Abstract
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Severe insect defoliation induced non-lignified tracheids and thin-walled latewood tracheids in the defoliation year in Larix kaempferi. These anomalous tracheids had heterogenous lignin deposition of S2 layer.
Abstract
Severe insect defoliation induces the formation of light ring consisted of thin-walled latewood tracheids in larch trees, which would affect wood quality. However, the identity of the secondary wall layers affected by insect defoliation remains unclear. The aim of this study is to clarify the effects of insect defoliation on the formation of secondary cell walls of tracheids in Larix kaempferi with focus on the defoliation timing. We observed by light microscopy and transmission electron microscopy (TEM) the secondary cell walls of tracheids produced in a defoliation year in L. kaempferi trees on which needles were attacked in July (gypsy moth, GM samples) or August (larch sawfly, LS samples). Light microscopy observations revealed that GM samples produced non-lignified tracheids in the transition zone between earlywood and latewood, as well as thin-walled latewood tracheids, and non-lignified tracheids were observed near the cambial zone in LS samples following defoliation for two consecutive years. TEM observations revealed that the tracheids in both samples had anomalous layers in secondary walls such as thin S2 layers with heterogeneous lignin deposition. The production of non-lignified tracheids corresponded to defoliation date in both samples, unlike changes in the layer composition of anomalous tracheids. Our study suggests that changes in wood structure depend on the date of insect defoliation and that insect defoliation affects the formation of secondary cell walls of tracheids, presumably in response to inadequate photosynthate supply as a result of defoliation.
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References
Aloni R (2007) Phytohormonal mechanisms that control wood quality formation in young and mature trees. In: Entwistle K, Harris P, Walker J (eds) The compromised wood workshop. Univ. of Canterbury, Christchurch, Wood Technology Research Centre, pp 1–22
Axelson JN, Bast A, Alfaro R, Smith DJ, Gärtner H (2014) Variation in wood anatomical structure of Douglas-fir defoliated by the western spruce budworm: a case study in the coastal-transitional zone of British Columbia, Canada. Trees Struct Funct 28:1837–1846. https://doi.org/10.1007/s00468-014-1091-1
Babst BA, Ferrieri RA, Gray DW et al (2005) Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 167:63–72. https://doi.org/10.1111/j.1469-8137.2005.01388.x
Baltensweiler W, Weber UM, Cherubini P (2008) Tracing the influence of larch-bud-moth insect outbreaks and weather conditions on larch tree-ring growth in Engadine (Switzerland). Oikos 117:161–172. https://doi.org/10.1111/j.2007.0030-1299.16117.x
Barnett JR (1976) Rings of collapsed cells in Pinus radiata stemwood from lysimeter-grown trees subjected to drought. N Zeal J For Sci 6:461–465
Cook ER, Peters K (1981) The smoothing spline: a new approach to standardizing forest interior tree-ring width series for dendroclimatic studies. Tree Ring Bull 41:41–53
Deslauriers A, Caron L, Rossi S (2015) Carbon allocation during defoliation: testing a defense-growth trade-off in balsam fir. Front Plant Sci 6:338. https://doi.org/10.3389/fpls.2015.00338
Donaldson LA (1992) Lignin distribution during latewood formation in Pinus radiata D. Don. IAWA Bull 13:381–387. https://doi.org/10.1163/22941932-90001291
Donaldson LA (2002) Abnormal lignin distribution in wood from severely drought stressed Pinus radiata trees. IAWA J 23:161–178. https://doi.org/10.1163/22941932-90000295
Elek JA, Baker SC (2017) Timing and frequency are the critical factors affecting the impact of defoliation on long term growth of plantation eucalypts. For Ecol Manag 391:1–8. https://doi.org/10.1016/j.foreco.2017.02.004
Epron D, Bahn M, Derrien D et al (2012) Pulse-labelling trees to study carbon allocation dynamics: a review of methods, current knowledge and future prospects. Tree physiol 32:776–798. https://doi.org/10.1093/treephys/tps057
Filion L, Cournoyer L (1995) Variation in wood structure of eastern larch defoliated by the larch sawfly in subarctic Quebec, Canada. Can J For Res 25:1263–1268. https://doi.org/10.1139/x95-139
