Plant Protect. Sci., 2018, 54(4):272-283 | DOI: 10.17221/11/2018-PPS

Can late flushing trees avoid attack by moth larvae in temperate forests?Original Paper

Ján Kulfan1, Lenka Sarvašová1, 2, *, Michal Parák1, Marek Dzurenko1, 2, Peter Zach1
1 Institute of Forest Ecology, Slovak Academy of Sciences, Zvolen, Slovak Republic
2 Faculty of Ecology and Environmental Sciences, Technical University in Zvolen, Zvolen, Slovak Republic

We investigated moth larvae (Lepidoptera) developing in temperate forests in Central Europe shortly after the tree budburst (the "brumata-viridana complex"). Larvae were collected in southern Slovakia in May 2015 and May 2016 from young and mature trees of late flushing Quercus cerris L. and early flushing Q. pubescens Willd. Although Q. cerris yielded fewer species (40 species) than Q. pubescens (47 species), the rarefied number of species and the Chao index suggested a similar number of species on mature trees of both oak species. Both the total number of moth larvae in assemblages and the abundance of dominant species (pests) were significantly lower on Q. cerris than Q. pubescens. The results suggest the release of Q. cerris with delayed budburst from heavy infestations by folivorous moth larvae. Knowledge obtained can be applied in silvicultural and horticultural practices aimed to protect and maintain forest, fruit, and ornamental trees.

Keywords: Quercus cerris; Quercus pubescens; folivorous insects; Lepidoptera; phenology; budburst

Published: December 31, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Kulfan J, Sarvašová L, Parák M, Dzurenko M, Zach P. Can late flushing trees avoid attack by moth larvae in temperate forests? Plant Protect. Sci. 2018;54(4):272-283. doi: 10.17221/11/2018-PPS.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Abarca M., Boege K., Zaldívar-Riverón A., Giray T. (2014): Shelter-building behavior and natural history of two pyralid caterpillars feeding on Piper stipulaceum. Journal of Insect Science, 14: 39. doi: 10.1093/jis/14.1.39 Go to original source... Go to PubMed...
    2. Ahola M., Silvonen K. (2005): Pohjoisen Euroopan yökkösten toukat. Volume 1. Vaasa, KuvaSeppälä Yhtiöt Oy.
    3. Anderson M.J. (2001): A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26: 32-46. Go to original source...
    4. Basset Y., Springate N.D., Aberlenc H.P., Delvare G. (1997): A review of methods for sampling arthropods in tree canopies. In: Stork N.E., Adis J., Didham R.K. (eds): Canopy Arthropods. London, Chapman & Hall: 27-52.
    5. Bray J.R., Curtis J.T. (1957): An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs, 27: 325-349. Go to original source...
    6. Buck N., Callaghan T.V. (1999): The direct and indirect effects of enhanced UV-B on the moth caterpillar Epirrita autumnata. Ecological Bulletins, 47: 68-76.
    7. Canty A., Ripley B. (2016): boot: Bootstrap R (S-Plus) Functions. R package version 1.3-18. Go to original source...
    8. Chiu C.H., Wang Y.T., Walther B.A., Chao A. (2014): An improved nonparametric lower bound of species richness via a modified good-turing frequency formula. Biometrics, 70: 671-682. Go to original source... Go to PubMed...
    9. Csóka G., Szabóky C. (2005): Checklist of herbivorous insects of native and exotic oaks in Hungary I. (Lepidoptera). Acta Silvatica et Lignaria Hungarica, 1: 59-72. Go to original source...
    10. Cuming F.G. (1961): The distribution, life history, and economic importance of the winter moth, Operophtera brumata (L.) (Lepidoptera,Geometridae) in Nova Scotia. The Canadian Entomologist, 93: 135-142. Go to original source...
    11. Damman H. (1987): Leaf quality and enemy avoidance by the larvae of a pyralid moth. Ecology, 68: 88-97. Go to original source...
    12. De Cáceres M., Legendre P. (2009): Associations between species and groups of sites: indices and statistical inference. Ecology, 90: 3566-3574. Go to original source... Go to PubMed...
    13. De Vries H.H., Ens S.H., de Graaf G., Teunissen L., van der Velde R., Vogelaar L., Winterink A., Visser M.E. (2011): Synchronisation of egg hatching of brown hairstreak (Thecla betulae) and budburst of blackthorn (Prunus spinosa) in a warmer future. Journal of Insect Conservation, 15: 311-319. Go to original source...
