Skip to main content

Pathogen-induced defoliation impacts on transpiration, leaf gas exchange, and non-structural carbohydrate allocation in eastern white pine (Pinus strobus)

Trees volume 35, pages 357–373 (2021)Cite this article

Abstract

Key message

Pathogen-induced defoliation resulted in a reduction in transpiration, an upregulation of photosynthesis in the early growing season, and no change in NSC reserves across stem, root, and foliar tissues.

Abstract

The defoliation of eastern white pine (Pinus strobus L.) by native fungi associated with white pine needle damage (WPND) can substantially reduce foliar area for much of the growing season in the northeastern United States. Chronic defoliations in the region are known to have slowed growth rates in symptomatic stands, but the physiological impacts of WPND as it relates to tree water use and carbon assimilation are largely unresolved. We investigated how the severity of WPND defoliation influences transpiration throughout the course of a growing season. We also assessed leaf-level gas exchange between defoliation severity classes and needle age over time. Finally, we compared concentrations of non-structural carbohydrates (NSC) between defoliation severity classes in five different tissue types over time. We found that trees experiencing a high-severity defoliation had 20% lower sap flux density compared to low-severity individuals. We found that rates of photosynthesis were significantly influenced by the needle age class and time of year, while instantaneous water use efficiency was higher across all needle age classes late in the growing season. Our findings suggest that the residual current-year foliage of high-severity defoliated trees compensated for the loss of mature second- and third-year foliage in the early portion of the growing season. This study found that soluble sugars and starch varied significantly over time and by tissue type, but defoliation severity had little effect on NSC concentrations. Together with reduced basal area increment in high-severity trees relative to low-severity trees, this indicates that WPND-affected trees are prioritizing NSC storage over secondary growth.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Alvarado-Barrientos MS, Hernández-Santana V, Asbjornsen H (2013) Variability of the radial profile of sap velocity in Pinus patula from contrasting stands within the seasonal cloud forest zone of Veracruz, Mexico. Agric For Meteorol 168:108–119

    Google Scholar 

  • Ambrose AR, Sillett SC, Koch GW, Van Pelt R, Antoine ME, Dawson TE (2010) Effects of height on treetop transpiration and stomatal conductance in coast redwood (Sequoia sempervirens). Tree Physiol 30(10):1260–1272

    PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Scheipl F, Grothendieck G, Green P (2018) Package ‘lme4’, version, 1, 17

  • Broders K, Munck I, Wyka S, Iriarte G, Beaudoin E (2015) Characterization of fungal pathogens associated with White Pine Needle Damage (WPND) in Northeastern North America. Forests 6(11):4088–4104

    Google Scholar 

  • Burgess SS, Adams MA, Turner NC, Beverly CR, Ong CK, Khan AA, Bleby TM (2001) An improved heat pulse method to measure low and reverse rates of sap flow in woody plants. Tree Physiol 21(9):589–598

    CAS  PubMed  Google Scholar 

  • Costanza KKL, Whitney TD, Mcintire CD, Livingston WH, Gandhi KJK (2018) Forest ecology and management. A synthesis of emerging health issues of eastern white pine (Pinus strobus) in eastern North America. For Ecol Manag 423:3–17

    Google Scholar 

  • Cuny HE, Rathgeber CBK, Lebourgeois F, Fortin M, Fournier M (2012) Life strategies in intra-annual dynamics of wood formation: example of three conifer species in a temperate forest in north-east France. Tree Physiol 32(5):612–625

    PubMed  Google Scholar 

  • Damascos MA, Ronquim CC, Henrique C, Assis B (2005) Gas exchange and plant growth after defoliation on Leandra lacunosa, a Cerrado Woody species with continuous leaf production. Braz Arch Biol Technol 48:967–974

    Google Scholar 

  • Davis TW, Kuo C-M, Liang X, Yu P-S (2012) Sap flow sensors: construction, quality control and comparison. Sensors 12(12):954–971

