Birds exploit herbivore-induced plant volatiles to locate herbivorous prey

Ecology Letters

Volumn 16, Issue 11, 2013, Pages 1348-1355

  Amo, Luisa ^a,b   Jansen, Jeroen J ^c   van Dam, Nicole M ^c   Dicke, Marcel ^d   Visser, Marcel E ^a  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b DEPARTAMENTO DE ECOLOGÍA FUNCIONAL Y EVOLUTIVA   (Spain)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Apple trees; Avian olfaction; Foraging; Induced indirect plant defence; Insect herbivores; Insectivorous birds; Multitrophic interactions; Parus major

Indexed keywords

ARTHROPODA; AVES; HEXAPODA; LEPIDOPTERA; MALUS X DOMESTICA; PARUS MAJOR; VERTEBRATA;

VOLATILE ORGANIC COMPOUND;

ANIMAL; APPLE TREES; AVIAN OLFACTION; CHEMISTRY; FORAGING; HERBIVORY; INDUCED INDIRECT PLANT DEFENCE; INSECT HERBIVORES; INSECTIVOROUS BIRDS; LARVA; LETTER; MALUS; METABOLISM; MOTH; MULTITROPHIC INTERACTIONS; ODOR; PARUS MAJOR; PHYSIOLOGY; SONGBIRD;

APPLE TREES; AVIAN OLFACTION; FORAGING; INDUCED INDIRECT PLANT DEFENCE; INSECT HERBIVORES; INSECTIVOROUS BIRDS; MULTITROPHIC INTERACTIONS; PARUS MAJOR;

ANIMALS; HERBIVORY; LARVA; MALUS; MOTHS; PASSERIFORMES; SMELL; VOLATILE ORGANIC COMPOUNDS;

EID: 84885957553     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12177     Document Type: Article

References (41)

