Plant and Soil

, Volume 424, Issue 1–2, pp 103–122 | Cite as

Linking above- and belowground phenology of hybrid walnut growing along a climatic gradient in temperate agroforestry systems

  • Awaz Mohamed
  • Alexia Stokes
  • Zhun Mao
  • Christophe Jourdan
  • Sylvie Sabatier
  • François Pailler
  • Stephane Fourtier
  • Lydie Dufour
  • Yogan Monnier
Regular Article


Background and aims

Plant phenology is a sensitive indicator of plant response to climate change. Observations of phenological events belowground for most ecosystems are difficult to obtain and very little is known about the relationship between tree shoot and root phenology. We examined the influence of environmental factors on fine root production and mortality in relation with shoot phenology in hybrid walnut trees (Juglans sp.) growing in three different climates (oceanic, continental and Mediterranean) along a latitudinal gradient in France.


Eight rhizotrons were installed at each site for 21 months to monitor tree root dynamics. Root elongation rate (RER), root initiation quantity (RIQ) and root mortality quantity (RMQ) were recorded frequently using a scanner and time-lapse camera. Leaf phenology and stem radial growth were also measured. Fine roots were classified by topological order and 0–1 mm, 1–2 mm and 2–5 mm diameter classes and fine root longevity and risk of mortality were calculated during different periods over the year.


Root growth was not synchronous with leaf phenology in any climate or either year, but was synchronous with stem growth during the late growing season. A distinct bimodal pattern of root growth was observed during the aerial growing season. Mean RER was driven by soil temperature measured in the month preceding root growth in the oceanic climate site only. However, mean RER was significantly correlated with mean soil water potential measured in the month preceding root growth at both Mediterranean (positive relationship) and oceanic (negative relationship) sites. Mean RIQ was significantly higher at both continental and Mediterranean sites compared to the oceanic site. Soil temperature was a driver of mean RIQ during the late growing season at continental and Mediterranean sites only. Mean RMQ increased significantly with decreasing soil water potential during the late aerial growing season at the continental site only. Mean root longevity at the continental site was significantly greater than for roots at the oceanic and Mediterranean sites. Roots in the 0–1 mm and 1–2 mm diameter classes lived for significantly shorter periods compared to those in the 2–5 mm diameter class. First order roots (i.e. the primary or parents roots) lived longer than lateral branch roots at the Mediterranean site only and first order roots in the 0–1 mm diameter class had 44.5% less risk of mortality than that of lateral roots for the same class of diameter.


We conclude that factors driving root RER were not the same between climates. Soil temperature was the best predictor of root initiation at continental and Mediterranean sites only, but drivers of root mortality remained largely undetermined.


Agroforestry Rhizotron Root elongation Initiation Mortality Longevity 



Soil water potential


Dormant season


Early growing season


Late growing season


Root elongation rate


Root initiation quantity


Root mortality quantity



Thanks are due to Jérôme Nespoulous, Luis Merino Martin and Merlin Ramel (INRA) for technical assistance, to Camille Béral (Agroof, France) for help finding field sites and to the farmers M. Queuille and M. Becue for letting us work in their agroforests.


Funding for a Ph.D. bursary was provided by Campus France and the Kurdish Institute, France (AM), la Fondation de France (YM) and fieldwork was funded by the FOARDAPT project, INRA metaprogram AAFCC (Adaptation of Agriculture and Forests to Climate Change), France.

Compliance with ethical standards

Competing interest

The authors declare that they have no competing interests.

Availability of data and materials

The datasets about root survivorship generated and/or analyzed during the current study are available in the [Zenodo] repository, “” . The other datasets generated and/or analyzed during the current study are available from the corresponding author on request.

