSTEASaint-Martin-d’HèresFrance
  6. 6.Université Grenoble AlpesGrenobleFrance
  7. 7.INRA, UMR AMAPMontpellier Cedex 5France
  8. 8.Max Planck Institute for BiogeochemistryJenaGermany
  9. 9.CIRAD, UMR Eco&SolsMontpellierFrance

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