Abstract
Key message
Repeated defoliation soon after full leaf expansion reduces xylem hydraulic transport safety in beech trees.
Abstract
Japanese beech trees undergo branch dieback and eventual mortality following years of repeated leaf loss due to leaf-feeding insects attacking immediately after full leaf expansion. To study the impact of recurrent defoliation on beech debilitation and mortality, we investigated xylem hydraulic transport safety and observed the xylem vessel architecture in field-grown medium-sized Japanese beech trees that had been artificially defoliated repeatedly for 4 years immediately after full leaf expansion. Multiple years of defoliation immediately after full leaf expansion increased the susceptibility to xylem cavitation (P50 value; − 4.46 ± 0.38 MPa (mean ± SD) for non-defoliated control beeches, and − 2.32 ± 0.20 MPa for defoliated beeches), despite a decrease in their vessel diameter and an increase in their vessel density. In defoliated beech, many irregularly shaped, axially wrinkled and partially cracked vessels, mountain-folded intervessel pits, and fibers with thin and less-lignified cell walls were observed. The intervessel double-wall thickness of the defoliated beech was thinner than that of the control beech. Furthermore, the size and shape of intervessel pits did not change in defoliated beech, but the density of intervessel pits and the total number and total area of intervessel pits per 1 mm of vessel length increased. We conclude that the increased susceptibility to xylem cavitation caused by repeated defoliation immediately after full leaf expansion may be due to an increased total area of intervessel pits with thin pit membranes per unit vessel wall area, in addition to cell wall alteration and vessel deformation and damage.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data of this study are available upon reasonable request to the author for correspondence.
References
Aihara K, Aso T, Takeda M, Koshiji T (2004) Forest decline of the present situation and initiatives (II) The tree decline in Tanzawa Mountain, Kanagawa Prefecture. J Jpn Soc Atmos Environ 39:29–39
Alder NN, Pockman WT, Sperry JS, Nuismer S (1997) Use of centrifugal force in the study of xylem cavitation. J Exp Bot 48:665–674. https://doi.org/10.1093/jxb/48.3.665
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, 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. https://doi.org/10.1016/j.foreco.2009.09.001
Anderegg WRL, Hicke JA, Fisher RA (2015) Tree mortality from drought, insects, and their interactions in a changing climate. New Phytol 208:674–683. https://doi.org/10.1111/nph.13477
Anderegg WRL, Klein T, Bartlett M, Sack L, Pellegrini AFA, Choat B, Jansen S (2016) Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc Natl Acad Sci USA 113:5024–5029. https://doi.org/10.1073/pnas.152567811
Balduccia L, Fierravantia A, Rossia S, Delzonc S, De Grandpréd L, Kneeshawe DD, Deslauriersa A (2020) The paradox of defoliation: declining tree water status with increasing soil water content. Agric for Meteorol 290:108025. https://doi.org/10.1016/j.agrformet.2020.108025
Barotto AJ, Monteoliva S, Gyenge J, Martinez-Meier A, Melena F (2018) Functional relationships between wood structure and vulnerability to xylem cavitation in races of Eucalyptus globulus differing in wood density. Tree Physiol 38:243–251. https://doi.org/10.1093/treephys/tpx138
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755. https://doi.org/10.1038/nature11688
Choat B, Badel E, Burlett R, Delzon S, Cochard H, Jansen S (2016) Noninvasive measurement of vulnerability to drought-induced embolism by X-ray microtomography. Plant Physiol 170:273–282. https://doi.org/10.1104/pp.15.00732