Supplementary material

11104_2017_3417_MOESM1_ESM.docx (8.5 mb)
ESM 1 (DOCX 8678 kb)
11104_2017_3417_MOESM2_ESM.docx (39 kb)
ESM 2 (DOCX 39 kb)


  1. Abramoff RZ, Finzi AC (2015) Are above- and below-ground phenology in sync? New Phytol 205:1054–1061CrossRefPubMedGoogle Scholar
  2. Anderson L, Comas L, Lakso A, Eissenstat D (2003) Multiple risk factors in root survivorship: a 4- year study in concord grape. New Phytol 158:489–501CrossRefGoogle 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. Block RMA, Rees KCJ, Knight JD (2006) A review of fine root dynamics in Populus plantations. Agrofor Syst 67:73–84CrossRefGoogle Scholar
  5. Broschat TK (1998) Root and shoot growth patterns in four palm species and their relationships with air and soil temperatures. Hortscience 33:995–998Google Scholar
  6. Cardinael R, Mao Z, Prieto I, Stokes A, Dupraz C et al (2015) Competition with winter crops induces deeper rooting of walnut trees in a Mediterranean alley cropping agroforestry system. Plant Soil 391:219–235CrossRefGoogle Scholar
  7. Chen HY, Brassard BW (2013) Intrinsic and extrinsic controls of fine root life span. Crit Rev Plant Sci 32:151–161CrossRefGoogle Scholar
  8. Coll L, Camarero AJJ, Aragón JMD (2012) Fine root seasonal dynamics, plasticity, and Mycorrhization in 2 coexisting Mediterranean oaks with contrasting aboveground phenology. Ecoscience 19:238–245CrossRefGoogle Scholar
  9. Comas LH, Anderson L, Dunst R, Lakso A, Eissenstat D (2005) Canopy and environmental control of root dynamics in a long‐term study of Concord grape. New Phytol 167:829–40Google Scholar
  10. Contador ML, Comas LH, Metcalf SG, Stewart WL, Porris Gomez I et al (2015) Root growth dynamics linked to above-ground growth in walnut (Juglans Regia). Ann Bot-London 116:49–60CrossRefGoogle Scholar
  11. Diez JM, Ibáñez I, Miller-Rushing AJ, Mazer SJ, Crimmins TM et al (2012) Forecasting phenology: from species variability to community patterns. Ecol Lett 15:545–553CrossRefPubMedGoogle Scholar
  12. Du E, Fang J (2014) Linking belowground and aboveground phenology in two boreal forests in Northeast China. Oecologia 176:883–892CrossRefPubMedGoogle Scholar
  13. Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–362CrossRefPubMedGoogle Scholar
  14. Fukuzawa K, Shibata H, Takagi K, Satoh F, Koike T, Sasa K (2013) Temporal variation in fine-root biomass, production and mortality in a cool temperate forest covered with dense understory vegetation in northern Japan. For Ecol Manag 310:700–710CrossRefGoogle Scholar
  15. Gaudinski JB, Torn MS, Riley W, Swanston C, Trumbore SE, et al (2009) Use of stored carbon reserves in growth of temperate tree roots and leaf buds: analyses using radiocarbon measurements and modeling. Glob Chang Biol 15:992–1014Google Scholar
  16. Germon A, Cardinael R, Prieto I, Mao Z, Kim J et al (2016) Unexpected phenology and lifespan of shallow and deep fine roots of walnut trees grown in a silvoarable Mediterranean agroforestry system. Plant Soil 401:409–426CrossRefGoogle Scholar
  17. Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31CrossRefGoogle Scholar
  18. Green IJ, Dawson LA, Proctor J, Duff EI, Elston DA (2005) Fine root dynamics in a tropical rain forest is influenced by rainfall. Plant Soil 276:23–32CrossRefGoogle Scholar
  19. 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
  20. Guo D, Mitchell RJ, Withington JM, Fan P-P, Hendricks JJ (2008) 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
  21. Harris JR, Bassuk NL, Zobel RW, Whitlow TH (1995) Root and shoot growth periodicity of green ash, scarlet oak, turkish hazelnut, and tree lilac. J Am Soc Hortic Sci 120:211–216Google Scholar
