Interactive effects of defoliation and water deficit on growth, water status, and mortality of black spruce (Picea mariana (Mill.) B.S.P.)

  • Hibat Allah Bouzidi
  • Lorena Balducci
  • John Mackay
  • Annie DeslauriersEmail author
Research Paper
Part of the following topical collections:
  1. Wood formation and tree adaptation to climate


Key message

Defoliation followed by water deficit showed time-dependent effects on plant water status and growth in black spruce ( Picea mariana (Mill.) B.S.P.). Biotic stress negatively (during active defoliation by growing instars) and positively (after defoliation) affected plant water relations. However, water deficit, alone or combined with defoliation, prevails over defoliation-related stress for radial growth and sapling vitality.


Tree vitality is influenced by multiple factors such as insect damage, water deficit, and the timing of these stresses. Under drought, positive feedback via the reduction of leaf area may improve the water status of defoliated trees. However, the effect on tree mortality remains largely unknown.


We investigated the effects of defoliation followed by a water deficit on tree growth, plant water status, and mortality in black spruce (Picea mariana (Mill.) B.S.P.) saplings.


In a controlled greenhouse setting, saplings were submitted to combined treatments of defoliation and water stress. To assess the impact of these stresses and their interaction, we measured phenology, twig development, secondary growth of the stem, water potential, and mortality of the saplings.


Both defoliation and water deficits reduced growth; however, the effect was not additive. During active defoliation, we observed a higher evaporative demand and a lower midday leaf water potential Ψmd. We observed an opposite pattern of response post-stress. Drought alone increased sapling mortality immediately after the stress period, but after c.a. 20 days, mortality rates remained similar following combined drought and defoliation.


Our results highlight two key periods during which defoliation affects plant water relations either negatively (during active defoliation) or positively (after defoliation). Mortality in defoliated saplings was reduced immediately following drought because available internal water increased in the stem.


Black spruce saplings Spruce budworm Defoliation Irrigation regimes Bud phenology Primary growth Physiological parameters 



We thank S. Rivest for his help in collecting the data.


