Stem girdling does not allow mimicking changes in Norway spruce tree physiology during Eurasian spruce bark beetle infestation

Anna Candotti , Henrik Hartmann , Enrico Tomelleri

Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) : 109

PDF
Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) :109 DOI: 10.1007/s11676-026-02058-3
Original Paper
research-article
Stem girdling does not allow mimicking changes in Norway spruce tree physiology during Eurasian spruce bark beetle infestation
Author information +
History +
PDF

Abstract

Bark beetle infestations can cause rapid mortality in Norway spruce, yet the sequence of physiological changes leading to death is not fully understood. The aim of this research was to disentangle the earliest tree physiological signs of spruce bark beetle (Ips typographus L.) induced stress in Norway spruce (Picea abies L. Karst). Phloem girdling was used to attract bark beetles in an alpine forest and monitor tree physiological changes from the very beginning of the infestation, when symptoms are not yet visible in the crowns. Girdled–infested trees were compared with girdled–only and healthy control trees. Sap flux density, tree stem growth, and canopy optical properties were measured as indicative physiological parameters of tree stress response. Cessation of stem growth was the first stress signal after bark beetle infestation, while sap flux density declines > 40% occurred weeks later. Additionally, girdled–bark beetle–infested trees showed an anticipated decrease in sap flux density with increasing vapour pressure deficit and declines in canopy reflectance. Girdled–only trees did not show statistically significant differences in sap flux density or stem growth compared to the control, and have not yet experienced mortality since the start of the experiment. Mechanical phloem disruption alone does not cause rapid Norway spruce mortality, indicating that additional factors, such as fungal sapwood infection, might strongly contribute to bark beetle–induced death. Mortality appears to be preceded by a shift of resources from growth to defence, followed by hydraulic failure. Radial growth monitoring thus provides a valuable tool for early detection and modelling of beetle–driven spruce decline.

Keywords

Picea abies / Ips typographus / Ecophysiology / Forest disturbance / Insects

Cite this article

Download citation ▾
Anna Candotti, Henrik Hartmann, Enrico Tomelleri. Stem girdling does not allow mimicking changes in Norway spruce tree physiology during Eurasian spruce bark beetle infestation. Journal of Forestry Research, 2026, 37(1): 109 DOI:10.1007/s11676-026-02058-3

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Anderegg WRL, Hicke JA, Fisher RA, Allen CD, Aukema J, Bentz B, Hood S, Lichstein JW, Macalady AK, McDowell N, Pan YD, Raffa K, Sala AN, Shaw JD, Stephenson NL, Tague C, Zeppel M. Tree mortality from drought, insects, and their interactions in a changing climate. New Phytol, 2015, 208(3): 674-683

[2]

Aryal S, Häusser M, Grießinger J, Fan ZX, Bräuning A. “DendRoAnalyst”: a tool for processing and analysing dendrometer data. Dendrochronologia, 2020, 64: 125772

[3]

Asgharinia S, Leberecht M, Belelli Marchesini L, Friess N, Gianelle D, Nauss T, Opgenoorth L, Yates J, Valentini R. Towards continuous stem water content and sap flux density monitoring: IoT-based solution for detecting changes in stem water dynamics. Forests, 2022, 13(7): 1040

[4]

Ayres MP, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E. Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology, 2000, 81(8): 2198

[5]

Ballard RG, Walsh MA, Cole WE. Blue-stain fungi in xylem of lodgepole pine: a light-microscope study on extent of hyphal distribution. Can J Bot, 1982, 60(11): 2334-2341

[6]

Beetz K, Marrs C, Busse A, Poděbradská M, Kinalczyk D, Kranz J, Forkel M. Effects of bark beetle disturbance and fuel types on fire radiative power and burn severity in the Bohemian-Saxon Switzerland. Forestry, 2025, 98(1): 59-70

[7]

Børja I, Svĕtlík J, Nadezhdin V, Čermák J, Rosner S, Nadezhdina N. Sap flux–a real time assessment of health status in Norway spruce. Scand J for Res, 2016, 31(5): 450-457

[8]

