Advertisement

Arthropod-Plant Interactions

, Volume 8, Issue 2, pp 143–153 | Cite as

Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature?

  • Elina Mäntylä
  • James D. Blande
  • Tero Klemola
Original Paper

Abstract

Earlier studies have suggested that insectivorous birds, similar to invertebrate predators and parasitoids, may be guided by herbivore-induced plant volatiles (HIPVs) to damaged, herbivore-rich trees. Recent studies have also shown that birds use olfaction more than previously thought, underlying the potential for HIPVs to be sensed by insectivorous birds and utilised during foraging for prey. The HIPV production in plants is mediated, at least partly, by the jasmonic acid signalling pathway, and similar HIPVs to those induced by herbivores can often be induced by exposing plants to methyl jasmonate (MeJa). We studied the effects of MeJa on volatile emission and bird attraction using mature mountain birches (Betula pubescens ssp. czerepanovii) under natural conditions in northern Finland. Experimental trees were assigned to four treatment groups: herbivore-damaged [autumnal moth (Epirrita autumnata)], higher dose of MeJa (30 mM), lower dose of MeJa (15 mM) and control. All trees had three branches covered with mesh bags, but there were larvae inside the bags only of the herbivore-damage treatment. Bird predation rate was monitored with artificial plasticine larvae which were checked daily for peck marks. Birds most often pecked the larvae in the herbivore-damaged trees, but the attractiveness of MeJa-treated trees did not differ from the control. High within-treatment variation in systemic HIPV emissions probably masked MeJa treatment effects. The bird predation rate was high in birches that emitted large amounts of α-pinene. Thus, α-pinene may be one cue used by birds to find herbivore-rich birches.

Keywords

α-Pinene Avian predation Herbivory Methyl jasmonate Volatile organic compounds 

Notes

Acknowledgments

Thanks for the help in the field and laboratory work to Tea Ammunét, Tommi Andersson, Tanja Hannola, Liisa Huttunen, Minna Korjus, Kristiina Mutkala, Elisa Männistö, Robert Todd and Suvi Vanhakylä. We would like to thank anonymous reviewers for helpful comments on the draft manuscript. The study was funded by Emil Aaltonen foundation (Grant to EM). JDB acknowledges funding from Academy of Finland project no. 251898.

