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Russian Journal of Ecology

, Volume 50, Issue 6, pp 511–516 | Cite as

Levels of Leaf Damage by Phyllophages in Invasive Acer negundo and Native Betula pendula and Salix caprea

  • D. V. VeselkinEmail author
  • N. B. Kuyantseva
  • O. E. Chashchina
  • A. G. Mumber
  • G. A. Zamshina
  • D. A. Molchanova
Article
  • 9 Downloads

Abstract—

The validity of some concepts underlying the enemy release hypothesis was tested using the example of Acer negundo, an invasive tree species in Eurasia. For this purpose, the frequency of leaf damage and the proportion of leaf area removed by phyllophagous invertebrates were compared between A. negundo and two native species, Betula pendula and Salix caprea. The leaves of these trees were collected in the city of Miass, the Southern Urals, where three rounds of sampling were carried out in the same habitats during the same growing season. A total of 10 000 leaves were examined to record damage by leaf chewers, miners, or gall makers, other kinds of damage, and the proportion of removed leaf area. By the end of the growing season, the proportion of damaged leaves in A. negundo was estimated at 37%, compared to 66% in B. pendula and 78% in S. caprea, with damage by specialized endophagous species (leaf miners and gall makers) in the first species being very low or absent; the proportion of removed leaf area (relative to the total) in A. negundo was less than 1%, compared to 5.8% in B. pendula and 7.5% in S. caprea. Thus, the level of leaf damage by phyllophagous invertebrates in A. negundo growing in the Southern Urals proved to be lower than in tree species native to this region. Therefore, the absence or low activity of natural enemies for A. negundo may be one of the factors accounting for the success of its invasion in Eurasia.

Keywords:

enemy release hypothesis (ERH) invasive plants alien plants Acer negundo phyllophagous invertebrates leaf damage frequency 

Notes

FUNDING

This study was performed under the state assignments for the Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences and the South Urals Federal Research Center of Mineralogy and Geoecology, Ural Branch, Russian Academy of Sciences.