Brinkmann N, Eugster W, Zweifel R, Buchmann N, Kahmen A. Temperate tree species show identical response in tree water deficit but different sensitivities in sap flow to summer soil drying. Tree Physiol, 2016, 36(12): 1508-1519

[9]

Chakraborty A, Purohit A, Khara A, Modlinger R, Roy A. Life-stage and geographic location determine the microbial assemblage in Eurasian spruce bark beetle, Ips typographus L. (Coleoptera: Curculionidae). Front for Glob Change, 2023, 6: 1176160

[10]

Christman MA, Sperry JS, Smith DD. Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species. New Phytol, 2012, 193(3): 713-720

[11]

Daudet FA. Experimental analysis of the role of water and carbon in tree stem diameter variations. J Exp Bot, 2004, 56: 135-144

[12]

Do F, Rocheteau A. Influence of natural temperature gradients on measurements of xylem sap flow with thermal dissipation probes. 1. Field observations and possible remedies. Tree Physiol, 2002, 22(9): 641-648

[13]

Domec JC, Pruyn ML. Bole girdling affects metabolic properties and root, trunk and branch hydraulics of young ponderosa pine trees. Tree Physiol, 2008, 28(10): 1493-1504

[14]

Dunn JP, Lorio PL. Effects of bark girdling on carbohydrate supply and resistance of loblolly pine to southern pine beetle (Dendroctonus frontalis Zimm.) attack. For Ecol Manag, 1992, 50(3–4): 317-330

[15]

Edburg SL, Hicke JA, Brooks PD, Pendall EG, Ewers BE, Norton U, Gochis D, Gutmann ED, Meddens AJ. Cascading impacts of bark beetle-caused tree mortality on coupled biogeophysical and biogeochemical processes. Front Ecol Environ, 2012, 10(8): 416-424

[16]

Einzmann K, Atzberger C, Pinnel N, Glas C, Böck S, Seitz R, Immitzer M. Early detection of spruce vitality loss with hyperspectral data: results of an experimental study in Bavaria, Germany. Remote Sens Environ, 2021, 266: 112676

[17]

Franceschi VR, Krokene P, Christiansen E, Krekling T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol, 2005, 167(2): 353-376

[18]

Gaylord ML, Kolb TE, Pockman WT, Plaut JA, Yepez EA, Macalady AK, Pangle RE, McDowell NG. Drought predisposes piñon–juniper woodlands to insect attacks and mortality. New Phytol, 2013, 198(2): 567-578

[19]

Ghimire RP, Kivimäenpää M, Blomqvist M, Holopainen T, Lyytikäinen-Saarenmaa P, Holopainen JK. Effect of bark beetle (Ips typographus L.) attack on bark VOC emissions of Norway spruce (Picea abies L.) trees. Atmos Environ, 2016, 126: 145-152

[20]

Granier A. Une nouvelle méthode pour la mesure du flux de sève brute dans le tronc des arbres. Ann for Sci, 1985, 42(2): 193-200

[21]

Hammond WM, Yu KL, Wilson LA, Will RE, Anderegg WRL, Adams HD. Dead or dying? Quantifying the point of no return from hydraulic failure in drought-induced tree mortality. New Phytol, 2019, 223(4): 1834-1843

[22]

Hartmann H, Ziegler W, Trumbore S. Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol, 2013, 27(2): 413-427

[23]

Hartmann H, Moura CF, Anderegg WRL, Ruehr NK, Salmon Y, Allen CD, Arndt SK, Breshears DD, Davi H, Galbraith D, Ruthrof KX, Wunder J, Adams HD, Bloemen J, Cailleret M, Cobb R, Gessler A, Grams TEE, Jansen S, Kautz M, Lloret F, O’Brien M. Research frontiers for improving our understanding of drought-induced tree and forest mortality. New Phytol, 2018, 218(1): 15-28

[24]

Henriksson N, Tarvainen L, Lim H, Tor-Ngern P, Palmroth S, Oren R, Marshall J, Näsholm T. Stem compression reversibly reduces phloem transport inPinus sylvestristrees. Tree Physiol, 2015, 35(10): 1075-1085

[25]