1. Amo, L., Rodríguez-Gironés, M.A. & Barbosa, A. (2013). Olfactory detection of dimethyl sulphide in a krill-eating Antarctic penguin. Mar. Ecol. Prog. Ser., 474, 277-285.
2. Anderson, M.J. & Ter Braak, C.J.F. (2003). Permutation tests for multi-factorial analysis of variance. J. Stat. Comput. Simul., 73, 85-113.
3. Boeve, J.L., Lengwiler, U., Tollsten, L., Dorn, S. & Turlings, T.C.J. (1996). Volatiles emitted by apple fruitlets infested by larvae of the European apple sawfly. Phytochemistry, 42, 373-381.
4. Bruce, T.J.A. & Pickett, J.A. (2011). Perception of plant volatile blends by herbivorous insects - Finding the right mix. Phytochemistry, 72, 1605-1611.
5. Bylesjö, M., Rantalainen, M., Cloarec, O., Nicholson, J.K., Holmes, E. & Trygg, J. (2006). OPLS discriminant analysis: combining the strengths of PLS-DA and SIMCA classification. J. Chemometrics, 20, 341-351.
6. Cunningham, S.J., Castro, I. & Potter, M.A. (2009). The relative importance of olfaction and remote touch in prey detection by North Island brow kiwis. Anim. Behav., 78, 899-905.
7. Cuthill, I.C. (2006). Color perception. In: Bird Coloration. Volume I: Mechanisms and Measurements (eds Hill, G.E. & McGraw, K.J.). Harvard University Press, Cambridge, pp. 3-40.
8. Dicke, M. & Baldwin, I.T. (2010). The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. Trends Plant Sci., 15, 167-175.
9. Dicke, M., Van Beek, T.A., Posthumus, M.A., Ben Dom, N., Van Bokhoven, H. & De Groot, A.E. (1990a). Isolation and identification of volatile kairomone that affects acarine predator-prey interactions. Involvement of host plant in its production. J. Chem. Ecol., 16, 381-396.
10. Dicke, M., Sabelis, M.W., Takabayashi, J., Bruin, J. & Posthumus, M.A. (1990b). Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. J. Chem. Ecol., 16, 3091-3118.
11. Fritzsche Hoballah, M.E. & Turlings, T.C.J. (2001). Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evol. Ecol. Res., 3, 553-565.
12. Gomez, L.G., Houston, D.C., Cotton, P. & Tye, A. (1994). The role of greater yellow-headed vultures Cathartes melambrotus as scavengers in neotropical forest. Ibis, 136, 193-196.
13. Kelly, D.J. & Marples, N.M. (2004). The effects of novel odour and colour cues on food acceptance by the zebra finch, Taeniopygia guttata. Anim. Behav., 68, 1049-1054.
14. Landolt, P.J., Brumley, J.A., Smithhisler, C.L., Biddick, L.L. & Hofstetter, R.W. (2000). Apple fruit infested with codling moth are more attractive to neonate codling moth larvae and possess increased amounts of (E, E)-α-farnesene. J. Chem. Ecol., 26, 1685-1699.
15. van Loon, J.J.A., De Boer, J.G. & Dicke, M. (2000). Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomol. Exp. Appl., 97, 219-227.
16. Mäntylä, E., Klemola, T. & Haukioja, E. (2004). Attraction of willow warblers to sawfly-damaged mountain birches: novel function of inducible plant defences? Ecol. Lett., 7, 915-918.
17. Mäntylä, E., Klemola, T., Sirkiä, P. & Laaksonen, T. (2008a). Low light reflectance may explain the attraction of birds to defoliated trees. Behav. Ecol., 19, 325-330.
18. Mäntylä, E., Alessio, G.A., Blande, J.D., Heijari, J., Holopainen, J.K., Laaksonen, T. et al. (2008b). From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS ONE, 3(7), e2832.
19. Mäntylä, E., Klemola, T. & Laaksonen, T. (2011). Birds help plants: a meta-analysis of top-down trophic cascades caused by avian predators. Oecologia, 165, 143-151.
20. Marples, N.M. & Roper, T.J. (1996). Effects of novel colour and smell on the response of naïve chicks towards food and water. Anim. Behav., 51, 1417-1424.
21. Marquis, R.J. & Whelan, C.J. (1994). Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology, 75, 2007-2014.
22. Mols, C.M.M. & Visser, M.E. (2002). Great tits can reduce caterpillar damage in apple orchards. J. Appl. Ecol., 39, 888-899.
23. Mumm, R. & Dicke, M. (2010). Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can. J. Zool., 88, 628-667.
24. Naef-Daenzer, L., Naef-Daenzer, B. & Nager, R.G. (2000). Prey selection and foraging performance of breeding Great Tits Parus major in relation to food availability. J. Avian Biol., 31, 206-214.
25. Nevitt, G.A. (2011). The neuroecology of dimethyl sulfide: a global-climate regulator turned marine infochemical. Integr. Comp. Biol., 51, 819-825.
26. Nevitt, G.A., Veit, R.R. & Kareiva, P. (1995). Dimethyl sulphide as a foraging cue for Antarctic procellariiform seabirds. Nature, 376, 680-682.
27. Perrins, C.M. (1991). Tits and their caterpillar food supply. Ibis, S1(133), 49-54.
28. Pohnert, G., Steinke, M. & Tollrian, R. (2007). Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. Trends Ecol. Evol., 22, 198-204.
29. R Development Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
30. Rowland, H.M., Cuthill, I.C., Harvey, I.F., Speed, M.P. & Ruxton, G.D. (2008). Can't tell the caterpillars from the trees: countershading enhances survival in a woodland. Proc. Biol. Sci., 275, 2539-2545.
31. Schoonhoven, L.M., van Loon, J.J.A. & Dicke, M. (2005). Insect-Plant Biology. Oxford. Oxford Univ, Press.
32. Schuman, M.C., Barthel, K. & Baldwin, I.T. (2012). Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature. ELife, 1, e00007.
33. Sipura, M. (1999). Tritrophic interactions: willows, herbivorous insects and insectivorous birds. Oecologia, 121, 537-545.
34. Stewart-Jones, A. & Poppy, G.M. (2006). Comparison of glass vessels and plastic bags for enclosing living plant parts for headspace analysis. J. Chem. Ecol., 32, 845-864.
35. Takabayashi, J., Dicke, M. & Posthumus, M.A. (1991). Variation in composition of predator attracting allelochemical emitted by herbivore-infested plants: relative influence of plant and herbivore. Chemoecology, 2, 1-6.
36. Turlings, T.C.J. & Tumlinson, J.H. (1992). Systemic release of chemical signals by herbivore-injured corn. Proc. Natl Acad. Sci. USA, 89, 8399-8402.
37. Turlings, T.C.J., Tumlinson, J.H. & Lewis, W.J. (1990). Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science, 250, 1251-1253.
38. Vallat, A., Gu, H. & Dorn, S. (2005). How rainfall relative humidity and temperature influence volatile emissions from apple trees in situ. Phytochemistry, 66, 1540-1550.
39. Van Bael, S.A., Brawn, J.D. & Robinson, S.K. (2003). Birds defend trees from herbivores in a Neotropical forest Canopy. PNAS, 100, 8304-8307.
40. Vet, L.E.M. & Dicke, M. (1992). Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol., 37, 141-172.
41. Westerhuis, J., Hoefsloot, H.J., Smit, S., Vis, D., Smilde, A., Velzen, E.J. et al. (2008). Assessment of PLSDA cross validation. Metabolomics, 4, 81-89.