    14. Despland E. (2018): Effects of phenological synchronization on caterpillar early-instar survival under a changing climate. Canadian Journal of Forest Research, 48: 247-254. Go to original source...
    15. Du Merle P. (1983): Phénologies comparées du chêne pubescent, du chêne vert et de Tortrix viridana L. (Lep., Tortricidae). Mise en évidence chez l'insecte de deux populations sympatriques adaptées chacune à l'un des chênes. Acta Oecologica. Oecologia Applicata, 4: 55-74.
    16. Du Merle P. (1988): Phenological resistance of oaks to the green leafroller, Tortrix viridiana (Lepidoptera: Tortricidae). In: Mattson W.J., Levieux J., Bernard-Dagan C. (eds): Mechanisms of Woody Plant Defences against Insects. Berlin-Heidelberg-New York, Springer: 215-226. Go to original source...
    17. Du Merle P., Mazet R. (1983): Les facteurs de mortalité des oeufs de Tortrix viridana L. (Lep., Tortricidae). I. Le complexe des prédateurs (Hym., Formicidae; Derm., Forficulidae; Orth., Phaneropteridae; Neur., Chrysopidae). Agronomie, 3: 239-246. Go to original source...
    18. Dufrêne M., Legendre P. (1997): Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs, 67: 345-366. Go to original source...
    19. Ebert G., Steiner A., Trusch R. (2003): Ennominae (Geometridae). In: Ebert G. (ed.): Die Schmetterlinge BadenWürttembergs. Band 9 - Nachtfalter VII. Stuttgart, Ulmer: 294-579.
    20. Edland T. (1971): Wind dispersal of the winter moth larvae Operophtera brumata L. (Lep., Geometridae) and its relevance to control measures. Norsk Entomoligisk Tidsskrift, 18: 103-105.
    21. Edmunds G.F., Alstad D.N. (1978): Coevolution in insect herbivores and conifers. Science, 199 (4332): 941-945. Go to original source... Go to PubMed...
    22. Feeny P.P. (1968): Effect of oak leaf tannins on larval growth of the winter moth Operophtera brumata. Journal of Insect Physiology, 14: 805-817. Go to original source...
    23. Feeny P. (1970): Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology, 51: 565-581. https://doi.org/10.17221/11/2018-PPS Go to original source...
    24. Forkner R.E., Marquis R.J., Lill J.T., Le Corff J. (2008): Timing is everything? Phenological synchrony and population variability in leaf-chewing herbivores of Quercus. Ecological Entomology, 33: 276-285. Go to original source...
    25. Foster J.R., Townsend P.A., Mladenoff D.J. (2013): Mapping asynchrony between gypsy moth egg-hatch and forest leaf-out: Putting the phenological window hypothesis in a spatial context. Forest Ecology and Management, 287: 67-76. Go to original source...
    26. Führer E. (1998): Oak decline in Central Europe: a synopsis of hypothesis. In: McManus M.L., Liebhold A.M. (eds): Proceedings: Population dynamics, impacts, and integrated management of forest defoliating insects, Aug 18-23, 1996, Banská Štiavnica, Slovakia. Radnor, USDA Forest Service, Northeastern Research Station, General Technical Report NE-247: 7-24.
    27. Goater B., Ronkay L., Fibiger M. (2003): Noctuidae Europaeae, 10. Catocalinae & Plusiinae. Sorø, Entomological Press.
    28. Goliašová K., Michalková E. (2006): Flóra Slovenska V/3. Bratislava, VEDA.
    29. Graf B., Borer F., Höpli H.U., Hohn H., Dorn S. (1995): The winter moth Operophtera brumata L. (Lep., Geometridae) on apple and cherry: spatial and temporal aspects of recolonization in autumn. Journal of Applied Entomology, 119: 295-301. Go to original source...
    30. Grison P., Silvestre de Sacy R. (1954): Déplacement orienté de la femelle de cheimatobie (Operophtera brumata L.). Bulletin de la Societé Entomologique de France, 59: 151-154. Go to original source...
    31. Heck K.L., van Belle G., Simberloff D. (1975): Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology, 56: 1459-1461. Go to original source...