Gärtner H, Schweingruber FH (2013) Microscopic preparation techniques for plant stem analysis. Verlag Dr. Kessel, Remagen
Harper AG (1913) Defoliation: its effects upon the growth and structure of the wood of Larix. Ann Bot 27:621–642
Hartmann H, Adams HD, Hammond WM et al (2018) Identifying differences in carbohydrate dynamics of seedlings and mature trees to improve carbon allocation in models for trees and forests. Environ Exp Bot 152:7–18. https://doi.org/10.1016/j.envexpbot.2018.03.011
Haynes KJ, Allstadt AJ, Klimetzek D (2014) Forest defoliator outbreaks under climate change: effects on the frequency and severity of outbreaks of five pine insect pests. Glob Change Biol 20:2004–2018. https://doi.org/10.1111/gcb.12506
Hill SA, Waterhouse JS, Field EM, Switsur VR, Ap Rees T (1995) Rapid recycling of triose phosphates in oak stem tissue. Plant Cell Environ 18:931–936. https://doi.org/10.1111/j.1365-3040.1995.tb00603.x
Hogg EH, Brandt JP, Kochtubajda B (2002a) Growth and dieback of aspen forests in northwestern Alberta, Canada, in relation to climate and insects. Can J For Res 32:823–832. https://doi.org/10.1139/x01-152
Hogg EH, Hart M, Lieffers VJ (2002b) 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
Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree Ring Bull 43:69–75
Hultine KR, Nagler PL, Morino K et al (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. https://doi.org/10.1016/j.agrformet.2010.07.009
Imagawa H, Ishida S (1970) Study on the wood formation in trees. Report 1. Seasonal development of the xylem ring of Japanese larch stem, Larix leptolepis Gordon. Res Bull Coll Exp For Hokkaido Univ 27:373–394
Kagawa A, Sugimoto A, Maximov TC (2006) 13CO2 pulse-labelling of photoassimilates reveals carbon allocation within and between tree rings. Plant Cell Environ 29:1571–1584. https://doi.org/10.1111/j.1365-3040.2006.01533.x
Kitaoka S, Koike T, Quoreshi AM et al (2001) Seasonal changes in the photosynthetic capacity of Japanese larch trees planted on the Tomakomai National Forest, northern Japan. In: Proc international workshop for advanced flux network and flux evaluation, vol 1, pp 109–112
Kosola KR, Dickmann DI, Paul EA, Parry D (2001) Repeated insect defoliation effects on growth, nitrogen acquisition, carbohydrates, and root demography of poplars. Oecologia 129:65–74. https://doi.org/10.1007/s004420100694
Krause C, Morin H (1995) Impact of spruce budworm defoliation on the number of latewood tracheids in balsam fir and black spruce. Can J For Res 25:2029–2034. https://doi.org/10.1139/x95-219
Kulman HM (1971) Effects of insect defoliation on growth and mortality of trees. Annu Rev Entomol 16:289–324. https://doi.org/10.1146/annurev.en.16.010171.001445
Liang C, Filion L, Cournoyer L (1997) Wood structure of biotically and climatically induced light rings in eastern larch (Larix laricina). Can J For Res 27:1538–1547. https://doi.org/10.1139/x97-117
Liebhold A, Elkinton J, Williams D, Muzika RM (2000) What causes outbreaks of the gypsy moth in North America? Popul Ecol 42:257–266. https://doi.org/10.1007/PL00012004
Long RP, Trimpey DW, Wiemann MC, Stout SL (2012) Anomalous dark growth rings in black cherry. N J Appl For 29:150–154. https://doi.org/10.5849/njaf.11-043
Long RP, Wiemann MC, Kuster TA (2018) The frequency and anatomical characteristics of anomalous dark rings in black cherry, and their relation to cherry scallop shell moth defoliations. For Sci 65:324–335. https://doi.org/10.1093/forsci/fxy057
Nemoto M, Hamasaki T, Shimono H (2011) Extraordinary hot summer in Hokkaido decrease rice yield and satisfy growing of cultivar in Tohoku region “Hitomebore”. J Agric Meteorol 67:269–274. https://doi.org/10.2480/agrmet.67.4.1
Ozaki K, Fukuyama K, Isono M, Takao G (2004) Simultaneous outbreaks of three species of larch web-spinning sawflies: influences of weather and stand structure. For Ecol Manag 187:75–84. https://doi.org/10.1016/S0378-1127(03)00308-6
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 49:871–878. https://doi.org/10.1093/jxb/49.322.871
Paixao C, Krause C, Morin H, Achim A (2019) Wood quality of black spruce and balsam fir trees defoliated by spruce budworm: a case study in the boreal forest of Quebec, Canada. For Ecol Manag 437:201–210. https://doi.org/10.1016/j.foreco.2019.01.032
