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Insect herbivory may cause changes in the visual properties of leaves and affect the camouflage of herbivores to avian predators

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Abstract

‘Cry for help’ hypothesis predicts that attraction of predators with chemical or visual cues can decrease insect damage of plants. Visual cues involve changes in photosynthetic activity and the reflectance of leaves, and there is some evidence that birds may use these changes as foraging cues. However, changes in the visual properties of leaves have not been quantified and it is not known how birds see these changes. We also presented and tested a new ‘reduction in camouflage’ hypothesis (not mutually exclusive with cry for help) stating that herbivore-mediated changes in leaf colour can increase the conspicuousness of herbivore against leaves. To define changes in the visual properties of leaves, their detectability to birds, and whether these changes affect the conspicuousness of herbivore, we manipulated the level of herbivory in silver birch trees (Betula pendula) with autumnal moth (Epirrita autumnata) larvae, and used blue tit (Cyanistes caeruleus) vision models to images of leaves and larvae. Hue, luminance (lightness), contrast, light transmission, chlorophyll content, photosynthetic activity and water content of the leaves were compared between herbivore-damaged and control trees. The leaves of herbivore-damaged trees had a decreased chlorophyll a concentration, increased contrast and they reflected more longer wavelengths. However, these changes are likely not obvious to birds. In contrast to our expectation, there were only minor differences in conspicuousness of larvae against the leaves of damaged trees, which may be very subtle to predator vision. Nevertheless, according to visual models, larvae should be easily detectable to birds from both herbivore-damaged and control trees.

Significance statement

Herbivory affects photosynthetic machinery and light reflectance of leaves, and may thus provide visual foraging cues to birds, although it is not known how these changes appear to birds. We also hypothesized that the changes in leaves may reduce the camouflage of the herbivore. After applying herbivore treatment and using the avian vision models, we found that the leaves of herbivore damage may cause the leaves to appear to birds with higher contrast and greener or a more yellowish colour than control leaves. In addition, although the herbivore was visible to birds, it was slightly less conspicuous when on damaged trees, indicating that the herbivore can be adapted to changes in the food plant. Our results indicate that herbivory causes changes visual properties of leaves, but these changes are likely not obvious to birds.

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Acknowledgements

We thank Päivi M. Sirkiä for her valuable comments on the manuscript and Mariel Mansoniemi for conducting the photosynthesis and fluorescence measurements. We are also grateful to the anonymous reviewers; their comments significantly improved the manuscript. This study was financially supported by the University of Turku Graduate School (T-MK) and by the Academy of Finland (grant 218086 to TL; grants 259075 and 271832 to ET).

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Authors and Affiliations

  1. Section of Ecology, Department of Biology, University of Turku, FI-20014, Turku, Finland

    Tuuli-Marjaana Koski, Tero Klemola, Elina Mäntylä, Marjo Helander & Toni Laaksonen

  2. Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, FI-40014, Jyväskylä, Finland

    Carita Lindstedt

  3. Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Penryn, Cornwall, TR10 9FE, UK

    Jolyon Troscianko & Martin Stevens

  4. Department of Biochemistry/Molecular Plant Biology, University of Turku, FI-20014, Turku, Finland

    Esa Tyystjärvi

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  1. Tuuli-Marjaana Koski
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  2. Carita Lindstedt
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Correspondence to Tuuli-Marjaana Koski.

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Communicated by E. Fernandez-Juricic

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Table 1 Result from principal component scores explaining variation in leaf colour using UV-, short wave-, medium wave- and long wave-sensitive cone values of blue tit
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Koski, TM., Lindstedt, C., Klemola, T. et al. Insect herbivory may cause changes in the visual properties of leaves and affect the camouflage of herbivores to avian predators. Behav Ecol Sociobiol 71, 97 (2017). https://doi.org/10.1007/s00265-017-2326-0

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