    32. Holliday N.J. (1977): Population ecology of winter moth (Operophtera brumata) on apple in relation to larval dispersal and time of bud burst. Journal of Applied Ecology, 14: 803-813. Go to original source...
    33. Holm S. (1979): A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6: 65-70.
    34. Hunter A.F., Elkinton J.S. (2000): Effects of synchrony with host plant on populations of a spring-feeding Lepidopteran. Ecology, 81: 1248-1261. Go to original source...
    35. Hunter A.F., Lechowicz M.J. (1992): Foliage quality changes during canopy development of some northern hardwood trees. Oecologia, 89: 316-323. Go to original source... Go to PubMed...
    36. Hunter M.D. (1990): Differential susceptibility to variable plant phenology and its role in competition between two insect herbivores on oak. Ecological Entomology, 15: 401-408. Go to original source...
    37. Hunter M.D. (1992): A variable insect-plant interaction: the relationship between tree budburst phenology and population levels of insect herbivores among trees. Ecological Entomology, 16: 91-95. Go to original source...
    38. Hurlbert S.H. (1971): The nonconcept of species diversity: a critique and alternative parameters. Ecology, 52: 577-586. Go to original source... Go to PubMed...
    39. Ivashov A.V., Boyko G.E., Simchuk A.P. (2002): The role of host plant phenology in the development of the oak leafroller moth, Tortrix viridana L. (Lepidoptera: Tortricidae). Forest Ecology and Management, 157: 7-14. Go to original source...
    40. Jones B.C., Despland E. (2006): Effects of synchronization with host plant phenology occur early in the larval development of a spring folivore. Canadian Journal of Zoology, 84: 628-633. Go to original source...
    41. Kabíček J. (2017): Phytoseiid mites on Quercus cerris in an urban park. Plant Protection Science, 53: 181-186. Go to original source...
    42. Kamata N., Igarashi Y. (1994): Influence of rainfall on feeding behavior, growth, and mortality of larvae of the beech caterpillar, Quadricalcarifera punctatella (Motschulsky) (Lep. Notodontidae). Journal of Applied Entomology, 118: 347-353. Go to original source...
    43. Klimatický atlas Slovenska (2015): Climate Atlas of Slovakia. Bratislava, Slovenský hydrometeorologický ústav.
    44. Kruskal J.B. (1964): Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika, 29: 1-27. Go to original source...
    45. Kulfan J. (1992): Zur Struktur und Saisondynamik von Raupenzönosen (Lepidoptera) an Eichen. Biologia (Bratislava), 47: 653-661.
    46. Kulfan M. (2012): Structure of lepidopterocenoses on oaks Quercus dalechampii and Q. cerris in Central Europe and estimation of the most important species. Munis Entomology & Zoology, 7: 732-741.
    47. Macek J., Dvořák J., Traxler L., Červenka V. (2008): Motýli a housenky střední Evropy. Noční motýli II. - můrovití. Praha, Academia.
    48. Mannai Y., Ezzine O., Hausmann A., Nouira S., Jamâa M.L.B. (2017): Budburst phenology and host use by Operophtera brumata (Linnaeus, 1758) (Lepidoptera: Geometridae) in three Mediterranean oak species. Annals of Forest Science, 1 (74): 1-8. Go to original source...
    49. Martemyanov V.V., Pavlushin S.V., Dubovskiy I.M., Yushkova Y.V., Morosov S.V., Chernyak E.I., Efimov V.M., Ruuhola T., Glupov V.V. (2015): Asynchrony between host plant and insects-defoliator within a tritrophic system: The role of herbivore innate immunity. PloS ONE, 10 (6), e0130988. doi: 10.1371/journal.pone.0130988 Go to original source... Go to PubMed...
    50. Milanović S., Lazarević J., Popović Z., Miletić Z., Kostić M., Radulović Z., Karadžić D., Vuleta A. (2014): Preference and performance of the larvae of Lymantria dispar (Lepidoptera: Lymantriidae) on three species of European oaks. European Journal of Entomology, 111: 371-378. Go to original source...
    51. Mrkva R. (1968): Bionomie píďalky podzimní (Operophtera brumata L.) - motýl a vajíčko. Acta Universitatis Agriculturae (Brno), Series C, 37: 223-246.