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Dickman LT, Mcdowell NG, Sevanto S, Pangle RE, Pockman WT (2015) Carbohydrate dynamics and mortality in a piñon-juniper woodland under three future precipitation scenarios. Plant Cell Environ 38:729–739

    CAS  PubMed  Google Scholar 

  • Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65(1):667–687

    CAS  PubMed  Google Scholar 

  • Eyles A, Smith D, Pinkard EA, Smith I, Corkrey R, Elms S, Beadle C, Mohammed C (2011) Photosynthetic responses of field-grown Pinus radiata trees to artificial and aphid-induced defoliation. Tree Physiol 31:592–603

    CAS  PubMed  Google Scholar 

  • Furze ME, Huggett BA, Aubrecht DM, Stolz CD, Carbone MS, Richardson AD (2019) Whole-tree nonstructural carbohydrate storage and seasonal dynamics in five temperate species. New Phytol 221:1466–1477

    CAS  PubMed  Google Scholar 

  • Gebauer T, Horna V, Leuschner C (2008) Variability in radial sap flux density patterns and sapwood area among seven co-occurring temperate broad-leaved tree species. Tree Physiol 28(12):1821–1830

    PubMed  Google Scholar 

  • Gómez-Gallego M, Williams N, Leuzinger S, Scott PM, Bader MK (2020) No carbon limitation after lower crown loss in Pinus radiata. Ann Bot 125:955–967

    PubMed  PubMed Central  Google Scholar 

  • Gotsch SG, Asbjornsen H, Holwerda F, Goldsmith GR, Weintraub AE, Dawson TE (2014) Foggy days and dry nights determine crown-level water balance in a seasonal tropical montane cloud forest. Plant Cell Environ 37(1):261–272

    PubMed  Google Scholar 

  • Handa I, Korner C, Hattenschwiler S (2005) A test of the treeline carbon limitation hypothesis by in situ CO2 enrichment and defoliation. Ecology 86(5):1288–1300

    Google Scholar 

  • Hart M, Hogg EH, Lieffers VJ (2000) Enhanced water relations of residual foliage following defoliation in Populus tremuloides. Can J Bot 78(5):583–590

    Google Scholar 

  • Hirose T (2012) Leaf-level nitrogen use efficiency: definition and importance. Oecologia 169:591–597

    PubMed  Google Scholar 

  • Hudgeons JL, Knutson AE, Heinz KM, Deloach CJ, Dudley TL, Pattison RR, Kiniry JR (2007) Defoliation by introduced Diorhabda elongata leaf beetles (Coleoptera: Chrysomelidae) reduces carbohydrate reserves and regrowth of Tamarix (Tamaricaceae). Biol Control 43:213–221

    Google Scholar 

  • Hultine KR (2010) Sap-flux scaled transpiration by tamarisk (Tamarix spp.) before, during and after episodic defoliation by the Saltcedar Leaf Beetle (Diorhabda carinulata). Agric For Meteorol 150:1467–1475

    Google Scholar 

  • Jacquet J, Bosc A, O’Grady AP, Jactel H (2013) Pine growth response to processionary moth defoliation across a 40-year chronosequence. For Ecol Manag 293:29–38

    Google Scholar 

  • Jacquet J, Bosc A, Grady AO, Jactel H (2014) Combined effects of defoliation and water stress on pine growth and non-structural carbohydrates. Tree Physiol 34:1–10

    Google Scholar 

  • Jenkins JC, Chojnacky DC, Heath LS, Birdsey RA (2003) Comprehensive database of diameter-based biomass regressions for North American tree species. In: USDA Forest Service, General Technical Report NE-319, pp 1–48

  • Johnson JOND (1984) A rapid technique for estimating total surface area of pine needles. For Sci 30(4):913–921

    Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82(13):1–26

    Google Scholar 

  • Landhausser SM, Lieffers VJ (2012) Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees 26:653–661

