, Volume 134, Issue 3, pp 388–396 | Cite as

Microbial impacts on plant-herbivore interactions: the indirect effects of a birch pathogen on a birch aphid

  • Scott N. JohnsonEmail author
  • Angela E. Douglas
  • Stephen Woodward
  • Susan E. Hartley
Plant Animal Interactions


The role of indirect interactions in structuring communities is becoming increasingly recognised. Plant fungi can bring about changes in plant chemistry which may affect insect herbivores that share the same plant, and hence the two may interact indirectly. This study investigated the indirect effects of a fungal pathogen (Marssonina betulae) of silver birch (Betula pendula) on an aphid (Euceraphis betulae), and the processes underpinning the interaction. There was a strong positive association between natural populations of the aphid and leaves bearing high fungal infection. In choice tests, significantly more aphids settled on leaves inoculated with the fungus than on asymptomatic leaves. Individual aphids reared on inoculated leaves were heavier, possessed longer hind tibiae and displayed enhanced embryo development compared with aphids reared on asymptomatic leaves; population growth rate was also positively correlated with fungal infection when groups of aphids were reared on inoculated branches. Changes in leaf chemistry were associated with fungal infection with inoculated leaves containing higher concentrations of free-amino acids. This may reflect a plant-initiated response to fungal attack in which free amino acids from the degradation of mesophyll cells are translocated out of infected leaves via the phloem. These changes in plant chemistry are similar to those occurring during leaf senescence, and are proposed as the mechanistic basis for the positive interaction between the fungus and aphid.


Amino acids Indirect interactions Leaf spot disease Phenolics 



We are grateful to Dr. Peter Mayhew and Dr. Allan Watt for their invaluable critical comments on this manuscript and to Dr. David Elston of Biomathematics and Statistics (Scotland) for statistical guidance. Dr. Alison Karley, Lyn Minto and Kim Simpson are thanked for their assistance with HPLC analysis, as is Robert Strang-Steele for permission to use Dalhaikie Flat for field trials. This research was funded by a NERC PhD Studentship (GT04/98/302/TS).


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Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Scott N. Johnson
    • 1
    • 2
    • 4
    Email author
  • Angela E. Douglas
    • 1
  • Stephen Woodward
    • 3
  • Susan E. Hartley
    • 2
    • 5
  1. 1.Department of BiologyUniversity of YorkYorkUK
  2. 2.Centre for Ecology and HydrologyBanchoryUK
  3. 3.School of Biological SciencesUniversity of AberdeenUK
  4. 4.Department of Soil ScienceUniversity of ReadingWhiteknights, ReadingUK
  5. 5.School of Biological SciencesUniversity of SussexBrightonUK

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