Abstract
Deciduous trees can survive severe defoliation by herbivores and often refoliate in the same season. Refoliation following severe defoliation represents compensatory regrowth to recover foliage biomass. Although the relationship between defoliation intensity and degree of refoliation at the individual level has been quantified following artificial defoliation for saplings and small trees, no study has examined the relationship for canopy trees and interspecific differences in this relationship. In this study, defoliation by gypsy moths in an outbreak year and subsequent refoliation were visually surveyed for canopy trees of Fagus crenata (n = 80) and Quercus crispula (n = 113) in central Japan. Defoliation and refoliation estimates were scored in 10% classes as the ratio to foliage present before defoliation. The degree of refoliation and the proportion of refoliated trees were high in severely defoliated trees. For 60 and 100% defoliated trees, respective refoliations were 2 and 66% for F. crenata, and 37 and 88% for Q. crispula. All of the 90 and 100% defoliated trees refoliated. These results indicate that severely defoliated trees show an increased need for refoliation to maintain metabolism. Beta regression analysis showed that Q. crispula possessed higher refoliation capability than F. crenata. This is likely associated with the relatively large storage reserves and recurrent growth flush pattern of oak species, which are strong characteristics of oaks and adaptive for response to herbivory and catastrophic disturbances. Interspecific differences in refoliation capability may exert differential effects on forest ecosystem processes, such as influencing the growth of understory species.
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References
Abrams MD (1992) Fire and the development of oak forests. Bioscience 42:346–353. https://doi.org/10.2307/1311781
Arimoto M, Iwaizumi R (2014) Identification of Japanese Lymantria species (Lepidoptera: Lymantriidae) based on PCR–RFLP analysis of mitochondrial DNA. Appl Entomol Zool 49:159–169. https://doi.org/10.1007/s13355-013-0235-x
Augspurger CK (2009) Spring 2007 warmth and frost: phenology, damage and refoliation in a temperate deciduous forest. Func Ecol 23:1031–1039. https://doi.org/10.1111/j.1365-2435.2009.01587.x
Augspurger CK (2011) Frost damage and its cascading negative effects on Aesculus glabra. Plant Ecol 212:1193–1203. https://doi.org/10.1007/s11258-011-9897-z
Bell JL, Whitmore RC (1997) Eastern towhee numbers increase following defoliation by gypsy moths. Auk 114:708–716. https://doi.org/10.2307/4089290
Boege K (2005) Influence of plant ontogeny on compensation to leaf damage. Am J Bot 92:1632–1640. https://doi.org/10.3732/ajb.92.10.1632
Borchert R (1975) Endogenous shoot growth rhythms and indeterminate shoot growth in oak. Physiol Plant 35:152–157. https://doi.org/10.1111/j.1399-3054.1975.tb03885.x
Buck-Sorlin GH, Bell AD (2000) Models of crown architecture in Quercus petraea and Q. robur: shoot lengths and bud numbers. Forestry 73:1–19. https://doi.org/10.1093/forestry/73.1.1
Canham CD, Finzi AC, Pacala SW, Burbank DH (1994) Causes and consequences of resource heterogeneity in forests: interspecific variation in light transmission by canopy trees. Can J For Res 24:337–349. https://doi.org/10.1139/x94-046
Chaar H, Colin F, Collet C (1997) Effects of environmental factors on the shoot development of Quercus petraea seedlings: A methodological approach. For Ecol Manage 97:119–131. https://doi.org/10.1016/S0378-1127(97)00093-5