This study was funded by the “Programme de soutien à la recherche, volet Soutien à des initiatives internationales de recherche et d’innovation (PSR-SIIRI),” the Ministère du Développement économique, Innovation et Exportation du Québec (MDEIE), and the Natural Sciences and Engineering Research Council of Canada (Discovery Grant of A. Deslauriers).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EHT, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. CrossRefGoogle Scholar
  2. Balducci L, Deslauriers A, Giovannelli A, Rossi S, Rathgeber CBK (2013) Effects of temperature and water deficit on cambial activity and woody ring features in Picea mariana saplings. Tree Physiol 33:1006–1017. CrossRefPubMedGoogle Scholar
  3. Balducci L, Deslauriers A, Giovannelli A, Beaulieu M, Delzon S, Rossi S, Rathgeber CBK (2015) How do drought and warming influence survival and wood traits of Picea mariana saplings? J Exp Bot 66:377–389. CrossRefPubMedGoogle Scholar
  4. Bansal S, Hallsby G, Löfvenius MO, Nilsson M-C (2013) Synergistic, additive and antagonistic impacts of drought and herbivory on Pinus sylvestris: leaf, tissue and whole-plant responses and recovery. Tree Physiol 33:451–463. CrossRefPubMedGoogle Scholar
  5. Bergeron Y, Leduc A, Joyal C, Morin H (1995) Balsam fir mortality following the last spruce budworm outbreak in northwestern Quebec. Can J For Res 25:1375–1384. CrossRefGoogle Scholar
  6. Bernier PY (1993) Comparing natural and planted black spruce seedlings. I. Water relations and growth. Can J For Res 23:2427–2434. CrossRefGoogle Scholar
  7. Bond BJ, Kavanagh KL (1999) Stomatal behavior of four woody species in relation to leaf-specific hydraulic conductance and threshold water potential. Tree Physiol 19:503–510. CrossRefPubMedGoogle Scholar
  8. Bouchard M, Kneeshaw D, Bergeron Y (2005) Mortality and stand renewal patterns following the last spruce budworm outbreak in mixed forests of western Quebec. For Ecol Manag 204:297–313. CrossRefGoogle Scholar
  9. 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 long-term consequences. Ann For Sci 63:625–644. CrossRefGoogle Scholar
  10. Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149:575–584. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chen L, Huang J-G, Alam SA, Zhai L, Dawson A, Stadt KJ, Comeau PG (2017a) Drought causes reduced growth of trembling aspen in western Canada. Glob Chang Biol 23:2887–2902. CrossRefPubMedGoogle Scholar
  12. Chen L, Huang JG, Dawson A, Zhai L, Stadt KJ, Comeau PG, Whitehouse C (2017b) Contributions of insects and droughts to growth decline of trembling aspen mixed boreal forest of western Canada. Glob Chang Biol 24:655–667. CrossRefPubMedGoogle Scholar
  13. Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018) Triggers of tree mortality under drought. Nature 558:531–539. CrossRefPubMedGoogle Scholar
  14. Cochard H, Coll L, Le Roux X, Améglio T (2002) Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiol 128:282–290. CrossRefPubMedPubMedCentralGoogle Scholar
  15. De Grandpré L, Kneeshaw DD, Perigon S, Boucher D, Marchand M, Pureswaran D, Girardin MP (2019) Adverse climatic periods precede and amplify defoliator-induced tree mortality in eastern boreal North America. J Ecol 107:452–467. CrossRefGoogle Scholar
  16. Delzon S, Cochard H (2014) Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin. New Phytol 203:355–358. CrossRefPubMedGoogle Scholar
  17. Deslauriers A, Morin H, Bégin Y (2003) Cellular phenology of annual ring formation of Abies balsamea in Quebec boreal forest (Canada). Can J For Res 33:190–200. CrossRefGoogle Scholar
  18. Deslauriers A, Rossi S, Anfodillo T (2007) Dendrometer and intra-annual tree growth: what kind of information can be inferred? Dendrochronologia 25:113–124. CrossRefGoogle Scholar
  19. Deslauriers A, Caron L, Rossi S (2015) Carbon allocation during defoliation: testing a defense-growth trade-off in balsam fir. Front Plant Sci 6:1–13. CrossRefGoogle Scholar
  20. Deslauriers A, Huang J, Balducci L, Beaulieu M, Rossi S (2016) The contribution of carbon and water in modulating wood formation in black spruce saplings. Plant Physiol 170:2072–2084. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Deslauriers A, Fournier M-P, Cartenì F, Mackay J (2019) Spruce budworm defoliation leads to altered carbon allocation and earlier budburst in conifers. Tree Physiol, tpy135.
  22. Dhont C, Sylvestre P, Gros-Louis M-C, Isabel N (2010) Field guide for identifying apical bud break and bud formation stages in white spruce. Natural Resources Canada, QuébecGoogle Scholar
  23. Eyles A, Pinkard EA, Mohammed C (2009) Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Physiol 29:753–764. CrossRefPubMedGoogle Scholar
  24. Eyles A, Pinkard EA, Davies NW, Corkrey R, Churchill K, O’Grady AP, Sands P, Mohammed C (2013) Whole-plant versus leaf-level regulation of photosynthetic responses after partial defoliation in saplings. J Exp Bot 64:1625–1636. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fernández-de-Uña L, Rossi S, Aranda I, Fonti P, González-González BD, Cañellas I, Gea-Izquierdo G (2017) Xylem and leaf functional adjustments to drought in Pinus sylvestris and Quercus pyrenaica at their elevational boundary. Front Plant Sci 8:1–12. CrossRefGoogle Scholar