    52. Nowacki J., Wąsala R. (2008): Changes in groups of Noctuids (Lepidoptera, Noctuidae) of xerothermic rock swards in the Pieniny Mountains, caused by operation of Czorsztyn-Niedzica and Sromowce Wyżne water reservoirs. Polish Journal of Environmental Studies, 17: 71-77.
    53. Nowacki J., Sosiński J., Śliwa W. (2003): Catocala nymphagoga (ESPER, 1787) (Lepidoptera: Noctuidae) in Poland. Polskie Pismo Entomologiczne, 72: 331-333.
    54. Oksanen J., Blanchet F.G., Friendly M., Kindt R., Legendre P., McGlinn D., Minchin P.R., O'Hara R.B., Simpson G.L., Solymos P., Stevens M.H.H., Szoecs E., Wagner H. (2017): vegan: Community Ecology Package. R package version 2.4-3.
    55. Ovcharov D., Dojchev D., Todorov A. (2000): Differences in attack from leaf chewing pests (families Tortricidae and Geometridae, order Lepidoptera) by some Quercus species. In: Pipkov N., Zhelev P., Draganova I. (eds): Yubileen sbornik nauchni dokladi: 75 godini visshe lesotekhnichesko obrazovanie v Bulgariya. Sektsiya Ekologiya i opazvane na okolnata sreda, Sofia, Lesotekhnicheski Universitet: 269-378.
    56. Pastorális G., Kalivoda H., Panigaj Ľ. (2013): Zoznam motýľov (Lepidoptera) zistených na Slovensku. Folia Faunistica Slovaca, 18: 101-232.
    57. Patočka J. (1954): Húsenice na duboch v ČSR. Bratislava, Štátne pôdohospodárske nakladateľstvo.
    58. Patočka J. (1980): Die Raupen und Puppen der Eichenschmetterlinge Mitteleuropas. Monographien zur Angewandten Entomologie, 23: 1-188.
    59. Patočka J., Kulfan J. (2009): Lepidoptera of Slovakia: bionomics and ecology/Motýle Slovenska: bionómia a ekológia. Bratislava, VEDA.
    60. Patočka J., Krištín A., Kulfan J., Zach P. (1999): Die Eichenschädlinge und ihre Feinde. Zvolen, Institut für Waldökologie der Slowakischen Akademie der Wissenschaften.
    61. Pincebourde S., Sinoquet H., Combes D., Casas J. (2007): Regional climate modulates the canopy mosaic of favourable and risky microclimates for insects. Journal of Animal Ecology, 76: 424-438. Go to original source... Go to PubMed...
    62. R Core Team (2016): R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing. Available at www.R-project.org/ (accessed Jun 12, 2017).
    63. Raupp M.J., Werren J.H., Sadof C.S. (1988): Effects of short-term phenological changes in leaf suitability on the survivorship, growth and development of gypsy moth (Lepidoptera: Lymantriidae) larvae. Environmental Entomology, 17: 316-319. Go to original source...
    64. Rennwald E., Rodeland J. (2013): Lepiforum: Bestimmung von Schmetterlingen (Lepidoptera) und ihren Präimaginalstadien. Available at www.lepiforum.de (accessed Jun 5, 2015).
    65. Rock J., Puettmann K.J., Gockel H.A., Schulte A. (2004): Spatial aspects of the influence of silver birch (Betula pendula L.) on growth and quality of young oaks (Quercus spp.) in central Germany. Forestry, 77: 235-247. Go to original source...
    66. Schafellner C., Krämer W., Schopf A. (2005): Three trophic level interaction: the influence of host plants on the performance of gypsy moth (Lymantria dispar) and its parasitoid, Glyptapanteles liparidis (Hymenoptera, Braconidae). In: Villemant C., Lahbib M., Jamāa B. (eds): Proceedings of the Meeting, Oct 4-8, 2004, Hammamet, Tunisia. Integrated Protection in Oak Forests IOBC/wprs Bulletin, 28: 193-200.
    67. Schopf A., Hoch G., Klaus A., Novotny J., Zubrik M., Schafellner C. (1999): Influence of food quality of two oak species on the development and growth of gypsy moth larvae. In: Lieutier F., Mattson W.J., Wagner M.R. (eds): Physiology and Genetics of Tree-Phytophage Interactions. Paris, INRA: 231-247.