Chapin FS, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Ann Rev Ecol Syst 21:423–447. https://doi.org/10.1146/annurev.es.21.110190.002231
Cho DS, Boerner REJ (1991) Canopy disturbance patterns and regeneration of Quercus species in two Ohio old-growth forests. Vegetatio 93:9–18. https://doi.org/10.1007/BF00044920
Collins S (1961) Benefits to understory from canopy defoliation by gypsy moth larvae. Ecology 42:836–838. https://doi.org/10.2307/1933521
Cribari-Neto F, Zeileis A (2010) Beta regression in R. J Stat Softw 34(2):1–24. https://doi.org/10.18637/jss.v034.i02
de Beurs KM, Townsend PA (2008) Estimating the effect of gypsy moth defoliation using MODIS. Remote Sens Environ 112:3983–3990. https://doi.org/10.1016/j.rse.2008.07.008
Debussche M, Debussche G, Lepart J (2001) Changes in the vegetation of Quercus pubescens woodland after cessation of coppicing and grazing. J Veg Sci 12:81–92. https://doi.org/10.1111/j.1654-1103.2001.tb02619.x
Del Tredici P (2001) Sprouting in temperate trees: a morphological and ecological review. Bot Rev 67:121–140. https://doi.org/10.1007/BF02858075
Dobbertin M, Brang P (2001) Crown defoliation improves tree mortality models. For Ecol Manage 141:271–284. https://doi.org/10.1016/S0378-1127(00)00335-2
Embree DG (1967) Effects of the winter moth on growth and mortality of red oak in Nova Scotia. For Sci 13:295–299
Eschtruth AK, Battles JJ (2014) Ephemeral disturbances have long-lasting impacts on forest invasion dynamics. Ecology 95:1770–1779. https://doi.org/10.1890/13-1980.1
Fajvan MA, Rentch J, Gottschalk K (2008) The effects of thinning and gypsy moth defoliation on wood volume growth in oaks. Trees 22:257–268. https://doi.org/10.1007/s00468-007-0183-6
Ferrari SLP, Cribari-Neto F (2004) Beta regression for modelling rates and proportions. J Appl Stat 31:799–815. https://doi.org/10.1080/0266476042000214501
Furuno T (1964) On the feeding quantity of the gypsy moth (Lymantria dispar LINNE) and the camphor silk moth (Dictyoploca japonica BUTLER). J Jpn For Soc 46:14–19 (in Japanese with English summary)
Gottschalk KW (1993) Silvicultural guidelines for forest stands threatened by the gypsy moth. General technical report NE-221. USDA Forest Service, Northeastern Forest Experiment Station, Radnor
Gottschalk KW, Colbert JJ, Feicht DL (1998) Tree mortality risk of oak due to gypsy moth. Eur J For Path 28:121–132. https://doi.org/10.1111/j.1439-0329.1998.tb01173.x
Grace JR (1986) The influence of gypsy moth on the composition and nutrient content of litter fall in a Pennsylvania oak forest. For Sci 32:855–870
Gregory RA, Wargo PM (1986) Timing of defoliation and its effect on bud development, starch reserves, and sap sugar concentration in sugar maple. Can J For Res 16:10–17. https://doi.org/10.1139/x86-003
Hanson PJ, Dickson RE, Isebrands JG, Crow TR, Dixon RK (1986) A morphological index of Quercus seedling ontogeny for use in studies of physiology and growth. Tree Physiol 2:273–281. https://doi.org/10.1093/treephys/2.1-2-3.273
Hashizume H (1979) Characteristics of growth of Buna (Fagus crenata) seedlings and nursery practice. Bull Tottori Univ For 11:55–69 (in Japanese with English summary)
Heichel GH, Turner NC (1976) Phenology and leaf growth of defoliated hardwood trees. In: Anderson JF, Kaya HK (eds) Perspectives in forest entomology. Academic Press, New York, pp 31–40
Heichel GH, Turner NC (1983) CO2 assimilation of primary and regrowth foliage of red maple (Acer rubrum L.) and red oak (Quercus rubra L.): response to defoliation. Oecologia 57:14–19. https://doi.org/10.1007/BF00379555