Christman MA, Sperry JS, Adler FR (2009) Testing the ‘rare pit’ hypothesis for xylem cavitation resistance in three species of Acer. New Phytol 182:664–674. https://doi.org/10.1111/j.1469-8137.2009.02776.x
Cochard H, Cruiziat P, Tyree MT (1992) Use of positive pressures to establish vulnerability curves—further support for the air-seeding hypothesis and implications for pressure volume analysis. Plant Physiol 100:205–209. https://doi.org/10.1104/pp.100.1.205
Conrad K (2008) Correlation between the distribution of lignin and pectin and distribution of sorbed metal ions (lead and zinc) on coir (Cocos nucifera L.). Bioresour Technol 99:8476–8484. https://doi.org/10.1016/j.biortech.2007.08.088
Domec JC, Rivera LN, King JS, Peszlen I, Hain F, Smith B, Frampton J (2013) Hemlock woolly adelgid (Adelges Tugae) infestation affects Water and carbon relations of eastern hemlock (Tsuga canadensis) and Carolina hemlock (Tsuga caroliniana). New Phytol 199:163–452. https://doi.org/10.1111/nph.12263
Dória LC, Podadera DS, del Arco M, Chauvin T, Smets E, Delzon S, Lens F (2018) Insular woody daisies (Argyranthemum, Asteraceae) are more resistant to drought-induced hydraulic failure than their herbaceous relatives. Funct Ecol 32:1467–1478. https://doi.org/10.1111/1365-2435.13085
Foster JR (2017) Xylem traits, leaf longevity and growth phenology predict growth and mortality response to defoliation in northern temperate forests. Tree Physiol 37:1151–1165. https://doi.org/10.1093/treephys/tpx043
Girardin MP, Tardif J, Bergeron Y (2001) Radial growth analysis of Larix laricina from the Lake Deparquet area, Quebec, in relation to climate and larch sawfly outbreaks. Ecoscience 8:127–138. https://doi.org/10.1080/11956860.2001.11682638
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:619–701. https://doi.org/10.1093/treephys/26.6.689
Hillabrand RM, Hacke UG, Lieffers VJ (2019) Defoliation constrains xylem and phloem functionality. Tree Physiol 39:1099–1108. https://doi.org/10.1093/treephys/tpz029
Hogg EH, Hart M, Lieffers VJ (2002) White tree rings formed in trembling aspen saplings following experimental defoliation. Can J for Res 32:1929–1934. https://doi.org/10.1139/x02-114
Hotta I, Morikawa Y, Touge H, Matumot Y, Maruyama Y, Ishizuka K (1993) Forest decline. Kashiyo, Tokyo
Hudson PJ, Limousin JM, Krofcheck DJ (2018) Impacts of long-term precipitation manipulation on hydraulic architecture and xylem anatomy of piñon and juniper in Southwest USA. Plant Cell Environ 41:421–435. https://doi.org/10.1111/pce.13109
Huggett BA, Savage JA, Hao G, Preisser EL, Holbrook NM (2018) Impact of hemlock woolly adelgid (Adelges tsugae) infestation on xylem structure and function and leaf physiology in eastern hemlock (Tsuga canadensis). Funct Plant Biol 45:501–508. https://doi.org/10.1071/FP17233
Jacobsen AL, Ewers FW, Pratt RB, Paddock WA III, Davis SD (2005) Do xylem fibers affect vessel cavitation resistance? Plant Physiol 139:546–556. https://doi.org/10.1104/pp.104.058404
Jansen S, Choat B, Pletsers A (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am J Bot 96:409–419. https://doi.org/10.3732/ajb.0800248
Jansen S, Gortan E, Lens F, Lo Gullo MA, Salleo S, Scholz A, Stein A, Trifilò P, Nardini A (2011) Do quantitative vessel and pit characters account for ion-mediated changes in the hydraulic conductance of angiosperm xylem? New Phytol 189:218–228. https://doi.org/10.1111/j.1469-8137.2010.03448.x
Kaack L, Weber M, Isasa E, Karimi Z, Li S, Pereira L, Trabi CL, Zhang Y, Schenk HJ, Schuldt B (2021) Pore constrictions intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms. New Phytol 230:1829–1843. https://doi.org/10.1111/nph.17282