    Google Scholar 

  • Lenth R, Singmann H, Love J, Buerkner P, Herve M (2018) Emmeans: estimated marginal means, aka least-squares means. R package version 1(1):3

  • Li M, Hoch G, Körner C (2002) Source/sink removal affects mobile carbohydrates in Pinus cembra at the Swiss treeline. Trees 16(4–5):331–337

    CAS  Google Scholar 

  • Li M, Kong G, Zhu J (2009) Vertical and leaf-age-related variations of nonstructural carbohydrates in two alpine timberline species, southeastern Tibetan Plateau. J For Res 14(4):229–235

    CAS  Google Scholar 

  • Looker N, Martin J, Jencso K, Hu J (2016) Contribution of sapwood traits to uncertainty in conifer sap flow as estimated with the heat-ratio method. Agric For Meteorol 223:60–71

    Google Scholar 

  • Marshall DC (1958) Measurement of sap flow in conifers by heat transport. Plant Physiol 33(6):385–396

    CAS  PubMed  PubMed Central  Google Scholar 

  • McDowell NG (2011) Mechanisms linking dought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155(3):1051–1059

    CAS  PubMed  PubMed Central  Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178(4):719–739

    PubMed  Google Scholar 

  • McIntire CD, Munck IA, Ducey MJ, Asbjornsen H (2018) Thinning treatments reduce severity of foliar pathogens in eastern white pine. For Ecol Manag 423:106–113

    Google Scholar 

  • McIntire C, Munck I, Vadeboncoeur MA, Livingston W, Asbjornsen H (2018) Impacts of White Pine Needle Damage on seasonal litterfall dynamics and wood growth of eastern white pine (Pinus strobus) in New England. For Ecol Manag 423:27–36

    Google Scholar 

  • Meinzer FC, Grantz DA (1991) Coordination of stomatal, hydraulic, and canopy boundary layer properties: do stomata balance conductances by measuring transpiration? Physiol Plant 83(2):324–329

    Google Scholar 

  • Meinzer FC, Woodruff DR, Shaw DC (2004) Integrated responses of hydraulic architecture, water and carbon relations of western hemlock to dwarf mistletoe infection. Plant Cell Environ 27:937–946

    Google Scholar 

  • Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30(9):1083–1095

    CAS  PubMed  Google Scholar 

  • Munck IA, Ostrofsky WD, Burns B (2012) Eastern White Pine Needle Damage. In: USDA Forest Service Northeastern Area State and Private Forestry (NA-PR-01-11), pp 1–4

  • Neris J, Tejedor M, Rodríguez M, Fuentes J, Jimenez C (2013) Effect of forestfloor characteristics on water repellency, infiltration, runoff and soilloss in Andisols of Tenerife (Canary Islands, Spain). Cantena 108:50–57

    Google Scholar 

  • Oishi AC, Hawthorne DA, Oren R (2016) ScienceDirect Baseliner: an open-source, interactive tool for processing sap flux data from thermal dissipation probes. SoftwareX 5:139–143

    Google Scholar 

  • Palacio S, Hester AJ, Maestro M, Millard P (2008) Browsed Betula pubescens trees are not carbon-limited. Funct Ecol 22(5):808–815

    Google Scholar 

  • Palacio S, Hernández R, Maestro-Martínez M, Camarero J (2012) Fast replenishment of initial carbon stores after defoliation by the pine processionary moth and its relationship to the re-growth ability of trees. Trees Struct Funct 26(5):1627–1640

    Google Scholar 

  • Pataki DE, Oren R, Phillips N (1998) Responses of sap flux and stomatal conductance of Pinus taeda L. trees to stepwise reductions in leaf area. J Exp Bot 49(322):871–878

    CAS  Google Scholar 

  • Piper FI, Gundale MJ, Fajardo A (2015) Extreme defoliation reduces tree growth but not C and N storage in a winter-deciduous species. Ann Bot 115(7):1093–1103