Hikosaka K, Takashima T, Kabeya D, Hirose T, Kamata N (2005) Biomass allocation and leaf chemical defence in defoliated seedlings of Quercus serrata with respect to carbon–nitrogen balance. Ann Bot 95:1025–1032. https://doi.org/10.1093/aob/mci111
Hilton GM, Packham JR, Willis AJ (1987) Effects of experimental defoliation on a population of pedunculate oak (Quercus robur L.). New Phytol 107:603–612. https://doi.org/10.1111/j.1469-8137.1987.tb02930.x
Hoogesteger J, Karlsson PS (1992) Effects of defoliation on radial stem growth and photosynthesis in the mountain birch (Betula pubescens ssp. tortuosa). Func Ecol 6:317–323. https://doi.org/10.2307/2389523
Hunter MD (1987) Opposing effects of spring defoliation on late season oak caterpillars. Ecol Entomol 12:373–382. https://doi.org/10.1111/j.1365-2311.1987.tb01018.x
Hurley A, Watts D, Burke B, Richards C (2004) Identifying gypsy moth defoliation in Ohio using Landsat data. Environ Eng Geosci 10:321–328. https://doi.org/10.2113/10.4.321
Iwasa Y, Kubo T (1997) Optimal size of storage for recovery after unpredictable disturbances. Evol Ecol 11:41–65. https://doi.org/10.1023/A:1018483429029
Jedlicka J, Vandermeer J, Aviles-Vazquez K, Barros O, Perfecto I (2004) Gypsy moth defoliation of oak trees and a positive response of red maple and black cherry: an example of indirect interaction. Am Midl Nat 152:231–236. https://doi.org/10.1674/0003-0031(2004)152[0231:GMDOOT]2.0.CO;2
Kaitaniemi P, Neuvonen S, Nyyssönen T (1999) Effects of cumulative defoliations on growth, reproduction, and insect resistance in mountain birch. Ecology 80:524–532. https://doi.org/10.1890/0012-9658(1999)080[0524:EOCDOG]2.0.CO;2
Kamata N (2002) Outbreaks of forest defoliating insects in Japan, 1950–2000. Bull Entomol Res 92:109–117. https://doi.org/10.1079/BER2002159
Kikuzawa K (1983) Leaf survival of woody plants in deciduous broad-leaved forests. 1. Tall trees. Can J Bot 61:2133–2139. https://doi.org/10.1139/b83-230
Koike T (1988) Leaf structure and photosynthetic performance as related to the forest succession of deciduous broad-leaved trees. Plant Spec Biol 3:77–87. https://doi.org/10.1111/j.1442-1984.1988.tb00173.x
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
Kulman HM (1971) Effects of insect defoliation on growth and mortality of trees. Ann Rev Entomol 16:289–324. https://doi.org/10.1146/annurev.en.16.010171.001445
Långström B, Annila E, Hellqvist C, Varama M, Niemelä P (2001) Tree mortality, needle biomass recovery and growth losses in Scots pine following defoliation by Diprion pini (L.) and subsequent attack by Tomicus piniperda (L.). Scand J For Res 16:342–353. https://doi.org/10.1080/02827580118325
Liebhold AM, Gottschalk KW, Muzika R, Montgomery ME, Young R, O’Day K, Kelley B (1995) Suitability of North American tree species to the gypsy moth: a summary of field and laboratory tests. General technical report NE-221. USDA Forest Service, Northeastern Forest Experiment Station, Radnor
Logan JA, Régnière J, Powell JA (2003) Assessing the impacts of global warming on forest pest dynamics. Front Ecol Environ 1:130–137. https://doi.org/10.1890/1540-9295(2003)001[0130:ATIOGW]2.0.CO;2
Masaki T, Suzuki W, Niiyama K, Iida S, Tanaka H, Nakashizuka T (1992) Community structure of a species-rich temperate forest, Ogawa Forest Reserve, central Japan. Vegetatio 98:97–111. https://doi.org/10.1007/BF00045549
Mikan CJ, Orwig DA, Abrams MD (1994) Age structure and successional dynamics of a presettlement-origin chestnut oak forest in the Pennsylvania Piedmont. Bull Tor Bot Club 121:13–23. https://doi.org/10.2307/2996880
