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Defoliation by gypsy moths negatively affects the production of acorns by two Japanese oak species

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This study showed the negative effects of insect defoliation on the reproduction of canopy trees, where defoliation was not artificially manipulated but rather observed in a natural setting.

Abstract

The gypsy moth (Lymantria diapar) is a serious defoliator with the ability to completely defoliate forest canopies. Although the negative effects of defoliation on tree reproduction have been revealed in studies with artificially manipulated defoliation, few studies have examined the effect of insect defoliation on the reproduction of canopy trees under natural condition. In this study, visual surveys were used to clarify the effect of gypsy moth defoliation on the production of acorns by oaks (Quercus spp.). Surveys were conducted in an outbreak year at 22 sites in central Japan (13 sites with Quercus crispula and nine sites with Q. serrata). Five of the Q. crispula sites were severely defoliated (mean defoliation ranged from 67 to 88 %), while the remainder of the Q. crispula sites and all of the Q. serrata sites were lightly defoliated (0–20 %). A negative effect of gypsy moth defoliation on acorn production was detected for Q. crispula. However, there was a synchronous decrease in acorn production from the previous year and crop levels were low at all sites regardless of the defoliation severity. The consistent low crop levels were likely the result of weather-related factors. Defoliation also negatively affected the production of acorns for Q. serrata; however, severe defoliation was not present at any Q. serrata sites. This study suggests that insect defoliation can affect forest ecosystem processes, such as the regeneration of host trees and the behavior of wildlife that depend on seed production, by reducing the reproductive potential of host trees.

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References

  • Akasofu Y (1973) Extraordinary outbreak of gypsy moth in Takaoka City. For Pests 22:214–217 (in Japanese)

    Google Scholar 

  • Alalouni U, Schädler M, Brandl R (2013) Natural enemies and environmental factors affecting the population dynamics of the gypsy moth. J Appl Entomol 137:721–738. doi:10.1111/jen.12072

    Article  Google Scholar 

  • Aoki J (1974) Mixed infection of the gypsy moth, Lymantria dispar japonica MOTSCHULSKY (Lepidoptera: Lymantriidae), in a larch forest by Entomophthora aulicae (REICH.) SOROK. and Paecilomyces canadensis (VUILL.) BROWN et SMITH. Appl Entomol Zool 9:185–190. doi:10.1303/aez.9.185

    Google Scholar 

  • 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. doi:10.1007/s13355-013-0235-x

    Article  CAS  Google Scholar 

  • Baker WL (1941) Effect of gypsy moth defoliation on certain forest trees. J Forestry 39:1017–1022

    Google Scholar 

  • Bell JL, Whitmore RC (1997) Eastern towhee numbers increase following defoliation by gypsy moths. Auk 114:708–716. doi:10.2307/4089290

    Article  Google Scholar 

  • Campbell RW, Sloan RJ (1977) Forest stand responses to defoliation by the gypsy moth. For Sci Monogr 19:1–34

    Google Scholar 

  • Collins S (1961) Benefits to understory from canopy defoliation by gypsy moth larvae. Ecology 42:836–838. doi:10.2307/1933521

    Article  Google Scholar 

  • Crawley MJ (1985) Reduction of oak fecundity by low-density herbivore populations. Nature 314:163–164. doi:10.1038/314163a0

    Article  Google Scholar 

  • de Beurs KM, Townsend PA (2008) Estimating the effect of gypsy moth defoliation using MODIS. Remote Sens Environ 112:3983–3990. doi:10.1016/j.rse.2008.07.008

    Article  Google Scholar 

  • Eisenbies MH, Davidson C, Johnson J, Amateis R, Gottschalk K (2007) Tree mortality in mixed pine–hardwood stands defoliated by the European gypsy moth (Lymantria dispar L.). For Sci 53:683–691

    Google Scholar 

  • Eschtruth AK, Battles JJ (2014) Ephemeral disturbances have long-lasting impacts on forest invasion dynamics. Ecology 95:1770–1779. doi:10.1890/13-1980.1