Hlásny T, König L, Krokene P, Lindner M, Montagné-Huck C, Müller J, Qin H, Raffa KF, Schelhaas MJ, Svoboda M, Viiri H, Seidl R. Bark beetle outbreaks in Europe: state of knowledge and ways forward for management. Curr for Rep, 2021, 7(3): 138-165

[26]

Hornslein NJ, Siegert CM, Renninger HJ. Changes in physiological functioning in loblolly pine trees undergoing bark beetle simulated mortality. For Sci, 2019, 65(3): 312-323

[27]

Huang JB, Kautz M, Trowbridge AM, Hammerbacher A, Raffa KF, Adams HD, Goodsman DW, Xu CG, Meddens AJH, Kandasamy D, Gershenzon J, Seidl R, Hartmann H. Tree defence and bark beetles in a drying world: carbon partitioning, functioning and modelling. New Phytol, 2020, 225(1): 26-36

[28]

Hubbard RM, Rhoades CC, Elder K, Negron J. Changes in transpiration and foliage growth in lodgepole pine trees following mountain pine beetle attack and mechanical girdling. For Ecol Manag, 2013, 289: 312-317

[29]

Iglesias DJ, Lliso I, Tadeo FR, Talon M. Regulation of photosynthesis through source: sink imbalance in Citrus is mediated by carbohydrate content in leaves. Physiol Plant, 2002, 116(4): 563-572

[30]

Jian SQ, Han YF, Kasanen R, Honkaniemi J, Junttila S, Asiegbu FO. Implications for the distributional range of the European bark beetles under future climate change. Sci Rep, 2025, 15: 29556

[31]

Jolly WM, Parsons RA, Hadlow AM, Cohn GM, McAllister SS, Popp JB, Hubbard RM, Negron JF. Relationships between moisture, chemistry, and ignition of Pinus contorta needles during the early stages of mountain pine beetle attack. For Ecol Manag, 2012, 269: 52-59

[32]

Junttila S, Yrttimaa T, Blomqvist M, Paljakka T, Pelto-Arvo M, Vastaranta M. Influence of bark beetle infestation on stem diameter dynamics. Trees for People, 2025, 19: 100777

[33]

Kandasamy D, Zaman R, Nakamura Y, Zhao T, Hartmann H, Andersson MN, Hammerbacher A, Gershenzon J. Conifer-killing bark beetles locate fungal symbionts by detecting volatile fungal metabolites of host tree resin monoterpenes. PLoS Biol, 2023, 21(2): e3001887

[34]

Kautz M, Peter FJ, Harms L, Kammen S, Delb H. Patterns, drivers and detectability of infestation symptoms following attacks by the European spruce bark beetle. J Pest Sci, 2023, 96(1): 403-414

[35]

Keeling CI, Bohlmann J. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol, 2006, 170(4): 657-675

[36]

Kirisits T, Offenthaler I. Xylem sap flow of Norway spruce after inoculation with the blue-stain fungus Ceratocystis polonica. Plant Pathol, 2002, 51(3): 359-364

[37]

Krokene P. Conifer defense and resistance to bark beetles. Bark beetles, 2015, Amsterdam. Elsevier: 177-207

[38]

Kshatriya K, Gershenzon J. Disarming the defenses: Insect detoxification of plant defense-related specialized metabolites. Curr Opin Plant Biol, 2024, 81: 102577

[39]

López R, Brossa R, Gil L, Pita P. Stem girdling evidences a trade-off between cambial activity and sprouting and dramatically reduces plant transpiration due to feedback inhibition of photosynthesis and hormone signaling. Front Plant Sci, 2015, 6: 285

[40]

Marini L, Lindelöw Å, Jönsson AM, Wulff S, Schroeder LM. Population dynamics of the spruce bark beetle: a long-term study. Oikos, 2013, 122(12): 1768-1776

[41]

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

[42]

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

[43]

McDowell NG, Sapes G, Pivovaroff A, Adams HD, Allen CD, Anderegg WRL, Arend M, Breshears DD, Brodribb T, Choat B, Cochard H, De Cáceres M, De Kauwe MG, Grossiord C, Hammond WM, Hartmann H, Hoch G, Kahmen A, Klein T, MacKay DS, Mantova M, Martínez-Vilalta J, Medlyn BE, Mencuccini M, Nardini A, Oliveira RS, Sala AN, Tissue DT, Torres-Ruiz JM, Trowbridge AM, Trugman AT, Wiley E, Xu CG. Mechanisms of woody-plant mortality under rising drought, CO2 and vapour pressure deficit. Nat Rev Earth Environ, 2022, 3(5): 294-308