COMPLIANCE WITH ETHICAL STANDARDS

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

REFERENCES

  1. 1.
    Keane, R. and Crawley, M.J., Exotic plant invasions and the enemy release hypothesis, Trends. Ecol. Evol., 2002, vol. 17, no. 4, pp. 164–170.  https://doi.org/10.1016/S0169-5347(02)02499-0 CrossRefGoogle Scholar
  2. 2.
    Cincotta, C.L., Adams, J.M., and Holzapfel, C., Testing the enemy release hypothesis: A comparison of foliar insect herbivory of the exotic Norway maple (Acer platanoides L.) and the native sugar maple (A. saccharum L.), Biol. Invasions, 2009, vol. 11, no. 2, pp. 379–388.  https://doi.org/10.1007/s10530-008-9255-9 CrossRefGoogle Scholar
  3. 3.
    Liebhold, A.M., Brockerhoff, E.G., Kalisz, S., et al., Biological invasions in forest ecosystems, Biol. Invasions, 2017, vol. 19, no. 11, pp. 3437–3458.  https://doi.org/10.1007/s10530-017-1458-5 CrossRefGoogle Scholar
  4. 4.
    Reinhart, K.O. and Callaway, R.M., Soil biota facilitate exotic Acer invasions in Europe and North America, Ecol. Appl., 2004, vol. 14, no. 6, pp. 1737–1745.  https://doi.org/10.1890/03-5204 CrossRefGoogle Scholar
  5. 5.
    O’Hanlon-Manners, D.L. and Kotanen, P.M., Losses of seeds of temperate trees to soil fungi: Effects of habitat and host ecology, Plant Ecol., 2006, vol. 187, no. 1, pp. 49–58.  https://doi.org/10.1007/s11258-006-9132-5 CrossRefGoogle Scholar
  6. 6.
    Adams, J.M., Fang, W., Callaway, R.M., et al., A cross-continental test of the enemy release hypothesis: Leaf herbivory on Acer platanoides (L.) is three times lower in North America than in its native Europe, Biol. Invasions, 2009, vol. 11, no. 4, pp. 1005–1016.  https://doi.org/10.1007/s10530-008-9312-4 CrossRefGoogle Scholar
  7. 7.
    Ponomareva, E.A. and Bessonova, V.P., Structure of leaf damage by woody plant pests in roadside forest belts, Vestn. Altaisk. Gos. Agrarn. Univ., 2016, no. 1 (135), pp. 77–82.Google Scholar
  8. 8.
    Kirichenko, N. and Kenis, M., Using a botanical garden to assess factors influencing the colonization of exotic woody plants by phyllophagous insects, Oecologia, 2016, vol. 182, no. 1, pp. 243–252.  https://doi.org/10.1007/s00442-016-3645-y CrossRefPubMedGoogle Scholar
  9. 9.
    Schultheis, E.H. and Macguigan, G.J., Competitive ability, not tolerance, may explain success of invasive plants over natives, Biol. Invasions, 2018, vol. 20, no. 10, pp. 2793–2806.  https://doi.org/10.1007/s10530-018-1733-0 CrossRefGoogle Scholar
  10. 10.
    Chun, Y.J., van Kleunen, M., and Dawson, W., The role of enemy release, tolerance and resistance in plant invasions: Linking damage to performance, Ecol. Lett., 2010, vol. 13, no. 8, pp. 937–946.  https://doi.org/10.1111/j.1461-0248.2010.01498.x CrossRefPubMedGoogle Scholar
  11. 11.
    Dostal, P., Allan, E., Dawson, W., et al., Enemy damage of exotic plant species is similar to that of natives and increases with productivity, J. Ecol., 2013, vol. 101, no. 2, pp. 388–399.  https://doi.org/10.1111/1365-2745.12037 CrossRefGoogle Scholar
  12. 12.
    Kirichenko, N., Pere, C., Baranchikov, Yu., et al., Do alien plants escape from natural enemies of congeneric residents? Yes but not from all, Biol. Invasions, 2013, vol. 15, no. 9, pp. 2105–2113.  https://doi.org/10.1007/s10530-013-0436-9 CrossRefGoogle Scholar
  13. 13.
    Najberek, K., Solarz, W., and Chmura, D., Do local enemies attack alien and native impatiens alike?, Acta Soc. Bot. Pol., 2017, vol. 86, no. 4, e3562.  https://doi.org/10.5586/asbp.3562 CrossRefGoogle Scholar
  14. 14.
    Ponomarev, V.I., Il’inykh, A.V., Gninenko, Yu.I., et al., Neparnyi shelkopryad v Zaural’e i Zapadnoi Sibiri (Gypsy Moth in the Transural Region and Western Siberia), Yekaterinburg: Ural. Otd. Ross. Akad. Nauk, 2012.Google Scholar
  15. 15.
    Ponomarev, V.I., Sokolov, G.I., and Klobukov, G.I., Dynamics of Transural gypsy moth population in 2003 to 2013, Lesovedenie, 2016, no. 3, pp. 223–235.Google Scholar
  16. 16.
    Weather and Climate: Reference Information Portal. http://www.pogodaiklimat.ru/history/28647.htm. Cited June 1, 2019.Google Scholar
  17. 17.
    Letopis’ prirody. Kompleksnoe ekologicheskoe obsledovanie i monitoring territorii Il’menskogo gosudarstvennogo zapovednika (promezhutochnyi otchet za 2018 god) (Annals of Nature. Comprehensive Ecological Survey and Monitoring of Ilmen State Nature Reserve: Intermediate Status Report as of 2018), Miass: Yuzhno-Ural. Fed. Nauch, Tsentr Mineralog. Geoekol. Ural Otd. Rioss. Akad. Nauk, 2019.Google Scholar
  18. 18.