    Article  PubMed  Google Scholar 

  • Fajvan MA, Wood JM (1996) Stand structure and development after gypsy moth defoliation in the Appalachian Plateau. For Ecol Manage 89:79–88. doi:10.1016/S0378-1127(96)03865-0

    Article  Google Scholar 

  • 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. doi:10.1007/s00468-007-0183-6

    Article  Google Scholar 

  • Fukumoto H, Kajimura H (2011) Effects of asynchronous acorn production by co-occurring Quercus trees on resource utilization by acorn-feeding insects. J For Res 16:62–67. doi:10.1007/s10310-010-0208-7

    Article  Google Scholar 

  • Fukuyama K, Yamaguchi H, Koizumi C (1990) Comparative analysis of mortality factors of artificial larval populations of the gypsy moth, Lymantria dispar (Lepidotera: Lymantriidae) in Hokkaido: I. Mortality factors in five different types of forests. Appl Entomol Zool 25:205–213. doi:10.1303/aez.25.205

    Google Scholar 

  • 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)

    Google Scholar 

  • Furuta K (1982) Natural control of Lymantria dispar L. (Lep., Lymantriidae) population at low density levels in Hokkaido (Japan). Zeitschrift für Angewandte Entomologie 93:513–522. doi:10.1111/j.1439-0418.1982.tb03629.x

    Article  Google Scholar 

  • Gandhi KJK, Herms DA (2010) Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol Invasions 12:389–405. doi:10.1007/s10530-009-9627-9

    Article  Google Scholar 

  • Gottschalk KW (1990) Gypsy moth effects on mast production. In: McGee CE (ed) Proceedings of the workshop: Southern Appalachian mast management. Knoxville, Tennessee, pp 42–50

    Google Scholar 

  • Gottschalk KW, Colbert JJ, Feicht DL (1998) Tree mortality risk of oak due to gypsy moth. Eur J For Path 28:121–132. doi:10.1111/j.1439-0329.1998.tb01173.x

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Haynes KJ, Liebhold AM, Johnson DM (2012) Elevational gradient in the cyclicity of a forest-defoliating insect. Popul Ecol 54:239–250. doi:10.1007/s10144-012-0305-x

    Article  Google Scholar 

  • Higashiura Y (1980) Analysis of factors affecting bird predation on gypsy moth egg masses by using Holling’s disc-quation. Res Popul Ecol 22:147–162. doi:10.1007/BF02513542

    Article  Google Scholar 

  • Higashiura Y (1987) Larval densities and a life-table for the gypsy moth, Lymantria dispar, estimated using the head-capsule collection method. Ecol Entomol 12:25–30. doi:10.1111/j.1365-2311.1987.tb00981.x

    Article  Google Scholar 

  • Higashiura Y, Yamaguchi H, Ishihara M, Ono N, Tsukagoshi H, Yokobori S, Tokishita S, Yamagata H, Fukatsu T (2011) Male death resulting from hybridization between subspecies of the gypsy moth, Lymantria dispar. Heredity 106:603–613. doi:10.1038/hdy.2010.92

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hoch G (2005) Fruit-bearing branchlets are carbon autonomous in mature broad-leaved temperate forest trees. Plant Cell Environ 28:651–659. doi:10.1111/j.1365-3040.2004.01311.x

    Article  CAS  Google Scholar 

  • Hoch G, Siegwolf RW, Keel SG, Körner C, Han Q (2013) Fruit production in three masting tree species does not rely on stored carbon reserves. Oecologia 171:653–662. doi:10.1007/s00442-012-2579-2

    Article  PubMed  Google Scholar 

  • Ichie T, Igarashi S, Yoshida S, Kenzo T, Masaki T, Tayasu I (2013) Are stored carbohydrates necessary for seed production in temperate deciduous trees? J Ecol 101:525–531. doi:10.1111/1365-2745.12038