Miquelle DG (1983) Browse regrowth and consumption following summer defoliation by moose. J Wildl Manage 47:17–24. https://doi.org/10.2307/3808047
Mizumachi E, Osawa N, Akiyama R, Tokuchi N (2004) The effects of herbivory and soil fertility on the growth patterns of Quercus serrata and Q. crispula saplings at the shoot and individual levels. Popul Ecol 46:203–211. https://doi.org/10.1007/s10144-004-0188-6
Muzika RM, Liebhold AM (1999) Changes in radial increment of host and nonhost tree species with gypsy moth defoliation. Can J For Res 29:1365–1373. https://doi.org/10.1139/x99-098
Nakajima H (2015a) Defoliation by gypsy moths negatively affects the production of acorns by two Japanese oak species. Trees 29:1559–1566. https://doi.org/10.1007/s00468-015-1237-9
Nakajima H (2015b) Estimating sound seedfall density of Fagus crenata using a visual survey. J For Res 20:94–103. https://doi.org/10.1007/s10310-014-0440-7
Nakajima H, Ishida M (2014) Decline of Quercus crispula in abandoned coppice forests caused by secondary succession and Japanese oak wilt disease: stand dynamics over twenty years. For Ecol Manage 334:18–27. https://doi.org/10.1016/j.foreco.2014.08.021
Nakajima H, Kume A, Ishida M, Ohmiya T, Mizoue N (2011) Evaluation of estimates of crown condition in forest monitoring: comparison between visual estimation and automated crown image analysis. Ann For Sci 68:1333–1340. https://doi.org/10.1007/s13595-011-0132-9
Nakamura M, Kagata H, Ohgushi T (2006) Trunk cutting initiates bottom-up cascades in a tri-trophic system: sprouting increases biodiversity of herbivorous and predaceous arthropods on willows. Oikos 113:259–268. https://doi.org/10.1111/j.2006.0030-1299.14251.x
Namikawa K, Ishikawa Y, Sano J (1997) Stand dynamics during a 12-year period in a second-growth stand in a cool temperature forest in northern Japan. Ecol Res 12:277–287. https://doi.org/10.1007/BF02529457
Neuvonen S, Hanhimak S, Suomela J, Haukioja E (1988) Early season damage to birch foliage affects the performance of a late season herbivore. J Appl Entomol 105:182–189. https://doi.org/10.1111/j.1439-0418.1988.tb00174.x
Ohno Y, Umeki K, Watanabe I, Takiya M, Terazawa K, Hara H, Matsuki S (2008) Variation in shoot mortality within crowns of severely defoliated Betula maximowicziana trees in Hokkaido, northern Japan. Ecol Res 23:355–362. https://doi.org/10.1007/s11284-007-0386-8
Onodera K, Hara H (2011) Suitability of plant species as food for Asian gypsy moth larvae of the Hokkaido population. Bull Hokkaido For Res Inst 48:47–54 (in Japanese with English summary)
Palacio S, Hernández R, Maestro–Martínez M, Camarero JJ (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 26:1627–1640. https://doi.org/10.1007/s00468-012-0739-y
Piper FI, Fajardo A (2014) Foliar habit, tolerance to defoliation and their link to carbon and nitrogen storage. J Ecol 102:1101–1111. https://doi.org/10.1111/1365-2745.12284
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
Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251. https://doi.org/10.2307/3545270
R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reich PB, Teskey RO, Johnson PS, Hinckley TM (1980) Periodic root and shoot growth in oak. For Sci 26:590–598
Rooke T, Bergström R (2007) Growth, chemical responses and herbivory after simulated leaf browsing in Combretum apiculatum. Plant Ecol 189:201–212. https://doi.org/10.1007/s11258-006-9177-5
Rozenbergar D, Diaci J (2014) Architecture of Fagus sylvatica regeneration improves over time in mixed old-growth and managed forests. For Ecol Manage 318:334–340. https://doi.org/10.1016/j.foreco.2014.01.037