    Obzor sanitarnogo i lesopatologicheskogo sostoyaniya lesov Chelyabinskoi oblasti za 2018 god i prognoz na 2019 god (A Review of Sanitary and Forest-Pathological State of Forests in Chelyabinsk Oblast in 2018 and Prediction for 2019) Shiryaev, L.P., Ed., Chelyabinsk: Tsentr Zashchity Lesa, 2019.Google Scholar
  19. 19.
    Belov, D.A., Identification of leaf mining insects developing on plants of the genus Acer based on the kinds of damage they inflict, Lesnoi Vestn., 2017, vol. 21, no. 3, pp. 15–48.Google Scholar
  20. 20.
    Hodkinson, I.D. and Hughes, M.K., Insect Herbivory, London: Chapman and Hall, 1982.CrossRefGoogle Scholar
  21. 21.
    Baranchikov, Yu.N., Similarity in the functional role of phyllophagous insects in forest biocenoses of the earth, in II Vsesoyuznoe soveshchanie: obshchie problemy biogeotsenologii (General Problems in Biogeocenology: II All-Union Conf.), Moscow, 1986, pp. 252–253.Google Scholar
  22. 22.
    Bogacheva, I.A., Vzaimootnosheniya nasekomykh-fitofagov i rastenii v ekosistemakh Subarktiki (Relationships between Phytophagous Insects and Plants in Ecosystems of the Subarctic), Sverdlovsk: Ural. Otd. Akad. Nauk SSSR, 1990.Google Scholar
  23. 23.
    Schowalter, T.D., Hargrove, W.W., and Crossley, D.A., Jr., Herbivory in forested ecosystems, Annu. Rev. Entomol., 1986, vol. 31, no. 1, pp. 177–196.CrossRefGoogle Scholar
  24. 24.
    Kozlov, M., Losses of birch foliage due to insect herbivory along geographical gradients in Europe: A climate-driven pattern, Clim. Change, 2008, vol. 87, nos. 1–2, pp. 107–117.  https://doi.org/10.1007/s10584-007-9348-y CrossRefGoogle Scholar
  25. 25.
    Kozlov, M.V., Zvereva, E.L., and Zverev, V.E., Impacts of Point Polluters on Terrestrial Biota: Comparative Analysis of 18 Contaminated Areas, Dordrecht: Springer, 2009.CrossRefGoogle Scholar
  26. 26.
    Kozlov, M.V., Filippov, B.Yu., Zubrij, N.A., and Zverev, V., Abrupt changes in invertebrate herbivory on woody plants at the forest–tundra ecotone, Polar Biol., 2015, vol. 38, no. 7, pp. 967–974.  https://doi.org/10.1007/s00300-015-1655-6 CrossRefGoogle Scholar
  27. 27.
    Bogacheva, I.A., Dependence of the abundance of phytophagous insects on the level of fluorine pollution in forest biocenoses, in Tekhnogennye elementy i zhivotnyi organizm (polevye nablyudeniya i eksperiment) (Technogenic Elements and Animal Organism: Field Observations and Experiment), Sverdlovsk: Ural. Nauch Tsentr Akad. Nauk SSSR, 1986, pp. 43–47.Google Scholar
  28. 28.
    Belskaya, E.A. and Vorobeichik, E.L., Changes in the trophic activity of leaf-eating insects in birch along the pollution gradient near a Middle Ural copper smelter, Contemp. Probl. Ecol., 2015, vol. 8, no. 3, pp. 397–404.  https://doi.org/10.1134/S199542551503004X CrossRefGoogle Scholar
  29. 29.
    Belskaya, E.A., Dynamics of trophic activity of leaf-eating insects on birch during reduction of emissions from the Middle Ural Copper Smelter, Russ. J. Ecol., 2018, vol. 49, no. 1, pp. 87–92.  https://doi.org/10.1134/S1067413617060029 CrossRefGoogle Scholar
  30. 30.
    Belskaya, E.A. and Vorobeichik, E.L., Responses of leaf-eating insects feeding on aspen to emissions from the Middle Ural Copper Smelter, Russ. J. Ecol., 2013, vol. 44, no. 2, pp. 108–117.  https://doi.org/10.1134/S1067413613020045 CrossRefGoogle Scholar
  31. 31.
    Ashton, I.W. and Lerdau, M.T., Tolerance to herbivory, and not resistance, may explain differential success of invasive, naturalized, and native North American temperate vines: Resistance and tolerance of invasive vines, Divers. Distrib., 2008, vol. 14, pp. 169–178.  https://doi.org/10.1111/j.1472-4642.2007.00425.x CrossRefGoogle Scholar
  32. 32.
    Veselkin, D.V. and Prokina, N.E., Mycorrhiza formation in ash-leaved maple (Acer negundo L.) within the urbanization gradient, Russ. J. Biol. Invasions, 2016, vol. 7, no. 2, pp. 123–128.  https://doi.org/10.1134/S2075111716020132 CrossRefGoogle Scholar
  33. 33.
    Veselkin, D.V., P’yankov, S.V., Safonov, M.A., and Betekhtina, A.A., The structure of absorbing roots in invasive and native maple species, Russ. J. Ecol., 2017, vol. 48, no. 4, pp. 303–310.  https://doi.org/10.1134/S1067413617040166 CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • D. V. Veselkin
    • 1
    Email author
  • N. B. Kuyantseva
    • 2
    • 3
  • O. E. Chashchina
    • 2
  • A. G. Mumber
    • 2
  • G. A. Zamshina
    • 1
  • D. A. Molchanova
    • 1
  1. 1.Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of SciencesYekaterinburgRussia
  2. 2.Ilmeny State Reserve, South Urals Federal Research Center of Mineralogy and Geoecology, Ural Branch, Russian Academy of SciencesMiassRussia
  3. 3.South Ural State UniversityMiassRussia

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