    Article  CAS  Google Scholar 

  • Imada M, Nakai T, Nakamura T, Mabuchi T, Takahashi Y (1990) Acorn dispersal in natural stands of Mizunara (Quercus mongolica var. grosseserrata) for twenty years. J Jpn For Soc 72:426–430

    Google Scholar 

  • Ishihama N, Yasaka M, Ohno Y, Hasui S, Nakagawa M, Takiya M (2011) Damage by outbreaks of gypsy moth in newly planted larch species plantations at Higashikagura, central Hokkaido. Trans Mtg Hokkaido Br Jpn For Soc 59:59–62 (in Japanese)

    Google Scholar 

  • Janzen DH (1976) Effect of defoliation on fruit-bearing branches of the Kentucky coffee tree, Gymnoclaudus dioicus (Leguminosae). Am Midl Nat 95:474–478. doi:10.2307/2424414

    Article  Google Scholar 

  • 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. doi:10.1674/0003-0031(2004)152[0231:GMDOOT]2.0.CO;2

  • Jikumaru S, Sano T (2007) Distribution of late instar Lymantria dispar cadavers killed by Entomophaga maimaiga on trunks of several tree species in southwestern Japan. Can J Bot 85:25–30. doi:10.1139/b06-146

    Article  Google Scholar 

  • Kaitaniemi P, Neuvonen S, Nyyssönen T (1999) Effects of cumulative defoliations on growth, reproduction, and insect resistance in mountain birch. Ecology 80:524–532. doi: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. doi:10.1079/BER2002159

    CAS  PubMed  Google Scholar 

  • Kasbohm JW (1994) Response of black bears to gypsy moth infestation in Shenandoah National Park, Virginia. PhD thesis, Virginia Polytechnic Institute and State University, Blacksburg, Virginia

  • Kasbohm JW, Kraus JG, Vaughan MR (1995) Food habits and nutrition of black bears during a gypsy moth infestation. Can J Zool 73:1771–1775. doi:10.1139/z95-208

    Article  Google Scholar 

  • Kasbohm JW, Vaughan MR, Kraus JG (1998) Black bear home range dynamics and movement patterns during a gypsy moth infestation. Ursus 10:259–267

    Google Scholar 

  • Koenig WD, Knops JMH (2013) Large-scale spatial synchrony and cross-synchrony in acorn production by two California oaks. Ecology 94:83–93. doi:10.1890/12-0940.1

    Article  PubMed  Google Scholar 

  • Koenig WD, Knops JMH (2014) Environmental correlates of acorn production by four species of Minnesota oaks. Popul Ecol 56:63–71. doi:10.1007/s10144-013-0408-z

    Article  Google Scholar 

  • Koenig WD, Knops JMH, Carmen WJ, Stanback MT, Mumme RL (1994) Estimating acorn crops using visual surveys. Can J For Res 24:2105–2112. doi:10.1139/x94-270

    Article  Google Scholar 

  • 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. doi:10.1007/s004420100694

    Article  Google Scholar 

  • Koyama R (1954) Two epizootic diseases of gypsy moth. For Pests 3:296–298 (in Japanese)

    Google Scholar 

  • Kozakai C, Yamazaki K, Nemoto Y, Nakajima A, Koike S, Abe S, Masaki T, Kaji K (2011) Effect of mast production on home range use of Japanese black bears. J Wildl Manage 75:867–875. doi:10.1002/jwmg.122

    Article  Google Scholar 

  • Kulman HM (1971) Effects of insect defoliation on growth and mortality of trees. Ann Rev Entomol 16:289–324. doi:10.1146/annurev.en.16.010171.001445

    Article  Google Scholar 

  • Lesnoff M, Lancelot R (2012) aod: Analysis of overdispersed data. R package version 1.3. http://cran.r-project.org/package=aod

  • 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

  • Liebhold AM, Higashiura Y, Unno A (1998) Forest type affects predation on gypsy moth (Lepidoptera: Lymantriidae) pupae in Japan. Environ Entomol 27:858–862. doi:10.1093/ee/27.4.858