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puri E, Hoch G, Körner C (2015a) Defoliation reduces growth but not carbon reserves in Mediterranean Pinus pinaster trees. Trees 29(4):1187–1196

    Google Scholar 

  • Puri E, Hoch G, Körner C (2015b) Defoliation reduces growth but not carbon reserves in Mediterranean Pinus pinaster trees. Trees 29(4):1187–1196

    Google Scholar 

  • 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(3):356–364

    Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Reich PB, Walters MB, Krause SC, Vanderklein DW, Raffs KF, Tabone T (1993) Growth, nutrition and gas exchange of Pinus resinosa following artificial defoliation. Trees 7(2):67–77

    Google Scholar 

  • Richardson AD, Carbone MS, Huggett BA, Furze ME, Czimczik CI, Walker JC, Xu X, Schaberg PG, Murakami P (2015) Distribution and mixing of old and new nonstructural carbon in two temperate trees. New Phytol 206(2):590–597

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ritz C, Baty F, Streibig JC, Gerhard D (2015) Dose-response analysis using R. PLoS ONE 10(12):1–13

    Google Scholar 

  • Rossi S, Rathgeber CB, Deslauriers A (2009) Comparing needle and shoot phenology with xylem development on three conifer species in Italy. Ann For Sci 66(2):206–213

    Google Scholar 

  • Saffell BJ, Meinzer FC, Voelker SL, Shaw DC, Brooks JR, Lachenbruch B, Mckay J (2014a) Tree-ring stable isotopes record the impact of a foliar fungal pathogen on CO2 assimilation and growth in Douglas-fir. Plant Cell Environ 37:1536–1547

    CAS  PubMed  Google Scholar 

  • Saffell BJ, Meinzer FC, Woodruff DR, Shaw DC, Voelker SL, Lachenbruch B, Falk K (2014b) Seasonal carbohydrate dynamics and growth in Douglas-fir trees experiencing chronic, fungal-mediated reduction in functional leaf area. Tree Physiol 34(3):218–228

    CAS  PubMed  Google Scholar 

  • Sampson DA, Albaugh TJ, Johnsen KH, Allen HL, Zarnoch SJ (2003) Monthly leaf area index estimates from point-in-time measurements and needle phenology for Pinus taeda. Can J For Res 33(12):2477–2490

    Google Scholar 

  • Simonin KA, Burns E, Choat B, Barbour MM, Dawson TE, Franks PJ (2015) Increasing leaf hydraulic conductance with transpiration rate minimizes the water potential drawdown from stem to leaf. J Exp Bot 66(5):1303–1315

    CAS  PubMed  Google Scholar 

  • Steppe K, De Pauw DJW, Doody TM, Teskey RO (2010) A comparison of sap flux density using thermal dissipation, heat pulse velocity and heat field deformation methods. Agric For Meteorol 150(7–8):1046–1056

    Google Scholar 

  • Thomas AH, Sadras VO (2001) The capture and gratuitous disposal of resources by plants. Br Ecol Soc 15(1):3–12

    Google Scholar 

  • Vandegehuchte MW, Steppe K (2012) Improving sap flux density measurements by correctly determining thermal diffusivity, differentiating between bound and unbound water. Tree Physiol 32(7):930–942

    PubMed  Google Scholar 

  • Venturas MD, Mackinnon ED, Jacobsen AL, Pratt RB (2015) Excising stem samples underwater at native tension does not induce xylem cavitation. Plant Cell Environ 38(6):1060–1068

    CAS  PubMed  Google Scholar 

  • Wargo PM, Minocha R, Wong BL, Long RP, Horsley SB, Hall TJ (2002) Measuring changes in stress and vitality indicators in limed sugar maple on the Allegheny Plateau in north-central Pennsylvania. Can J For Res 641:629–641

    Google Scholar 

  • Wiley E, Helliker B (2012) A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol 195(2):285–289

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wiley E, Casper BB, Helliker BR (2016) Recovery following defoliation involves shifts in allocation that favour storage and reproduction over radial growth in black oak. J Ecol 105:412