Piermattei A, Crivellaro A, Carrer M, Urbinati C (2015) The “blue ring”: anatomy and formation hypothesis of a new tree-ring anomaly in conifers. Trees 29:613–620. https://doi.org/10.1007/s00468-014-1107-x
Pinkantayong P, Kubo M, Terada T et al (2015) The effect of successive years of defoliation by the larch sawfly (Pristiphora erichsonii (Hartig)) on the foliage properties of the Japanese larch (Larix kaempferi (Lamb.) Carr.), with particular reference to the CN balance hypothesis. J For Res 20:104–113. https://doi.org/10.1007/s10310-014-0442-5
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 115:1093–1103. https://doi.org/10.1093/aob/mcv038
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
Puri E, Hoch G, Körner C (2015) Defoliation reduces growth but not carbon reserves in Mediterranean Pinus pinaster. Trees Struct Funct 29:1187–1196. https://doi.org/10.1007/s00468-015-1199-y
Rinne P, Tuominen H, Sundberg B (1993) Growth patterns and endogenous indole-3-acetic acid concentrations in current-year coppice shoots and seedlings of two Betula species. Physiol Plant 88:403–412. https://doi.org/10.1111/j.1399-3054.1993.tb01352.x
Ryu K, Watanabe M, Shibata H, Takagi K, Nomura M, Koike T (2009) Ecophysiological responses of the larch species in northern Japan to environmental changes as a basis for afforestation. Landsc Ecol Eng 5:99–106. https://doi.org/10.1007/s11355-009-0063-x
Sitbon F, Hennion S, Sundberg B, Little CA, Olsson O, Sandberg G (1992) Transgenic tobacco plants coexpressing the Agrobacterium tumefaciens iaaM and iaaH genes display altered growth and indoleacetic acid metabolism. Plant Physiol 99:1062–1069. https://doi.org/10.1104/pp.99.3.1062
Sitbon F, Hennion S, Little CA, Sundberg B (1999) Enhanced ethylene production and peroxidase activity in IAA-overproducing transgenic tobacco plants is associated with increased lignin content and altered lignin composition. Plant Sci 141:165–173. https://doi.org/10.1016/S0168-9452(98)00236-2
Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultra Mol Struct Res 26:31–43. https://doi.org/10.1016/S0022-5320(69)90033-1
Sundberg B, Little CA (1987) Effect of defoliation on tracheid production and the level of indole-3-acetic acid in Abies balsamea shoots. Physiol Plant 71:430–435. https://doi.org/10.1111/j.1399-3054.1987.tb02879.x
Sutton A, Tardif J (2005) Distribution and anatomical characteristics of white rings in Populus tremuloides. IAWA J 26:221–238
Thiéry JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6:987–1018
Tardif JC, Girardin MP, Conciatori F (2011) Light rings as bioindicators of climate change in Interior North America. Glob Planet Change 79:134–144. https://doi.org/10.1016/j.gloplacha.2011.09.001
Vazquez-Cooz I, Meyer RW (2002) A differential staining method to identify lignified and unlignified tissues. Biotech Histochem 77:277–282. https://doi.org/10.1080/bih.77.5-6.277.282
Villar-Salvador P, Uscola M, Jacobs DF (2015) The role of stored carbohydrates and nitrogen in the growth and stress tolerance of planted forest trees. New For 46:813–839. https://doi.org/10.1007/s11056-015-9499-z
Volney WJA, Mallett KI (1992) Light rings and the age of jack pine trees. Can J For Res 22:2011–2013. https://doi.org/10.1139/x92-264
Watanabe Y, Sano Y, Asada T, Funada R (2006) Histochemical study of the chemical composition of vestured pits in two species of Eucalyptus. IAWA J 27:33–43. https://doi.org/10.1163/22941932-90000135
Wiley E, Helliker B (2012) A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol 195:285–289. https://doi.org/10.1111/j.1469-8137.2012.04180.x
Acknowledgements
We thank N. Tashiro and S. Inoue for sampling in Ashoro Research Forest, Kyushu University. We also thank T. Ito for assistance with TEM studies and Y. Sano for useful advice on polarized light microscopy. This work was supported by JSPS KAKENHI Grant Numbers JP23580214, JP26450205, and JP15K0746605.
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Watanabe, Y., Ohno, Y. Severe insect defoliation at different timing affects cell wall formation of tracheids in secondary xylem of Larix kaempferi. Trees 34, 931–941 (2020). https://doi.org/10.1007/s00468-020-01971-2
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DOI: https://doi.org/10.1007/s00468-020-01971-2