    68. Schwenke W. (1978): Die Forstschädlinge Europas. 3. Band - Schmetterlinge. Hamburg-Berlin, Paul Parey.
    69. Tiberi R., Benassai D., Niccoli A. (2005): Influence of different host plants on the biology and behaviour of the green oak leaf roller, Tortrix viridana L.: first results. In: Villemant C., Lahbib M., Jamāa B. (eds): Proceedings of the Meeting, Oct 4-8, 2004, Hammamet, Tunisia. Integrated Protection in Oak Forests IOBC/wprs Bulletin, 28: 211-217.
    70. Tikkanen O.-P., Julkunen-Tiitto R. (2003): Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata. Oecologia, 136: 244-251. Go to original source... Go to PubMed...
    71. Tikkanen O.-P., Lyytikäinen-Saarenmaa P. (2002): Adaptation of a generalist moth, Operophtera brumata, to variable budburst phenology of host plants. Entomologia Experimentalis et Applicata, 103: 123-133. Go to original source...
    72. Tutin T.G., Heywood V.H., Burges N.A., Valentine D.H., Walters S.M., Webb D.A. (2001): Flora Europaea. Cambridge, Cambridge University Press.
    73. van Asch M., Salis L., Holleman L.J.M., van Lith B., Visser M.E. (2013): Evolutionary response of the egg hatching date of a herbivorous insect under climate change. Nature Climate Change, 3: 244-248. Go to original source...
    74. van Asch M., van Tienderen P.H., Holleman L.J.M., Visser M.E. (2007): Predicting adaptation of phenology in response to climatechange, an insect herbivore example. Global Change Biology, 13: 1596-1604. Go to original source...
    75. van Asch M., Visser M.E. (2007): Phenology of forest caterpillars and their host trees: the importance of synchrony. Annual Review of Entomology, 52: 37-55. https://doi.org/10.17221/11/2018-PPS Go to original source... Go to PubMed...
    76. Van Dongen S., Backeljau T., Matthysen E., Dhondt A.A. (1997): Synchronization of hatching date with budburst of individual host trees (Quercus robur) in the winter moth (Operophtera brumata) and its fitness consequences. Journal of Animal Ecology, 66: 113-121. Go to original source...
    77. Visser M.E., Holleman L.J.M. (2001): Warmer springs disrupt oak and moth phenology. Proceedings of the Real Society of London B, 268 (1464): 289-294. Go to original source... Go to PubMed...
    78. Wagenhoff E., Blum R., Engel K., Veit H., Delb H. (2013): Temporal synchrony of Thaumetopoea processionea egg hatch and Quercus robur budburst. Journal of Pest Science, 86: 193-202. Go to original source...
    79. Wagner W. (2005): Lepidoptera and their ecology. Available at www.pyrgus.de (accessed Jun 5, 2015).
    80. Wang Y., Naumann U., Wright S., Eddelbuettel D., Warton D. (2017): mvabund: Statistical Methods for Analysing Multivariate Abundance Data. R package version 3.12.3.
    81. Warton D.I., Thibaut L., Wang Y.A. (2017): The PIT-trap - A "model-free" bootstrap procedure for inference about regression models with discrete, multivariate responses. PloS ONE, 12 (7): e0181790. doi: 10.1371/journal.pone.0181790 Go to original source... Go to PubMed...
    82. Wesołowski T., Rowiński P. (2008): Late leaf development in pedunculate oak (Quercus robur): An antiherbivore defence? Scandinavian Journal of Forest Research, 23: 386-394. Go to original source...
    83. Wint W. (1983): The role of alternative host-plant species in the life of a polyphagous moth, Operophtera brumata (Lepidoptera: Geometridae). Journal of Animal Ecology, 52: 439-450. Go to original source...
    84. Zalucki M.P., Clarke A.R., Malcolm S.B. (2002): Ecology and behavior of first instar larval Lepidoptera. Annual Review of Entomology, 47: 361-393. Go to original source... Go to PubMed...
    85. Zúbrik M., Hajek A., Pilarska D., Špilda I., Georgiev G., Hrašovec B., Hirka A., Goertz D., Hoch G., Barta M., Saniga M., Kunca A., Nikolov C., Vakula J., Galko J., Pilarski P., Csóka G. (2016): The potential for Entomophaga maimaiga to regulate gypsy moth Lymantria dispar (L.) (Lepidoptera: Erebidae) in Europe. Journal of Applied Entomology, 140: 565-579. Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content