Koshiji T, Suzuki K, Suga K (1996) Investigation of forest decline in the Tanzawa mountain (1) Distribution of decline of Fagus crenata, Abies firma and other tree species. Bull Kanagawa Pref Res Inst 22:7–18
Koshiji M, Taniwaki T, Aihara K, Yamane M (2012) Sever damages on beec trees (Fagus crenata) caused by the outbreak of a sawfly (Fagineura crenativora) in Mt Hinokibotamaru. Bull Kanagawa Pref Nat Environ Conserv Cent 9:95–104
Lemaire C, Quilichini Y, Brunel-Michac N, Santini J, Berti L, Cartailler J, Conchon P, Badel E, Herbette S (2021) Plasticity of the xylem vulnerability to embolism in poplar relies on quantitative pit properties rather than on pit structure. Tree Physiol 41:1384–1399. https://doi.org/10.1093/treephys/tpab018
Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol 190:709–723. https://doi.org/10.1111/j.1469-8137.2010.03518.x
Lens F, Tixier A, Cochard H, Sperry JS, Jansen S, Herbette S (2013) Embolism resistance as a key mechanism to understand adaptive plant strategies. Curr Opin Plant Biol 16:287–292. https://doi.org/10.1016/j.pbi.2013.02.005
Lens F, Picon-Cochard C, Delmas CEL, Signarbieux C, Buttler A, Cochard H, Jansen S, Chauvin T, Doria LC, del Arco M, Delzon S (2016) Herbaceous angiosperms are not more vulnerable to drought-induced embolism than angiosperm trees. Plant Physiol 172:661–667. https://doi.org/10.1104/pp.16.00829
Lens F, Gleason SM, Bortolami G, Brodersen C, Delzon S, Jansen S (2022) Functional xylem characteristics associated with drought-induced embolism in angiosperms. New Phytol 236:2019–2036. https://doi.org/10.1111/nph.18447
Levionnois S, Jansen S, Wandji RT, Beauchêne J, Ziegler C, Calvet E, Coste S, Stahl C, Salmon C, Delzon S (2020) Linking drought-induced xylem embolism resistance to wood anatomical traits in neotropical trees. New Phytol 229:1453–1466. https://doi.org/10.1111/nph.16942
Li S, Lens F, Espino S, Karimi Z, Klepsch M, Schenk HJ, Schmitt M, Schuldt JS (2016) Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA J 37:152–171. https://doi.org/10.1163/22941932-20160128
Lobo A, Torres-Ruiz JM, Burlett R, Lemaire C, Parise C, Francioni C, Truffaut L, Tomášková I, Hansen JK, Kjær ED, Kremer A, Delzon S (2018) Assessing inter- and intraspecific variability of xylem vulnerability to embolism in oaks. For Ecol Manag 424:53–61. https://doi.org/10.1016/j.foreco.2018.04.031
Lopez OR, Kursar TA, Cochard H, Tyree MT (2005) Interspecific variation in xylem vulnerability to cavitation among tropical tree and shrub species. Tree Physiol 25:1553–1562. https://doi.org/10.1093/treephys/25.12.1553
Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199. https://doi.org/10.1890/02-0538
McDowell N, Pockman WT, Allen CD (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739. https://doi.org/10.1111/j.1469-8137.2008.02436.x
Neufeld HS, Grantz DA, Meinzer FC, Goldstein G, Crisostos GM, Crisostos C (1992) Genotypic variability in vulnerability of leaf xylem to cavitation in water-stressed and well-irrigated sugarcane. Plant Physiol 100:1020–1028. https://doi.org/10.1104/pp.100.2.1020
Ozawa M, Ueda M, Furui M, Uemura K (2019) Effects of artificial defoliation soon after leaf flushing simulating insect damage on both xylem hydraulic conductivity and fine-root mass of Japanese beech saplings. J Jpn Soc Reveget Tech 45:86–90. https://doi.org/10.7211/jjsrt.45.86
Pereira L, Domingues-Junior AP, Jansen S, Choat B, Marrafera P (2018) Is embolism resistance in plant xylem associated with quantity and characteristics of lignin? Trees 32:349–358. https://doi.org/10.1007/s00468-017-1574-y
Pfautsch S, Aspinwall MJ, Drake JE (2018) Traits and trade-offs in whole-tree hydraulic architecture along the vertical axis of Eucalyptus grandis. Ann Bot 121:129–141. https://doi.org/10.1093/aob/mcx137