  22. Hendrick RL, Pregitzer KS (1993a) The dynamics of fine root length, biomass, and nitrogen content in two northern hardwood ecosystems. Can J For Res 23:2507–2520CrossRefGoogle Scholar
  23. Hendrick RL, Pregitzer KS (1993b) Patterns of fine root mortality in 2 sugar maple forests. Nature 361:59–61CrossRefGoogle Scholar
  24. Hendrick RL, Pregitzer KS (1996a) Applications of minirhizotrons to understand root function in forests and other natural ecosystems. Plant Soil 185:293–304CrossRefGoogle Scholar
  25. Hendrick RL, Pregitzer KS (1996b) Temporal and depth-related patterns of fine root dynamics in northern hardwood forests. J Ecol 84:167–176CrossRefGoogle Scholar
  26. 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
  27. Hooker JE, Black KE, Perry RL, Atkinson D (1995) Arbuscular mycorrhizal fungi induced alteration to root longevity in poplar. Plant Soil 172:327–329Google Scholar
  28. Hubbart J, Link T, Campbell C, Cobos D (2005) Evaluation of a low- cost temperature measurement system for environmental applications. Hydrol Process 19:1517–1523CrossRefGoogle Scholar
  29. Huck MG, Taylor HM (1982) The rhizotron as a tool for root research. In: Brady NC (ed) Advances in agronomy. Academic Press, Cambridge, pp 1–35Google Scholar
  30. Huck M, Hoogenboom G, Peterson CM (1987) Soybean root senescence under drought stress. In: Taylor HM (ed) Minirhizotron observation tubes: Methods and applications for measuring rhizosphere dynamics. ASA Special Publication No. 50. ASA, CSSA, SSSA, Madison, pp 109–121Google Scholar
  31. Johnson MG (2001) Advancing fine root research with minirhizotrons. Environ Exp Bot 45:263–289CrossRefPubMedGoogle Scholar
  32. Joslin JD, Wolfe M (1998) Impacts of water input manipulations on fine root production and mortality in a mature hardwood Forest. Plant Soil 204:165–174CrossRefGoogle Scholar
  33. Joslin JD, Wolfe MH, Hanson PJ (2000) Effects of altered water regimes on forest root systems. New Phytol 147:117–129CrossRefGoogle Scholar
  34. Joslin JD, Wolfe MH, Hanson PJ (2001) Factors controlling the timing of root elongation intensity in a mature upland oak stand. Plant Soil 228:201–212CrossRefGoogle Scholar
  35. Jourdan C, Silva EV, Goncalves JLM, Ranger J, Moreira RM, Laclau JP (2008) Fine root production and turnover in Brazilian eucalyptus plantations under contrasting nitrogen fertilization regimes. For Ecol Manag 256:396–404CrossRefGoogle Scholar
  36. Kahle H (1993) Response of roots of trees to heavy metals. Environ Exp Bot 33:99–119CrossRefGoogle Scholar
  37. Kern CC, Friend AL, Johnson JM-F, Coleman MD (2004) Fine root dynamics in a developing Populus deltoides plantation. Tree Physiol 24:651–660CrossRefPubMedGoogle Scholar
  38. King J, Pregitzer K, Zak D (1999) Clonal variation in above- and below-ground growth responses of Populus tremuloides Michaux: influence of soil warming and nutrient availability. Plant Soil 217:119–130CrossRefGoogle Scholar
  39. Kuhns MR, Garrett HE, Teskey RO, Hinckley TM (1985) Root-growth of black walnut trees related to soil-temperature, soil-water potential, and leaf water potential. For Sci 31:617–629Google Scholar
  40. Lobet G, Pagès L, Draye X (2011) A novel image-analysis toolbox enabling quantitative analysis of root system architecture. Plant Physiol 157:29–39CrossRefPubMedPubMedCentralGoogle Scholar
  41. Majdi H (1996) Root sampling methods - applications and limitations of the minirhizotron technique. Plant Soil 185:255–258CrossRefGoogle Scholar
  42. Majdi H, Pregitzer K, Morén A-S, Nylund J-E, I. Ågren G. (2005) Measuring fine root turnover in Forest ecosystems. Plant Soil 276:1–8CrossRefGoogle Scholar