Rozendaal DMA, Kobe RK (2014) Competitive balance among tree species altered by forest tent caterpillar defoliation. For Ecol Manage 327:18–25. https://doi.org/10.1016/j.foreco.2014.04.037
Saitoh T, Vik JO, Stenseth NC, Takanishi T, Hayakashi S, Ishida N, Ohmori M, Morita T, Uemura S, Kadomatsu M, Osawa J, Maekawa K (2008) Effects of acorns abundance on density dependence in a Japanese wood mice (Apodemus speciosus) population. Popul Ecol 50:159–167. https://doi.org/10.1007/s10144-008-0076-6
Sakai A, Sakai S, Akiyama F (1997) Do sprouting tree species on erosion-prone sites carry large reserves of resources? Ann Bot 79:625–630. https://doi.org/10.1006/anbo.1996.0389
Schowalter TD, Hargrove WW, Crossley DA (1986) Herbivory in forested ecosystems. Ann Rev Entomol 31:177–196. https://doi.org/10.1146/annurev.en.31.010186.001141
Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151. https://doi.org/10.1126/science.217.4555.149
Seiwa K, Kikuzawa K (1991) Phenology of tree seedlings in relation to seed size. Can J Bot 69:532–538. https://doi.org/10.1139/b91-072
Shibata R, Shibata M, Tanaka H, Iida S, Masaki T, Hatta F, Kurokawa H, Nakashizuka T (2014) Interspecific variation in the size-dependent resprouting ability of temperate woody species and its adaptive significance. J Ecol 102:209–220. https://doi.org/10.1111/1365-2745.12174
Smithson M, Verkuilen J (2006) A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychol Methods 11:54–71. https://doi.org/10.1037/1082-989X.11.1.54
Takahashi K, Goto A (2012) Morphological and physiological responses of beech and oak seedlings to canopy conditions: why does beech dominate the understory of unmanaged oak fuelwood stands? Can J For Res 42:1623–1630. https://doi.org/10.1139/x2012-097
Valladares F, Chico J, Aranda I, Balaguer L, Dizengremel P, Manrique E, Dreyer E (2002) The greater seedling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. Trees 16:395–403. https://doi.org/10.1007/s00468-002-0184-4
van der Heyden F, Stock WD (1996) Regrowth of a semiarid shrub following simulated browsing: the role of reserve carbon. Func Ecol 10:647–653. https://doi.org/10.2307/2390175
Wargo PM, Parker J, Houston DR (1972) Starch content in roots of defoliated sugar maple. For Sci 18:203–204
Welander NT, Ottosson B (1998) The influence of shading on growth and morphology in seedlings of Quercus robur L. and Fagus sylvatica L. For Ecol Manage 107:117–126. https://doi.org/10.1016/S0378-1127(97)00326-5
West C (1985) Factors underlying the late seasonal appearance of the lepidopterous leaf-mining guild on oak. Ecol Entomol 10:111–120. https://doi.org/10.1111/j.1365-2311.1985.tb00540.x
Williams DW, Fuester RW, Metterhouse WW, Balaam RJ, Bullock RH, Chianese RJ (1991) Oak defoliation and population density relationships for the gypsy moth (Lepidoptera: Lymantriidae). J Econ Entomol 84:1508–1514. https://doi.org/10.1093/jee/84.5.1508
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I am grateful to my colleagues at Toyama Prefectural Government for their helpful support. This study was funded by Toyama Prefecture, Japan.
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Communicated by William E. Rogers.
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Nakajima, H. Refoliation of deciduous canopy trees following severe insect defoliation: comparison of Fagus crenata and Quercus crispula. Plant Ecol 219, 665–675 (2018). https://doi.org/10.1007/s11258-018-0825-3
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DOI: https://doi.org/10.1007/s11258-018-0825-3