Insectivorous Birds Are Attracted by Plant Traits Induced by Insect Egg Deposition
- 732 Downloads
Insectivorous birds feed upon all developmental stages of herbivorous insects, including insect eggs if larvae and adults are unavailable. Insect egg deposition on plants can induce plant traits that are subsequently exploited by egg parasitoids searching for hosts. However, it is unknown whether avian predators can also use egg-induced plant changes for prey localization. Here, we studied whether great tits (Parus major) and blue tits (Cyanistes caeruleus) are attracted by traits of the Scots pine (Pinus sylvestris) induced by pine sawfly (Diprion pini) egg deposition. We chose this plant – insect system because sawfly egg deposition on pine needles is known to locally and systemically induce a change in pine volatile organic compounds (VOCs), and tits are known to prey upon sawfly eggs. In dual choice laboratory experiments, we simultaneously offered the birds an egg-free control branch and a systemically egg-induced branch. Significantly more birds visited the egg-induced branch first. We confirmed by GC-MS analyses that systemically egg-induced branches released more (E)-β-farnesene compared to control branches. Spectrophotometric analyses showed that control branches reflected more light than egg-induced branches throughout the avian visual range. Although a discrimination threshold model for blue tits suggests that the birds are poor at discriminating this visual difference, the role of visual stimuli in attracting the birds to egg-induced pines cannot be discounted. Our study shows, for the first time, that egg-induced odorous and/or visual plant traits can help birds to locate insect eggs without smelling or seeing those eggs.
KeywordsInsect egg deposition Light reflectance Olfaction Terpenoids Vision Volatile organic compounds
We thank Ute Braun, Freie Universität Berlin, for her help in rearing the sawflies and collecting pine branches. We also thank Prof. Dr. Holger Dau and Dr. Ivelina Zaharieva from the Physics Department, Freie Universität Berlin, for assistance with the spectrophotometer. The study was supported financially by the Finnish Cultural Foundation (grant to EM), the ERC grant no 669609 (EM) and the Academy of Finland via the project no 257581 (CL).
Compliance with Ethical Standards
The birds were studied with a license from Landesamt für Gesundheit und Soziales, Berlin (no. 0149/12), and ringed with a license from Vogelwarte Radolfzell (no. 1882). The experimental procedure never caused damage or signs of severe distress to the birds. All birds were released back into the wild, close to their place of capture, immediately after the experiment. The time in captivity for each bird was 40.0 (31.0, 54.0) minutes [median (lower quartile, upper quartile)].
- Adamik P, Koman M, Vojtek J (2003) The effect of habitat structure on guild patterns and the foraging strategies of insectivorous birds in forests. Biologia 58:275–286Google Scholar
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Series B 57:289–300Google Scholar
- Bereczki K, Molnár D, Csóka G, Báldi A (2017) Factors affecting the bird predation of low density gypsy moth egg masses in three types of hardwood forests in Southwest Hungary. Bull Insectol 70:201–207Google Scholar
- Bombosch S, Ramakers PMJ (1976) Zur Dauerzucht von Gilpinia hercyniae (Htg). Zeitschr. Pflanzenkrankh Pflanzenschutz 83:40–44Google Scholar
- Cuthill IC (2006) Colour perception. In: Hill GE, McGraw KJ (eds) Bird Colouration, mechanisms and measurements. Harvard University Press, Cambridge, pp 3–40Google Scholar
- Hilker M, Fatouros NE (2015) Plant responses to insect egg deposition. Annu Rev Entomol 60:493–515. https://doi.org/10.1146/annurev-ento-010814-020620 CrossRefPubMedGoogle Scholar
- König WA, Joulain D, Hochmuth DH (2006) GC/MS Library: Terpenoids and Related Constituents of Essential Oils. Retrieved from http://massfinder.com/wiki/Terpenoids_Library (Accessed 18 June 2014)
- Koski T-M, Lindstedt C, Klemola T, Troscianko J, Mäntylä E, Tyystjärvi E, Stevens M, Helander M, Laaksonen T (2017) 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. https://doi.org/10.1007/s00265-017-2326-0 CrossRefGoogle Scholar
- Mäntylä E, Alessio GA, Blande JD, Heijari J, Holopainen JK, Laaksonen T, Piirtola P, Klemola T (2008a) From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS One 3(7):e2832. https://doi.org/10.1371/journal.pone.0002832 CrossRefPubMedPubMedCentralGoogle Scholar
- Mooney KA, Gruner DS, Barber NA, Van Bael SA, Philpott SM, Greenberg R (2010) Interactions among predators and the cascading effects of vertebrate insectivores on arthropod communities and plants. Proc Natl Acad Sci U S A 107:7335–7340. https://doi.org/10.1073/pnas.1001934107 CrossRefPubMedPubMedCentralGoogle Scholar
- Naef-Daenzer B, Keller LF (1999) The foraging performance of great and blue tits (Parus major and P. caeruleus) in relation to caterpillar development, and its consequences for nestling growth and fledging weight. J Anim Ecol 68:708–718. https://doi.org/10.1046/j.1365-2656.1999.00318.x CrossRefGoogle Scholar
- Olofsson E (1986) Winter feeding by the great tit, Parus major, on eggs of the European pine sawfly, Neodiprion sertifer. Ornis Fennica 63:91–92Google Scholar
- Stein SE (2011) Retention indices. In: Linstrom PJ, Mallard WG (eds) NIST Chemistry WebBook, NIST Standard Reference Database Number 69. National Institute of Standards and Technology, Gaithersburg, retrieved from http://webbook.nist.gov/
- Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172. https://doi.org/10.1146/annurev.en.37.010192.001041 CrossRefGoogle Scholar
- Ziegler R (1997) Lipid synthesis by ovaries and fat bodies of Aedes aegypti (Diptera: Culicidae). Eur J Entomol 94:385–391Google Scholar