  26. Forner A, Valladares F, Bonal D, Granier A, Grossiord C, Aranda I (2018) Extreme droughts affecting Mediterranean tree species’ growth and water-use efficiency: the importance of timing. Tree Physiol 38:1127–1137. CrossRefPubMedGoogle Scholar
  27. Giovannelli A, Deslauriers A, Fragnelli G, Scaletti L, Castro G, Rossi S, Crivellaro A (2007) Evaluation of drought response of two poplar clones (Populus×canadensis Mönch ‘I-214’ and P. deltoides Marsh. ‘Dvina’) through high resolution analysis of stem growth. J Exp Bot 58:2673–2683. CrossRefPubMedGoogle Scholar
  28. Goldstein G, Andrade JL, Meinzer FC, Holbrook NM, Cavelier J, Jackson P, Celis A (1998) Stem water storage and diurnal patterns of water use in tropical forest canopy trees. Plant Cell Environ 21:397–406. CrossRefGoogle Scholar
  29. Grossnickle SC, Blake TJ (1987) Water relation patterns of bare-root and container jack pine and black spruce seedlings planted on boreal cut-over sites. New For 1:101–116. CrossRefGoogle Scholar
  30. Gruber A, Strobl S, Veit B, Oberhuber W (2010) Impact of drought on the temporal dynamics of wood formation in Pinus sylvestris. Tree Physiol 30:490–501. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hennigar CR, MacLean DA, Quiring DT, Kershaw JA (2008) Differences in spruce budworm defoliation among balsam fir and white, red, and black spruce. For Sci 54:158–166. CrossRefGoogle Scholar
  32. Jacquet J-S, Bosc A, O’Grady A, Jactel H (2014) Combined effects of defoliation and water stress on pine growth and non-structural carbohydrates. Tree Physiol 34:367–376. CrossRefPubMedGoogle Scholar
  33. Maclean DA, Lidstone RG (1982) Defoliation by spruce budworm: estimation by ocular and shoot-count methods and variability among branches, trees, and stands. Can J For Res 12:582–594. CrossRefGoogle Scholar
  34. Mencuccini M (2003) The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ 26:163–182. CrossRefGoogle Scholar
  35. Mitchell PJ, Battaglia M, Pinkard EA (2013) Counting the costs of multiple stressors: is the whole greater than the sum of the parts? Tree Physiol 33:447–450. CrossRefPubMedGoogle Scholar
  36. Morin H, Laprise D, Bergeron Y (1993) Chronology of spruce budwom outbreaks near Lake Duparquet, Abitibi region, Québec. Can J For Res 23:1497–1506. CrossRefGoogle Scholar
  37. Muller B, Pantin F, Genard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729. CrossRefGoogle Scholar
  38. Niinemets Ü (2010) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. For Ecol Manag 260:1623–1639. CrossRefGoogle Scholar
  39. Oberhuber W, Swidrak I, Pirkebner D, Gruber A (2011) Temporal dynamics of nonstructural carbohydrates and xylem growth in Pinus sylvestris exposed to drought. Can J For Res 41:1590–1597. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Páez A, González OME, Yrausquín X, Salazar A, Casanova A (1995) Water stress and clipping management effects on Guineagrass: I. Growth and biomass allocation. Agron J 87:698–706. CrossRefGoogle Scholar
  41. Park Williams A, Allen CD, Macalady AK, Griffin D, Woodhouse CA, Meko DM, Swetnam TW, Rauscher SA, Seager R, Grissino-Mayer HD, Dean JS, Cook ER, Gangodagamage C, Cai M, McDowell N (2013) Temperature as a potent driver of regional forest drought stress and tree mortality. Nat Clim Chang 3:292–297. CrossRefGoogle Scholar
  42. Peng C, Ma Z, Lei X, Zhu Q, Chen H, Wang W, Liu S, Li W, Fang X, Zhou X (2011) A drought-induced pervasive increase in tree mortality across Canada’s boreal forests. Nat Clim Chang 1:467–471. CrossRefGoogle Scholar
  43. Piene H, Maclean DA, Wall RE (1981) Effects of spruce budworm-caused defoliation on the growth of balsam fir: experimental design and methodology. Environment Canada, Canadian Forestry Service, Maritimes Forest Research Centre, FrederictonGoogle Scholar
  44. Pureswaran DS, De Grandpré L, Paré D, Taylor A, Barrette M, Morin H, Régnière J, Kneeshaw DD (2015) Climate-induced changes in host tree-insect phenology may drive ecological state-shift in boreal forests. Ecology 96:1480–1491. CrossRefGoogle Scholar
  45. Quentin AG, O’Grady AP, Beadle CL, Worledge D, Pinkard EA (2011) Responses of transpiration and canopy conductance to partial defoliation of Eucalyptus globulus trees. Agric For Meteorol 151:356–364. CrossRefGoogle Scholar
  46. Quentin AG, O’Grady AP, Beadle CL, Mohammed C, Pinkard EA (2012) Interactive effects of water supply and defoliation on photosynthesis, plant water status and growth of Eucalyptus globulus Labill. Tree Physiol 32:958–967. CrossRefPubMedGoogle Scholar
  47. Roe AD, Demidovich M, Dedes J (2018) Origins and history of laboratory insect stocks in a multispecies insect production facility, with the proposal of standardized nomenclature and designation of formal standard names. J Insect Sci 18:1–9. CrossRefPubMedCentralGoogle Scholar
  48. Rossi S, Isabel N (2017) Bud break responds more strongly to daytime than night-time temperature under asymmetric experimental warming. Glob Chang Biol 23:446–454. CrossRefPubMedGoogle Scholar
  49. Rossi S, Morin H (2011) Demography and spatial dynamics in balsam fir stands after a spruce budworm outbreak. Can J For Res 41:1112–1120. CrossRefGoogle Scholar