Pinto CA, David JS, Cochard H, Calderia MC, Henriques MO, Quilho T, Paco TA, Pereira JS, David TS (2012) Drought-induced embolism in current-year shoots of two Mediterranean evergreen oaks. For Ecol Manag 285:1–10. https://doi.org/10.1016/j.foreco.2012.08.005
Plavcová L, Hacke UG (2012) Phenotypic and developmental plasticity of xylem in hybrid poplar saplings subjected to experimental drought, nitrogen fertilization, and shading. J Exp Bot 63:6481–6491. https://doi.org/10.1093/jxb/ers303
Pureswaran DS, Roques A, Battisti A (2018) Forest insects and climate change. Curr for Rep 4:35–50. https://doi.org/10.1007/s40725-018-0075-6
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Sakai WS (1973) Simple method for differential staining of paraffin embedded plant material using toluidine blue O. Stain Technol 48:247–249. https://doi.org/10.3109/10520297309116632
Salleo S, Nardini A, Raimondo F, 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. https://doi.org/10.1007/s00468-003-0247-1
Scholz A, Klepsch M, Karimi Z, Jansen S (2013) How to quantify conduits in wood? Front Plant Sci 4:56. https://doi.org/10.3389/fpls.2013.00056
Seidl R, Thom D, Kautz M, Martin-Benito D, Peltoniemi M, Vacchiano G, Wild J, Ascoli D, Petr M, Honkaniemi J, Lexer MJ, Trotsiuk V, Mairota P, Svoboda M, Fabrika M, Nagel TA, Reyer CPO (2017) Forest disturbances under climate change. Nat Clim Change 7:395–402. https://doi.org/10.1038/nclimate3303
Shen Y, Fukatsu E, Muraoka H, Saitoh TM, Hirano Y, Yasue K (2020) Climate responses of ring widths and radial growth phenology of Betula ermanii, Fagus crenata and Quercus crispula in a cool temperate forest in central Japan. Trees 34:679–692. https://doi.org/10.1007/s00468-019-01948-w
Skelton RP, Dawson TE, Thompson SE, Shen Y, Weitz AP, Ackerly D (2018) Low vulnerability to xylem embolism in leaves and stems of North American oaks. Plant Physiol 177:1066–1077. https://doi.org/10.1104/pp.18.00103
Sperry JS, Saliendra NZ (1994) Intra- and inter-plant variation in xylem cavitation in Betula occidentalis. Plant Cell Environ 17:1233–1241. https://doi.org/10.1111/j.1365-3040.1994.tb02021.x
Sperry JS, Saliendra NZ, Pockman WT, Cochard H, Cruiziat P, Davis SD, Ewers FW, Tyree MT (1996) New evidence for large negative xylem pressures and their measurement by the pressure chamber method. Plant Cell Environ 19:427–436. https://doi.org/10.1111/j.1365-3040.1996.tb00334.x
Sterck FJ, Zweifel R, Sass-Klaassen UTE, Chowdhury Q (2008) Persisting soil drought reduces leaf specific conductivity in Scots pine (Pinus sylvestris) and pubescent oak (Quercus pubescens). Tree Physiol 28:529–536. https://doi.org/10.1093/treephys/28.4.529
Sutton A, Tardif J (2005) Distribution and anatomical characteristics of white rings in Populus tremuloides. IAWA J 26:221–238
Takahashi S, Okada N, Nobuchi T (2013) Relationship between the timing of vessel formation and leaf phenology. Ecol Res 28:615–624. https://doi.org/10.1007/s11284-013-1053-x
Tani S, Banno H, Ymagami A (2009) Relationship between temperature and development speed in the egg and larval stages of a sawfly, Fagineura crenativora (Insecta Hymenoptera, Tenehredinidae) from Mt. Tanzawa, Kanagawa prefecture, Japan. Bull Lib Arts Educ Cent Tokai Univ 29:107–113
Taniwaki T, Koshiji M, Yamane M, Fujisawa T, Tamura A, Uchiyama Y, Sasakawa H (2008) Studies on monitoring methods of the population density of the sawfly Fagineura crenativora. Kantoshinnrinnkennkyu 59:239–242
Taniwaki T, Aihara K, Saito H, Yamane M (2016) Factors and its interactive effects on beech forests decline in the Tanzawa Mountains. Bull Kanagawa Pref Nat Environ Conserv Cent 14:1–12