  43. Mao Z, Bonis M-L, Rey H, Saint-André L, Stokes A, Jourdan C (2013a) Which processes drive fine root elongation in a natural mountain forest ecosystem? Plant Ecolog Divers 6:231–243CrossRefGoogle Scholar
  44. Mao Z, Jourdan C, Bonis M-L, Pailler F, Rey H et al (2013b) Modelling root demography in heterogeneous mountain forests and applications for slope stability analysis. Plant Soil 363:357–382CrossRefGoogle Scholar
  45. Mapelli S, Lombardi L, Brambilla I, Iulini A, Bertani A. (1995–1996) III International Walnut Congress 4421995:129–36Google Scholar
  46. Mathieu L, Lobet G, Tocquin P, Périlleux C (2015) “Rhizoponics”: a novel hydroponic rhizotron for root system analyses on mature Arabidopsis thaliana plants. Plant Methods 11:1–8CrossRefGoogle Scholar
  47. M’bou AT, Jourdan C, Deleporte P, Nouvellon Y, Saint-André L, et al (2008) Root elongation in tropical Eucalyptus plantations: effect of soil water content. Ann For Sci 65:609–09Google Scholar
  48. McAdam SAM, Brodribb TJ, Ross JJ (2016) Shoot-derived abscisic acid promotes root growth. Plant Cell Environ 39:652–659CrossRefPubMedGoogle Scholar
  49. McCormack ML, Guo D (2014) Impacts of environmental factors on fine root lifespan. Front Plant Sci 5:205CrossRefPubMedPubMedCentralGoogle Scholar
  50. McCormack M, Adams TS, Smithwick EAH, Eissenstat DM (2012) Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195:823–831CrossRefGoogle Scholar
  51. 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
  52. McCormack ML, Gaines K, Pastore M, Eissensat DM (2015) Early season fine root and leaf phenology in six diverse temperate tree species. Plant Soil 389:121–129CrossRefGoogle Scholar
  53. Menzel A (2003) Plant Phenological anomalies in Germany and their relation to air temperature and NAO. Clim Chang 57:243–263CrossRefGoogle Scholar
  54. Metcalfe DB, Meir P, Aragão LEO, da Costa AC, Braga AP et al (2008) The effects of water availability on root growth and morphology in an Amazon rainforest. Plant Soil 311:189–199CrossRefGoogle Scholar
  55. Misra RK (1999) Root and shoot elongation of rhizotron-grown seedlings of Eucalyptus nitens and Eucalyptus globulus in relation to temperature. Plant Soil 206:37–46CrossRefGoogle Scholar
  56. 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
  57. Mohamed A, Monnier Y, Mao Z, Lobet G, Maeght J-L et al (2017) An evaluation of inexpensive methods for root image acquisition when using rhizotrons. Plant Methods 13:11CrossRefPubMedPubMedCentralGoogle Scholar
  58. Morin X, Roy J, Sonié L, Chuine I (2010) Changes in leaf phenology of three European oak species in response to experimental climate change. New Phytol 186:900–910CrossRefPubMedGoogle Scholar
  59. 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
  60. Najar A, Landhäusser SM, Whitehill JG, Bonello P, Erbilgin N (2014) Reserves accumulated in nonphotosynthetic organs during the previous growing season drive plant defenses and growth in aspen in the subsequent growing season. J Chem Ecol 40:21–30Google Scholar
  61. Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408Google Scholar
  62. Norby RJ, Jackson RB (2000) Root dynamics and global change: seeking an ecosystem perspective. New Phytol 147:3–12Google Scholar
  63. Olesinski J, Lavigne MB, Krasowski MJ (2011) Effects of soil moisture manipulations on fine root dynamics in a mature balsam fir (Abies balsamea L. Mill.) forest. Tree Physiol 31:339–48Google Scholar
  64. Pregitzer KS, King JS, Burton AJ, Brown SE (2000) Responses of tree fine roots to temperature. New Phytol 147:105–115CrossRefGoogle Scholar
  65. Psarras G, Merwin IA, Lakso AN, Ray JA (2000) Root growth phenology, root longevity, and Rhizosphere respiration of field grown Mutsu' apple trees on Malling rootstock. J Am Soc Hortic Sci 125:596–602Google Scholar
  66. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  67. Radville L, McCormack ML, Post E, Eissenstat DM (2016a) Root phenology in a changing climate. J Exp Bot 67(12):3617–3628CrossRefPubMedGoogle Scholar
  68. Radville L, Post E, Eissenstat DM (2016b) Root phenology in an Arctic shrub-graminoid community: the effects of long-term warming and herbivore exclusion. Clim Chang Res 3:1–9CrossRefGoogle Scholar
  69. Reich P, Teskey R, Johnson P, Hinckley T (1980) Periodic root and shoot growth in oak. For Sci 26:590–598Google Scholar
  70. Richardson AD, Bailey AS, Denny EG, Martin CW, O'Keefe J (2006) Phenology of a northern hardwood forest canopy. Glob Chang Biol 12:1174–1188CrossRefGoogle Scholar
  71. Sloan VL, Fletcher BJ, Phoenix GK (2016) Contrasting synchrony in root and leaf phenology across multiple sub-Arctic plant communities. J Ecol 104:239–248CrossRefGoogle Scholar
  72. Steinaker DF, Wilson SD (2008) Phenology of fine roots and leaves in forest and grassland. J Ecol 96:1222–1229CrossRefGoogle Scholar
  73. Steinaker DF, Wilson SD, Peltzer DA (2010) Asynchronicity in root and shoot phenology in grasses and woody plants. Glob Chang Biol 16:2241–2251CrossRefGoogle Scholar
  74. Strand AE, Pritchard SG, McCormack ML, Davis MA, Oren R (2008) Irreconcilable differences: fineroot life spans and soil carbon persistence. Science 319Google Scholar
  75. Tanner SC, Reighard GL, Wells CE (2006) Soil treatments differentially affect peach tree root development and demography in a replant site. In: Infante R (ed) Proceedings of the VIth international peach symposium, Acta, pp 381–387Google Scholar
  76. Tierney GL, Fahey TJ (2002) Fine root turnover in a northern hardwood forest: a direct comparison of the radiocarbon and minirhizotron methods. Can J For Res 32:1692–1697CrossRefGoogle Scholar
  77. Vogt K, Vogt D, Palmiotto P, Boon P, O'Hara J, Asbjornsen H (1995) Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species. Plant Soil 187:159–219CrossRefGoogle Scholar
  78. Vogt KA, Vogt DJ, Bloomfield J (1998) Analysis of some direct and indirect methods for estimating root biomass and production of forests at an ecosystem level. In: Box J Jr (ed) Root demographics and their efficiencies in sustainable agriculture, grasslands and forest ecosystems. Springer Netherlands, Berlin, pp 687–720CrossRefGoogle Scholar
  79. Wan CG, Yilmaz I, Sosebee RE (2002) Seasonal soil-water availability influences snakeweed, root dynamics. J Arid Environ 51:255–264CrossRefGoogle Scholar
  80. Wang Z, Ding L, Wang J, Zuo X, Yao S, Feng J (2016) Effects of root diameter, branch order, root depth, season and warming on root longevity in an alpine meadow. Ecol Res 31:739–747CrossRefGoogle Scholar
  81. Wells CE, Eissenstat DM (2001) Marked differences in survivorship among apple roots of different diameters. Ecology 82:882–892CrossRefGoogle Scholar
  82. West JB, Espeleta JF, Donovan LA (2004) Fine root production and turnover across a complex edaphic gradient of a Pinus palustris–Aristida stricta savanna ecosystem. For Ecol Manag 189:397–406CrossRefGoogle Scholar
  83. Wielgolaski F-E (1999) Starting dates and basic temperatures in phenological observations of plants. Int J Biometeorol 42:158–168CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.AMAP, INRA, CNRS, IRD, CIRADUniversity of MontpellierMontpellierFrance
  2. 2.Eco&Sols, CIRAD, INRA, IRD, Montpellier SupAgroUniversity of MontpellierMontpellierFrance
  3. 3.UMR System, INRAMontpellier cedex 2France

Personalised recommendations