  50. Rossi S, Deslauriers A, Morin H (2003) Application of the Gompertz equation for the study of xylem cell development. Dendrochronologia 21:33–39. CrossRefGoogle Scholar
  51. Rossi S, Simard S, Rathgeber CBK, Deslauriers A, De Zan C (2009) Effects of a 20-day-long dry period on cambial and apical meristem growth in Abies balsamea seedlings. Trees 23:85–93. CrossRefGoogle Scholar
  52. Salleo S, Nardini A, Raimondo F, Lo Gullo MA, Pace F, Giacomich P (2003) Effects of defoliation caused by the leaf miner Cameraria ohridella on wood production and efficiency in Aesculus hippocastanum growing in north-eastern Italy. Trees 17:367–375. CrossRefGoogle Scholar
  53. Salmon Y, Torres-Ruiz JM, Poyatos R, Martinez-Vilalta J, Meir P, Cochard H, Mencuccini M (2015) Balancing the risks of hydraulic failure and carbon starvation: a twig scale analysis in declining Scots pine. Plant Cell Environ 38:2575–2588. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Salomón RL, Limousin J-M, Ourcival J-M, Rodríguez-Calcerrada J, Steppe K (2017) Stem hydraulic capacitance decreases with drought stress: implications for modelling tree hydraulics in the Mediterranean oak Quercus ilex. Plant Cell Environ 40:1379–1391. CrossRefPubMedGoogle Scholar
  55. Scherrer B (2007) Biostatistique, 2e edn. Gaetan Morin, MontréalGoogle Scholar
  56. Schmid S, Palacio S, Hoch G (2017) Growth reduction after defoliation is independent of CO2 supply in deciduous and evergreen young oaks. New Phytol 214:1479–1490. CrossRefPubMedGoogle Scholar
  57. Simard S, Morin H, Krause C, Buhay WM, Treydte K (2012) Tree-ring widths and isotopes of artificially defoliated balsam firs: a simulation of spruce budworm outbreaks in Eastern Canada. Environ Exp Bol 81:44–54. CrossRefGoogle Scholar
  58. Steppe K, Sterck F, Deslauriers A (2015) Diel growth dynamics in tree stems: linking anatomy and ecophysiology. Trends Plant Sci 20:335–343. CrossRefPubMedGoogle Scholar
  59. Stewart JD, Bernier PY (1995) Gas exchange and water relations of 3 sizes of containerized Picea mariana seedlings subjected to atmospheric and edaphic water stress under controlled conditions. Ann For Sci 52:1–9. CrossRefGoogle Scholar
  60. Stewart JD, Zine El Abidine A, Bernier PY (1995) Stomatal and mesophyll limitations of photosynthesis in black spruce seedlings during multiple cycles of drought. Tree Physiol 15:57–64. CrossRefGoogle Scholar
  61. Tan W, Blake TJ (1997) Gas exchange and water relations responses to drought of fast- and slow-growing black spruce families. Can J Bot 75:1700–1706. CrossRefGoogle Scholar
  62. Tardieu F, Granier C, Muller B (2011) Water deficit and growth. Co-ordinating processes without an orchestrator? Curr Opin Plant Biol 14:283–289. CrossRefPubMedGoogle Scholar
  63. Tardieu F, Parent B, Caldeira CF, Welcker C (2014) Genetic and physiological controls of growth under water deficit. Plant Physiol 164:1628–1635. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Topp GC, Zebchuk WD, Davis JL, Bailey WG (1984) The measurement of soil water content using a portable TDR hand probe. Can J Soil Sci 64:313–321. CrossRefGoogle Scholar
  65. Tyree MT (2003) Hydraulic limits on tree performance: transpiration, carbon gain and growth of trees. Trees 17:95–100. CrossRefGoogle Scholar
  66. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, BerlinCrossRefGoogle Scholar
  67. Vanderklein DW, Reich PB (2000) European larch and eastern white pine respond similarly during three years of partial defoliation. Tree Physiol 20:283–287. CrossRefPubMedGoogle Scholar
  68. Wiley E, Huepenbecker S, Casper BB, Helliker BR (2013) The effects of defoliation on carbon allocation: can carbon limitation reduce growth in favour of storage? Tree Physiol 33:1216–1228. CrossRefPubMedGoogle Scholar
  69. Zhai L, Bergeron Y, Huang JG, Berninger F (2012) Variation in intra-annual wood formation, and foliage and shoot development of three major Canadian boreal tree species. Am J Bot 99:827–837. CrossRefPubMedGoogle Scholar
  70. Zhang X, Lei Y, Ma Z, Kneeshaw D, Peng CH (2014) Insect-induced tree mortality of boreal forest in eastern Canada under a changing climate. Ecol Evol 4:2384–2394. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Zine El Abidine A, Bernier PY, Stewart JD, Plamondon AP (1994) Water stress preconditioning of black spruce seedlings from lowland and upland sites. Can J Bot 72:1511–1518. CrossRefGoogle Scholar
  72. Zweifel R, Zimmermann L, Zeugin F, Newbery D (2006) Intra-annual radial growth and water relations of trees: implications towards a growth mechanism. J Exp Bot 57:1445–1459. CrossRefPubMedGoogle Scholar

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© INRA and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Département des Sciences FondamentalesUniversité du Québec à ChicoutimiChicoutimiCanada
  2. 2.Centre d’Étude de la Foret, Département des Sciences du Bois et de la ForetUniversité LavalQuébecCanada
  3. 3.Institut de Biologie Intégrative et des SystèmesUniversité LavalQuébecCanada
  4. 4.Department of Plant SciencesUniversity of OxfordOxfordUK

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