Thonglim A, Delzon S, Larter M, Karami O, Rahimi A, Offringa R, Keurentjes JB, Balazadeh S, Smets E, Lens F (2020) Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions. Ann Bot 128:171–182. https://doi.org/10.1093/aob/mcaa196
Trueba S, Delzon S, Isnard S, Lens F (2019) Similar hydraulic efficiency and safety across vesselless angiosperms and vessel-bearing species with scalariform perforation plates. J Exp Bot 70:3227–3240. https://doi.org/10.1093/jxb/erz133
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Phys Mol Bio 40:19–38. https://doi.org/10.1146/annurev.pp.40.060189.000315
Ueda M (2024) Leaf water potentials and anatomical features of xylem vessels in Japanese beech trees (Fagus crenata Blume) growing on Mt. Hinokiboramaru, Tanzawa Mountains, Japan. Jpn J For Environ 66 (In press)
Ueda M, Taniwaki T, Saitou H, Aihara K (2019) Effects of artificial defoliation and water stress on anatomical features of xylem vessels of current-year shoots of Japanese Beech (Fagus crenata). J Jpn for Soc 101:76–81. https://doi.org/10.4005/jjfs.101.76
Uemura K, Ueda M, Taniwaki T, Saito H, Aihara K (2019) Effects of artificial defoliation on anatomical features of xylem vessels of current-year shoots of field grown middle-size Japanese beech (Fagus crenata Blume) trees. J Jpn Soc Reveget Technol 45:91–96. https://doi.org/10.7211/jjsrt.45.91
Wason JW, Anstreicher KS, Stephansky N, Huggett BA, Brodersen CR (2018) Hydraulic safety margins and air-seeding thresholds in roots, trunks, branches and petioles of four northern hardwood trees. New Phytol 219:77–88. https://doi.org/10.1111/nph.15135
Watanabe S (2011) An observation of the vascular bundle as an inquiring activity-development of teaching materials and method using the toluidine blue staining. Jpn J Biol Educ 52:1–12
Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Intervessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ 28:800–812. https://doi.org/10.1111/j.1365-3040.2005.01330.x
Yamagami A, Tani S, Banno H (2007) Dieback of beech trees (Fagus crenata) caused by the sawfly (Fagineura crenativora) damage and beech forest decline. In: The comprehensive Investigation Team of Tanzawa-Oyama (ed) The results of the scientific research on the Tanzawa Mountains. The Hiraoka Environmental Science Laboratory, Sagamihara, pp 256–268
Yamane M, Fujisawa T, Tamura A, Uchiyama Y, Sasagawa H, Koshiji T, Saito H (2007) The current situation of beech forest at Tanzawa Mountains. In: The comprehensive Investigation Team of Tanzawa-Oyama (ed) The results of the scientific research on the Tanzawa Mountains. The Hiraoka Environmental Science Laboratory, Sagamihara, pp 479–484
Zimmermann MH (1983) Xylem structure and ascent of sap. Springer, Berlin
Acknowledgements
We thank Prof. Sugimoto of Kyoto University for his advice on pit classification, and Prof. Furuta of Kyoto Prefectural University for the convenience of SEM observation. We thank Dr. Taniwaki, Mr. Saito, Mr Aihara, and stuff at the Kanagawa Prefecture Natural Environment Conservation Center for their help with leaf plucking in the field.
Funding
A part of this study was funded by Kanagawa Prefecture Nature Conservation Center.
Author information
Authors and Affiliations
Contributions
Conceptualization and methodology: MU; formal analysis and investigation: KI, SU; writing: MU.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Achim Bräuning.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ueda, M., Izumi, K. & Ueo, S. Repeated artificial defoliation soon after full leaf expansion, simulating insect damage, reduces xylem hydraulic transport safety in Japanese beech (Fagus crenata Blume). Trees 38, 303–313 (2024). https://doi.org/10.1007/s00468-023-02475-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-023-02475-5