References

  1. Amo L, Jansen JJ, van Dam NM, Dicke M, Visser ME (2013) Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecol Lett 16:1348–1355PubMedCrossRefGoogle Scholar
  2. Arimura GI, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochem Biophy Acta 1734:1–111Google Scholar
  3. Beltrano J, Ronco MG, Montaldi ER, Carbone A (1998) Senescence of flag leaves and ears of wheat hastened by methyl jasmonate. J Plant Growth Regul 17:53–57CrossRefGoogle Scholar
  4. Cunningham SJ, Castro I, Potter MA (2009) The relative importance of olfaction and remote touch in prey detection by North Island brown kiwis. Anim Behav 78:899–905CrossRefGoogle Scholar
  5. De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573CrossRefGoogle Scholar
  6. Degenhart DC, Lincoln DE (2006) Volatile emissions from an odorous plant in response to herbivory and methyl jasmonate exposure. J Chem Ecol 32:725–743CrossRefGoogle Scholar
  7. Dicke M, van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324PubMedCrossRefGoogle Scholar
  8. Elkington TT (1968) Introgressive hybridization between Betula nana L. and B. pubescens Ehrh in North-West Iceland. New Phytol 67:109–118CrossRefGoogle Scholar
  9. Farag MA, Paré PW (2002) C6-green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61:545–554PubMedCrossRefGoogle Scholar
  10. Filella I, Peñuelas J, Llusiá J (2006) Dynamics of the enhanced emissions of monoterpenes and methyl salicylate, and decreased uptake of formaldehyde, by Quercus ilex leaves after application of jasmonic acid. New Phytol 169:135–144PubMedCrossRefGoogle Scholar
  11. Gould N, Reglinski T, Northcott GL, Spiers M, Taylor JT (2009) Physiological and biochemical responses in Pinus radiata seedlings associated with methyl jasmonate-induced resistance to Diplodia pinea. Physiol Mol Plant P 74:121–128CrossRefGoogle Scholar
  12. Guenther AB, Zimmerman PR, Harley PC, Monson RK, Fall R (1993) Isoprene and monoterpene emission rate variability: model evaluations and sensitivity analyses. J Geophys Res 98:12609–12617CrossRefGoogle Scholar
  13. Hagen SB, Jepsen JU, Yoccoz NG, Ims RA (2008) Anisotropic patterned population synchrony in climatic gradients indicates nonlinear climatic forcing. Proc R Soc B 275:1509–1515PubMedCentralPubMedCrossRefGoogle Scholar
  14. Hare JD (2007) Variation in herbivore and methyl jasmonate-induced volatiles among genetic lines of Datura wrightii. J Chem Ecol 33:2028–2043PubMedCrossRefGoogle Scholar
  15. Haukioja E (2003) Putting the insect into the birch–insect interaction. Oecologia 136:161–168PubMedCrossRefGoogle Scholar
  16. Haukioja E, Niemelä P (1979) Birch leaves as a resource for herbivores: seasonal occurrence of increased resistance in foliage after mechanical damage to adjacent leaves. Oecologia 39:151–159CrossRefGoogle Scholar
  17. Heijari J, Blande JD, Holopainen JK (2011) Feeding of large pine weevil on Scots pine stem triggers localized bark and systemic shoot emission of volatile organic compounds. Environ Exp Bot 71:390–398Google Scholar
  18. Heil M (2004) Induction of two indirect defences benefits Lima bean (Phaseolus lunatus, Fabaceae) in nature. J Ecol 92:527–536CrossRefGoogle Scholar
  19. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472PubMedCentralPubMedCrossRefGoogle Scholar
  20. Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272PubMedCrossRefGoogle Scholar
  21. Helmig D, Ortega J, Guenther A, Herrick JD, Geron C (2006) Sesquiterpene emissions from loblolly pine and their potential contribution to biogenic aerosol formation in the Southeastern US. Atmos Environ 40:4150–4157CrossRefGoogle Scholar
  22. Hopke J, Donath J, Blechert S, Boland W (1994) Herbivore-induced volatiles: the emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a betaglucosidase and jasmonic acid. FEBS Lett 352:146–150PubMedCrossRefGoogle Scholar
  23. Hristova VA, Popova LP (2002) Treatment with methyl jasmonate alleviates the effects of paraquat on photosynthesis in barley plants. Photosynthetica 40:567–574CrossRefGoogle Scholar
  24. Kaitaniemi P, Ruohomäki K (2001) Sources of variability in plant resistance against insects: free caterpillars show strongest effects. Oikos 95:461–470CrossRefGoogle Scholar
  25. Kallio P, Mäkinen Y (1978) Vascular flora of Inari Lapland: 4. Betulaceae Rep Kevo Subarct Res Stat 14:38–63Google Scholar
  26. Kapari L, Haukioja E, Rantala MJ, Ruuhola T (2006) Defoliating insect immune defense interacts with induced plant defense during a population outbreak. Ecology 87:291–296PubMedCrossRefGoogle Scholar
  27. Kaplan I (2012) Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire? Biol Control 60:77–89CrossRefGoogle Scholar
  28. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144PubMedCrossRefGoogle Scholar
  29. Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25:348–357CrossRefGoogle Scholar
  30. Kigathi RN, Unsicker SB, Reichelt M, Kesselmeier J, Gershenzon J, Weisser WW (2009) Emission of volatile organic compounds after herbivory from Trifolium pratense (L.) under laboratory and field conditions. J Chem Ecol 35:1335–1348PubMedCentralPubMedCrossRefGoogle Scholar
  31. Klemola T, Ammunét T, Andersson T, Klemola N, Ruohomäki K (2012) Larval parasitism rate increases in herbivore-damaged trees: a field experiment with cyclic birch feeding moths. Oikos 121:1525–1531CrossRefGoogle Scholar
  32. Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94:619–628CrossRefGoogle Scholar
  33. Mäntylä E, Klemola T, Haukioja E (2004) Attraction of willow warblers to sawfly-damaged mountain birches: novel function of inducible plant defences? Ecol Lett 7:915–918CrossRefGoogle Scholar
  34. 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):e2832PubMedCentralPubMedCrossRefGoogle Scholar
  35. Mäntylä E, Klemola T, Sirkiä P, Laaksonen T (2008b) Low light reflectance may explain the attraction of birds to defoliated trees. Behav Ecol 19:325–330CrossRefGoogle Scholar
  36. Mäntylä E, Klemola T, Laaksonen T (2011) Birds help plants: a meta-analysis of top-down trophic cascades caused by avian predators. Oecologia 165:143–151PubMedCrossRefGoogle Scholar
  37. Mennerat A (2008) Blue tits (Cyanistes caeruleus) respond to an experimental change in the aromatic plant odour composition of their nest. Behav Process 79:189–191CrossRefGoogle Scholar
  38. 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 USA 107:7335–7340PubMedCentralPubMedCrossRefGoogle Scholar
  39. Pareja M, Mohib A, Birkett MA, Dufour S, Glinwood RT (2009) Multivariate statistics coupled to generalized linear models reveal complex use of chemical cues by a parasitoid. Anim Behav 77:901–909CrossRefGoogle Scholar
  40. Parejo D, Amo L, Rodríguez J, Avilés JM (2012) Rollers smell the fear of nestlings. Biol Lett 8:502–504PubMedCentralPubMedCrossRefGoogle Scholar
  41. Peñuelas J, Munné-Bosch S, Llusià J, Filella I (2004) Leaf reflectance and photo- and antioxidant protection in field-grown summer-stressed Phillyrea angustifolia. Optical signals of oxidative stress? New Phytol 162:115–124CrossRefGoogle Scholar
  42. Pieterse CMJ, