Insect herbivory may cause changes in the visual properties of leaves and affect the camouflage of herbivores to avian predators
- 489 Downloads
‘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.
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.
KeywordsTrophic interactions Avian vision model Background matching Herbivory Camouflage
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).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
- Cott HB (1940) Adaptive coloration in animals. Methuen, LondonGoogle Scholar
- Cuthill IC (2006) Color perception. In: Hill GE, McGraw KJ (eds) Bird coloration, mechanisms and measurements. Harvard University Press, Cambridge, pp 3–40Google Scholar
- Edmunds M (1990) Evolution of cryptic coloration. In: Evans DL, Schmidt JO (eds) Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany, pp 3–21Google Scholar
- Endler JA (1978) A predator’s view of animal colour patterns. Evol Biol 11:319–364Google Scholar
- Hussain A, Razaq M, Shahzad W, Mahmood K, Khan FZA (2014) Influence of aphid herbivory on the photosynthetic parameters of Brassica campestris at Multan, Punjab, Pakistan. J Biodivers Environ Sci 5:410–416Google Scholar
- Jokinen KJ, Honkanen J, Seppänen P, Törmälä T (1991) Biotechnology of the silver birch (Betula pendula Roth). Agro Food Ind Hi Tech 2:23–26Google Scholar
- Koponen S (1983) Phytophagous insects of birch foliage in northernmost woodlands of Europe and eastern North America. Nordicana 47:165–176Google Scholar
- Silvonen K, Top-Jensen M, Fibiger M (2014) Suomen päivä-ja yöperhoset—maastokäsikirja (a field guide to the butterflies and moths of Finland). Bugbook Publishing, OestermarieGoogle Scholar
- Thayer GH (1909) Concealing coloration in the animal kingdom; an exposition of the laws of disguise through color and pattern; being a summary of Abbott H. Thayer’s disclosures by Gerald H. Thayer with an introductory essay by A.H. Thayer. MacMillan, New YorkGoogle Scholar
- Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358Google Scholar