Oecologia

, Volume 157, Issue 2, pp 259–267 | Cite as

Impact of epidermal leaf mining by the aspen leaf miner (Phyllocnistis populiella) on the growth, physiology, and leaf longevity of quaking aspen

  • Diane Wagner
  • Linda DeFoliart
  • Patricia Doak
  • Jenny Schneiderheinze
Plant-Animal Interactions - Original Paper

Abstract

The aspen leaf miner, Phyllocnistis populiella, feeds on the contents of epidermal cells on both top (adaxial) and bottom (abaxial) surfaces of quaking aspen leaves, leaving the photosynthetic tissue of the mesophyll intact. This type of feeding is taxonomically restricted to a small subset of leaf mining insects but can cause widespread plant damage during outbreaks. We studied the effect of epidermal mining on aspen growth and physiology during an outbreak of P. populiella in the boreal forest of interior Alaska. Experimental reduction of leaf miner density across two sites and 3 years significantly increased annual aspen growth rates relative to naturally mined controls. Leaf mining damage was negatively related to leaf longevity. Leaves with heavy mining damage abscised 4 weeks earlier, on average, than leaves with minimal mining damage. Mining damage to the top and bottom surfaces of leaves had different effects on physiology. Mining on the top surface of the leaf had no significant effect on photosynthesis or conductance and was unrelated to leaf stable C isotope ratio (δ13C). Mining damage to the bottom leaf surface, where stomata are located, had significant negative effects on net photosynthesis and water vapor conductance. Percent bottom mining was positively related to leaf δ13C. Taken together, the data suggest that the primary mechanism for the reduction of photosynthesis by epidermal leaf mining by P. populiella is the failure of stomata to open normally on bottom-mined leaves.