[44]

Mencuccini M, Minunno F, Salmon Y, Martínez-Vilalta J, Hölttä T. Coordination of physiological traits involved in drought-induced mortality of woody plants. New Phytol, 2015, 208(2): 396-409

[45]

Miller RH, Berryman AA. Carbohydrate allocation and mountain pine beetle attack in girdled lodgepole pines. Can J for Res, 1986, 16(5): 1036-1040

[46]

Netherer S, Hammerbacher A. The Eurasian spruce bark beetle in a warming climate: Phenology, behavior, and biotic interactions. Bark beetle management, ecology, and climate change, 2022, Amsterdam. Elsevier: 89-131

[47]

Pierrat ZA, Magney TS, Richardson WP, Runkle BRK, Diehl JL, Yang X, Woodgate W, Smith WK, Johnston MR, Ginting YRS, Koren G, Albert LP, Kibler CL, Morgan BE, Barnes M, Uscanga A, Devine C, Javadian M, Meza K, Julitta T, Tagliabue G, Dannenberg MP, Antala M, Wong CYS, Santos ALD, Hufkens K, Marrs JK, Stovall AEL, Liu YJ, Fisher JB, Gamon JA, Cawse-Nicholson K. Proximal remote sensing: an essential tool for bridging the gap between high-resolution ecosystem monitoring and global ecology. New Phytol, 2025, 246(2): 419-436

[48]

Preisler Y, Tatarinov F, Grünzweig JM, Bert D, Ogée J, Wingate L, Rotenberg E, Rohatyn S, Her N, Moshe I, Klein T, Yakir D. Mortality versus survival in drought-affected Aleppo pine forest depends on the extent of rock cover and soil stoniness. Funct Ecol, 2019, 33(5): 901-912

[49]

Preisler Y, Tatarinov F, Grünzweig JM, Yakir D. Seeking the “point of no return” in the sequence of events leading to mortality of mature trees. Plant Cell Environ, 2021, 44(5): 1315-1328

[50]

Pugh E, Gordon E. A conceptual model of water yield effects from beetle-induced tree death in snow-dominated lodgepole pine forests. Hydrol Process, 2013, 27(14): 2048-2060

[51]

Rademacher TT, Basler D, Eckes-Shephard AH, Fonti P, Friend AD, Le Moine J, Richardson AD. Using direct phloem transport manipulation to advance understanding of carbon dynamics in forest trees. Front for Glob Change, 2019, 2: 11

[52]

Rademacher TT, Fonti P, LeMoine JM, Fonti MV, Basler D, Chen YZ, Friend AD, Seyednasrollah B, Eckes-Shephard AH, Richardson AD. Manipulating phloem transport affects wood formation but not local nonstructural carbon reserves in an evergreen conifer. Plant Cell Environ, 2021, 44(8): 2506-2521

[53]

Raffa KF, Berryman AA. The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). Ecol Monogr, 1983, 53(1): 27-49

[54]

Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA, Turner MG, Romme WH. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. Bioscience, 2008, 58(6): 501-517

[55]

Setter TL, Brun WA, Brenner ML. Stomatal closure and photosynthetic inhibition in soybean leaves induced by petiole girdling and pod removal. Plant Physiol, 1980, 65(5): 884-887

[56]

Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ, 2014, 37(1): 153-161

[57]

Six DL, Wingfield MJ. The role of phytopathogenicity in bark beetle–fungus symbioses: a challenge to the classic paradigm. Annu Rev Entomol, 2011, 56: 255-272

[58]

Six DL, Hammerbacher A, Trowbridge A, Bullington L. From beginning to end: the synecology of tree-killing bark beetles, fungi, and trees. Biol Rev, 2026, 101(1): 314-335

[59]

Sperry JS. Hydraulic constraints on plant gas exchange. Agric for Meteor, 2000, 104(1): 13-23

[60]

Stříbrská B, Hradecký J, Čepl J, Modlinger R, Tomášková I, Jirošová A. Physiological and biochemical indicators in Norway spruces freshly infested by Ips typographus: potential for early detection methods. Front for Glob Change, 2023, 6: 1197229

[61]

Thurner M, Beer C, Crowther T, Falster D, Manzoni S, Prokushkin A, Schulze ED. Sapwood biomass carbon in northern boreal and temperate forests. Global Ecol Biogeogr, 2019, 28(5): 640-660

[62]

Toffin E, Gabriel E, Louis M, Deneubourg JL, Grégoire JC. Colonization of weakened trees by mass-attacking bark beetles: no penalty for pioneers, scattered initial distributions and final regular patterns. R Soc Open Sci, 2018, 5(1): 170454

[63]

Tomelleri E, Belelli Marchesini L, Yaroslavtsev A, Asgharinia S, Valentini R. Toward a unified TreeTalker data curation process. Forests, 2022, 13(6): 855

[64]

Vaglio Laurin G, Cotrina-Sanchez A, Belelli-Marchesini L, Tomelleri E, Battipaglia G, Cocozza C, Niccoli F, Kabala JP, Gianelle D, Vescovo L, Da Ros L, Valentini R. Comparing ground below-canopy and satellite spectral data for an improved and integrated forest phenology monitoring system. Ecol Indic, 2024, 158: 111328

[65]

Valentini R, Marchesini LB, Gianelle D, Tognetti R, Panzacchi P, Marshall J. New tree monitoring systems: from industry 4.0 to nature 4.0. Ann Silvic Res, 2019, 43: 84-88

[66]

Vázquez-González C, Zas R, Erbilgin N, Ferrenberg S, Rozas V, Sampedro L. Resin ducts as resistance traits in conifers: linking dendrochronology and resin-based defences. Tree Physiol, 2020, 40(10): 1313-1326

[67]

Williams LE, Retzlaff WA, Yang WG, Biscay PJ, Ebisuda N. Effect of girdling on leaf gas exchange, water status, and non-structural carbohydrates of field-grown Vitis vinifera L. (cv. flame seedless). Am J Enol Vitic, 2000, 51(1): 49-54

[68]

Wullschleger SD, McLaughlin SB, Ayres MP. High-resolution analysis of stem increment and sap flow for loblolly pine trees attacked by southern pine beetle. Can J for Res, 2004, 34(11): 2387-2393

[69]

Yamaoka Y, Swanson RH, Hiratsuka Y. Inoculation of lodgepole pine with four blue-stain fungi associated with mountain pine beetle, monitored by a heat pulse velocity (HPV) instrument. Can J for Res, 1990, 20(1): 31-36

[70]

Zarco-Tejada PJ, Camino C, Beck PSA, Calderon R, Hornero A, Hernández-Clemente R, Kattenborn T, Montes-Borrego M, Susca L, Morelli M, Gonzalez-Dugo V, North PRJ, Landa BB, Boscia D, Saponari M, Navas-Cortes JA. Previsual symptoms of Xylella fastidiosa infection revealed in spectral plant-trait alterations. Nat Plants, 2018, 4(7): 432-439

[71]

Zhang X, Zhang X, Terfa BK, Nam WH, Zeng JY, Ma HL, Gu XH, Du WY, Wang C, Yang J, Wang P, Niyogi D, Chen NC. Mapping global drought-induced forest mortality based on multiple satellite vegetation optical depth data. Remote Sens Environ, 2024, 315: 114406

[72]

Zhao SY, Erbilgin N. Larger resin ducts are linked to the survival of lodgepole pine trees during mountain pine beetle outbreak. Front Plant Sci, 2019, 10: 1459

[73]

Zweifel R, Zimmermann L, Newbery DM. Modeling tree water deficit from microclimate: an approach to quantifying drought stress. Tree Physiol, 2005, 25(2): 147-156

Funding

Libera Università di Bolzano

RIGHTS & PERMISSIONS

The Author(s)

PDF

0

Accesses

0

Citation

Detail

Sections
Recommended

/