    Article  Google Scholar 

  • Liebhold A, Elkinton J, Williams D, Muzika RM (2000) What causes outbreaks of the gypsy moth in North America? Popul Ecol 42:257–266. doi:10.1007/PL00012004

    Article  Google Scholar 

  • Liebhold AM, Turcáni M, Kamata N (2008) Inference of adult female dispersal from the distribution of gypsy moth egg masses in a Japanese city. Agric For Entomol 10:69–73. doi:10.1111/j.1461-9563.2007.00359.x

    Article  Google Scholar 

  • Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD (2006) Forest ecosystem responses to exotic pests and pathogens in eastern north America. Bioscience 56:395–405. doi:10.1641/0006-3568(2006)056[0395:FERTEP]2.0.CO;2

  • Maeto K, Ozaki K (2003) Prolonged diapause of specialist seed-feeders makes predator satiation unstable in masting of Quercus crispula. Oecologia 137:392–398. doi:10.1007/s00442-003-1381-6

    Article  PubMed  Google Scholar 

  • Marquis RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226:537–539. doi:10.1126/science.226.4674.537

    Article  CAS  PubMed  Google Scholar 

  • Massad TJ (2013) Ontogenetic differences of herbivory on woody and herbaceous plants: a meta-analysis demonstrating unique effects of herbivory on the young and the old, the slow and the fast. Oecologia 172:1–10. doi:10.1007/s00442-012-2470-1

    Article  PubMed  Google Scholar 

  • May JD, Killingbeck KT (1995) Effects of herbivore-induced nutrient stress on correlates of fitness and on nutrient resorption in scrub oak (Quercus ilicifolia). Can J For Res 25:1858–1864. doi:10.1139/x95-200

    Article  Google Scholar 

  • Mizui N (1991) Classification of seed production based on the correlation between seed-weight and seed-number in deciduous broadleaved tree species. J Jpn For Soc 73:258–263 (in Japanese with English summary)

    Google Scholar 

  • Mizutani M (2014) Gypsy moth outbreaks and their impacts on acorn production of Quercus crispula in Fukui Prefecture in 2013. Chubu For Res 62:63–66 (in Japanese)

    Google Scholar 

  • Mizutani M, Nakajima H, Kodani J, Nogami T, Tada M (2013) Relationship between the acorn crops of Fagaceae trees and the mass intrusions of bears into residential areas in the Hokuriku region. J Jpn For Soc 95:76–82. doi:10.4005/jjfs.95.76 (in Japanese with English summary)

  • Morris WF, Hufbauer RA, Agrawal AA, Bever JD, Borowicz VA, Gilbert GS, Maron JL, Mitchell CE, Parker IM, Power AG, Torchin ME, Vázquez DP (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029. doi:10.1890/06-0442

    Article  PubMed  Google Scholar 

  • 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. doi:10.1139/x99-098

    Article  Google Scholar 

  • Naidoo R, Lechowicz MJ (2001) Effects of gypsy moth on radial growth of deciduous trees. For Sci 47:338–348

    Google Scholar 

  • Nakajima H (2013) Estimation of beech (Fagus crenata) seed crops from female inflorescence scars: Relationship between seed crops and degree of intrusion into residential areas by Asiatic black bears in Toyama Prefecture, Japan. J Jpn For Soc 95:71–75. doi:10.4005/jjfs.95.71 (in Japanese with English summary)

  • Nakajima H (2015) Estimating sound seedfall density of Fagus crenata using a visual survey. J For Res 20:94–103. doi:10.1007/s10310-014-0440-7

    Article  Google Scholar 

  • 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. doi:10.1016/j.foreco.2014.08.021

    Article  Google Scholar 

  • 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. doi:10.1007/s13595-011-0132-9

    Article  Google Scholar 

  • Obeso JR (1993) Does defoliation affect reproductive output in herbaceous perennials and woody plants in different ways? Func Ecol 7:150–155. doi:10.2307/2389881