Keywords

Populus tremuloides Phyllocnistis populiella Herbivory Leaf mining Growth 

References

  1. Abdel-Reheem S, Belal MH, Gupta G (1991) Photosynthesis inhibition of soybean leaves by insecticides. Environ Pollut 74:245–250PubMedCrossRefGoogle Scholar
  2. Bassman JH, Zwier JC (1993) Effect of partial defoliation on growth and carbon exchange of 2 clones of young Populus trichocarpa Torr and Gray. For Sci 39:419–431Google Scholar
  3. Bassman J, Myers W, Dickmann D, Wilson L (1982) Effect of simulated damage on early growth of nursery-grown hybrid poplars in northern Wisconsin. Can J For Res 12:1–9CrossRefGoogle Scholar
  4. Bonan GB, Shugart HH (1989) Environmental factors and ecological processes in boreal forests. Annu Rev Ecol Syst 20:1–28CrossRefGoogle Scholar
  5. Churchill GB, John HH, Duncan DP, Hodson AC (1964) Long-term effects of defolation of aspen by the forest tent caterpillar. Ecology 45:630–633CrossRefGoogle Scholar
  6. Condrashoff SF (1964) Bionomics of the aspen leaf miner, Phyllocnistis populiella Cham. (Lepidoptera: Gracillariidae). Can Entomol 96:857–874CrossRefGoogle Scholar
  7. Cooke BJ, Roland J (2007) Trembling aspen responses to drought and defoliation by forest tent caterpillar and reconstruction recent outbreaks in Ontario. Can J For Res 37:1586–1598CrossRefGoogle Scholar
  8. Coyle DR, Nebeker TE, Hart ER, Mattson WJ (2005) Biology and management of insect pests in North American intensively managed hardwood forest systems. Annu Rev Entomol 50:1–29PubMedCrossRefGoogle Scholar
  9. Doak P, Wagner D (2007) Variable extrafloral nectary expression and its consequences in quaking aspen. Can J Bot 85:1–9CrossRefGoogle Scholar
  10. Faeth ST, Connor EF, Simberloff D (1981) Early leaf abscission: a neglected source of mortality for folivores. Am Nat 117:409–415CrossRefGoogle Scholar
  11. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and intercellular carbon isotope discrimination and intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:212–127Google Scholar
  12. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537CrossRefGoogle Scholar
  13. Haile FJ, Peterson RKD, Higley LG (1999) Gas-exchange responses of alfalfa and soybean treated with insecticides. J Econ Entomol 92:954–958Google Scholar
  14. Haile FJ, Kerns DL, Richardson JM, Higley LG (2000) Impact of insecticides and surfactant on lettuce physiology and yield. Hortic Entomol 93:788–794Google Scholar
  15. Hering M (1951) Biology of the leaf miners. Junk, ’s-GravenhageGoogle Scholar
  16. Hogg EH, Brandt JP, Kochtubajda B (2002) Growth and dieback of aspen forests in northwestern Alberta, Canada, in relation to climate and insects. Can J For Res 32:823–832CrossRefGoogle Scholar
  17. Johnson MW, Welter SC, Toscano NC, Ting IP, Trumble JT (1983) Reduction of tomato leaflet photosythesis rates by mining activity of Liriomyza sativae (Diptera: Agromyzidae). J Econ Entomol 76:1061–1063Google Scholar
  18. Kosola KR, Dickmann DI, Paul EA, Parry D (2001) Repeated insect defoliation effects on growth, nitrogen acquisition, carbohydrates, and root demography of poplars. Oecologia 129:1432–1939CrossRefGoogle Scholar
  19. Kruger EL, Volin JC, Lindroth RL (1998) Influences of atmospheric CO2 enrichment on the responses of sugar maple and trembling aspen to defoliation. New Phytol 140:85–94CrossRefGoogle Scholar
  20. Krugh BW, Miles D (1996) Monitoring the effects of five “nonherbicidal” pesticide chemicals on terrestrial plants using chlorophyll fluorescence. Environ Toxicol Chem 15:495–500CrossRefGoogle Scholar
  21. Mattson WJ, Addy ND (1975) Phytophagous insects as primary regulators of forest primary production. Science 190:515–522Google Scholar
  22. Mattson WJ, Hart EA, Bolney WJA (2001) Insect pests of Populus: coping with the inevitable. In: Isebrands JG, Dickmann DI, Eckenwalder JE, Richardson J (eds) Poplar culture in North America. NRC Research Press, Ottawa, pp 219–248Google Scholar
  23. Murthy CSHN (1983) Effects of pesticides on photosynthesis. Residue Rev 86:107–129Google Scholar
  24. Nardini A, Raimondo F, Scimone M, Salleo S (2004) Impact of the leaf miner Cameraria ohridella on whole-plant photosynthetic productivity of Aesculus hippocastanum: insights from a model. Trees 18:714–721CrossRefGoogle Scholar
  25. Canada Natural Resources (2004) Yukon forest health report. Natural Resources Canada, OttawaGoogle Scholar
  26. Noormets A, Sôber A, Pell EJ, Dickson RE, Podila GK, Sôber J, Isebrands JG, Karnosky DF (2001) Stomatal and non-stomatal limitation to photosynthesis in two trembling aspen (Populus tremuloides Michx.) clones exposed to elevated CO2 and/or O3. Plant Cell Environ 24:327–336CrossRefGoogle Scholar
  27. Peña JE, Hunsberger A, Schaffer B (2000) Citrus leafminer (Lepidoptera: Gracillariidae) density: effect on yield of “Tahiti” lime. J Econ Entomol 93:374–379PubMedCrossRefGoogle Scholar
  28. Porter WB (1976) Aspects of the biology and dynamics of Phyllocnistis populiella Cham. (Lepidoptera: Phyllocnistidae) on trembling aspen in the Rocky Mountain Foothills of southern Alberta. PhD thesis, University of CalgaryGoogle Scholar
  29. Schaffer B, Pena JE, Colls AM, Hunsberger A (1997) Citrus leafminer (Lepidoptera: Gracillariidae) in lime: assessment of leaf damage and effects on photosynthesis. Crop Prot 164Google Scholar
  30. Pritchard IM, James R (1984) Leaf mines: their effect on leaf longevity. Oecologia 64:132–139CrossRefGoogle Scholar
  31. Proctor JTA, Bodnar JM, Blackburn WJ, Watson RL (1982) Analysis of the effects of the spotted tentiform leafminer (Pyllonorycter blancardella) on the photosynthestic characteristics of apple leaves. Can J Bot 60:2734–2740CrossRefGoogle Scholar
  32. Raimondo F, Ghirardelli LA, Nardini A, Salleo S (2003) Impact of the leaf miner Cameraria ohridella on photosynthesis, water relations and hydraulics of Aesculus hippocastanum leaves. Trees 17:376–382Google Scholar
  33. Reichenbacker RR, Schultz RC, Hart ER (1996) Articifial defoliation effect on Populus growth, biomass production, and total nonstructural carbohydrate concentration. Environ Entomol 25:632–642Google Scholar
  34. Schowalter TD, Hargrove WW, Crossley DA (1986) Herbivory in forested ecosystems. Annu Rev Entomol 31:177–196CrossRefGoogle Scholar
  35. Spieser F, Graf B, Walther P, Noesberger J (1998) Impact of apple rust mite (Acari: Eriophyiidae) feeding on apple leaf gas exchange and leaf color associated with changes in leaf tissue. Environ Entomol 27:1149–1156Google Scholar
  36. Stevens MT, Kruger EL, Lindroth RL (2008) Variation in tolerance to herbivory is mediated by differences in biomass allocation in aspen. Funct Ecol 22:40–47Google Scholar
  37. Trumble JT, Ting IP, Bates L (1985) Analysis of physiological growth and yield responses of celery to Liriomyza trifolii. Entomol Exp Appl 38:15–21CrossRefGoogle Scholar
  38. US Forest Service (2005) Forest health conditions in Alaska - 2005. A forest health protection report. US Forest Service Alaska Region R10-PR-5Google Scholar
  39. Welter SC (1989) Arthropod impact on plant gas exchange. Insect-Plant Interact 1:135–150Google Scholar
  40. Whittaker JB (1994) Physiological responses of leaves of Rumex obtusifolius to damage by a leaf miner. Funct Ecol 8:627–630CrossRefGoogle Scholar
  41. Youngman RR, Leigh TF, Kerby TA, Toscano NC, Jackson CE (1990) Pesticides and cotton: effect on photosynthesis, growth, and fruiting. J Econ Entomol 83:1549–1557Google Scholar
  42. Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum MR, de Lucia EH (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proc Natl Acad Sci USA 99:1088–1091PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Diane Wagner
    • 1
  • Linda DeFoliart
    • 2
  • Patricia Doak
    • 1
  • Jenny Schneiderheinze
    • 1
  1. 1.Institute of Arctic BiologyUniversity of AlaskaFairbanksUSA
  2. 2.Agricultural Research Service, United States Department of AgricultureUniversity of AlaskaFairbanksUSA

Personalised recommendations