    Google Scholar 

  • Williams JP, Hanavan RP, Rock BN, Minocha SC, Linder E (2016) Influence of Hemlock Woolly Adelgid infestation on the physiological and reflectance characteristics of Eastern Hemlock. Can J For Res 426:410–426

    Google Scholar 

  • Wullschleger SD, King AW (2000) Radial variation in sap velocity as a function of stem diameter and sapwood thickness in yellow-poplar trees. Tree Physiol 20(8):511–518

    PubMed  Google Scholar 

  • Wyka SA, Smith C, Munck IA, Rock BN, Ziniti BL, Broders K (2017) Emergence of White Pine Needle Damage (WPND) in the northeastern US is associated with changes in pathogen pressure in response to climate change. Glob Change Biol 23(1):392–405

    Google Scholar 

  • Wyka SA, Mcintire CD, Smith C, Munck IA, Rock BN, Asbjornsen H, Broders KD (2018a) Effect of climatic variables on abundance and dispersal of Lecanosticta acicola spores and impact of defoliation on eastern white pine. Phytopathology 108(3):374–383

    CAS  PubMed  Google Scholar 

  • Wyka SA, Munck IA, Brazee NJ, Broders KD (2018b) Response of eastern white pine and associated foliar, blister rust, canker and root rot pathogens to climate change. For Ecol Manag 238:18–26

    Google Scholar 

  • Yan C, Han S, Zhou Y, Wang C, Dai G, Xiao W, Li M-H (2012) Needle-age related variability in nitrogen, mobile carbohydrates, and d13C within Pinus koraiensis tree crowns. PLoS ONE 7(4):16–19

    Google Scholar 

Download references

Acknowledgements

This research was funded by USDA Forest Health Protection NA Grant 15DG-11420004-150 and the New Hampshire Agricultural Experiment Station. We are grateful for the cooperation of the USFS Northern Research Station, the Massabesic Experimental Forest, the Caroline A. Fox Research and Demonstration Forest, and the UNH Office of Woodlands and Natural Areas. The authors are also thankful for the field assistance from Steve Eisenhaure, Stephen Wyka, Connor Brenton, Sydney Snelling, and Katerine Sinacore.

Author information

Author notes

  1. Cameron D. McIntire

    Present address: USDA Forest Service, State and Private Forestry, 271 Mast Rd., Durham, NH, USA

Authors and Affiliations

  1. USDA Forest Service, State and Private Forestry, 271 Mast Rd., Durham, NH, USA

    Isabel A. Munck

  2. Department of Natural Resources and the Environment, University of New Hampshire, 56 College Rd., Durham, NH, USA

    Cameron D. McIntire & Heidi Asbjornsen

  3. Department of Biology, Bates College, 2 Andrews Rd., Lewiston, ME, USA

    Brett A. Huggett & Emma Dunn

  4. Earth Systems Research Center, University of New Hampshire, 8 College Rd., Durham, NH, USA

    Matthew A. Vadeboncoeur & Heidi Asbjornsen

Authors
  1. Cameron D. McIntire
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brett A. Huggett
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emma Dunn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Isabel A. Munck
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Matthew A. Vadeboncoeur
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heidi Asbjornsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cameron D. McIntire.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Ethical statement

This manuscript is not currently being considered for publication in another journal.

Additional information

Communicated by Jared LeBoldus.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 429 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

McIntire, C.D., Huggett, B.A., Dunn, E. et al. Pathogen-induced defoliation impacts on transpiration, leaf gas exchange, and non-structural carbohydrate allocation in eastern white pine (Pinus strobus). Trees 35, 357–373 (2021). https://doi.org/10.1007/s00468-020-02037-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-020-02037-z

Keywords

  • White pine needle damage
  • Defoliation
  • Forest pathogen
  • Sap flux
  • Leaf gas exchange
  • Non-structural carbohydrates