    Article  Google Scholar 

  • Obeso JR (1998) Effects of defoliation and girdling on fruit production in Ilex aquifolium. Func Ecol 12:486–491. doi:10.1046/j.1365-2435.1998.00216.x

    Article  Google Scholar 

  • Oka T, Miura S, Masaki T, Suzuki W, Osumi K, Saitoh S (2004) Relationship between changes in beechnut production and Asiatic black bears in northern Japan. J Wildl Manage 68:979–986. doi:10.2193/0022-541X(2004)068[0979:RBCIBP]2.0.CO;2

  • 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)

    Google Scholar 

  • 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. doi:10.1007/s00468-012-0739-y

    Article  Google Scholar 

  • Piper FI, Fajardo A (2014) Foliar habit, tolerance to defoliation and their link to carbon and nitrogen storage. J Ecol 102:1101–1111. doi:10.1111/1365-2745.12284

    Article  CAS  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rieske LK, Dillaway DN (2008) Response of two oak species to extensive defoliation: Tree growth and vigor, phytochemistry, and herbivore suitability. For Ecol Manage 256:121–128. doi:10.1016/j.foreco.2008.04.015

    Article  Google Scholar 

  • Rockwood LL (1973) The effect of defoliation on seed production of six Costa Rican tree species. Ecology 54:1363–1369. doi:10.2307/1934200

    Article  Google Scholar 

  • 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. doi:10.1007/s10144-008-0076-6

    Article  Google Scholar 

  • Salleo S, Nardini A, Raimondo F, Gullo MAL, 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. doi:10.1007/s00468-003-0247-1

    Google Scholar 

  • Schowalter TD, Hargrove WW, Crossley DA (1986) Herbivory in forested ecosystems. Ann Rev Entomol 31:177–196. doi:10.1146/annurev.en.31.010186.001141

    Article  Google Scholar 

  • Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151. doi:10.1126/science.217.4555.149

    Article  CAS  PubMed  Google Scholar 

  • Shibata M, Tanaka H, Iida S, Abe S, Masaki T, Niiyama K, Nakashizuka T (2002) Synchronized annual seed production by 16 principal tree species in a temperate deciduous forest, Japan. Ecology 83:1727–1742. doi:10.1890/0012-9658(2002)083[1727:SASPBP]2.0.CO;2

  • Stephenson AG (1980) Fruit set, herbivory, fruit reduction, and the fruiting strategy of Catalpa speciosa (Bignoniaceae). Ecology 61:57–64. doi:10.2307/1937155

    Article  Google Scholar 

  • Wargo PM (1972) Defoliation-induced chemical changes in sugar maple roots stimulate growth of Armillaria mellea. Phytopathology 62:1278–1283. doi:10.1094/Phyto-62-1278

    Article  CAS  Google Scholar 

  • Wargo PM, Parker J, Houston DR (1972) Starch content in roots of defoliated sugar maple. For Sci 18:203–204

    Google Scholar 

  • Wesołowski T, Rowiński P, Maziarz M (2015) Interannual variation in tree seed production in a primeval temperate forest: does masting prevail? Eur J For Res 134:99–112. doi:10.1007/s10342-014-0836-0

    Article  Google Scholar 

  • 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. doi:10.1093/jee/84.5.1508

    Article  Google Scholar 

  • Yasaka M, Takiya M, Watanabe I, Oono Y, Mizui N (2008) Variation in seed production among years and among individuals in 11 broadleaf tree species in northern Japan. J For Res 13:83–88. doi:10.1007/s10310-007-0052-6

    Article  Google Scholar 

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Acknowledgments

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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Correspondence to Haruki Nakajima.

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Communicated by T. Koike.

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Nakajima, H. Defoliation by gypsy moths negatively affects the production of acorns by two Japanese oak species. Trees 29, 1559–1566 (2015). https://doi.org/10.1007/s00468-015-1237-9

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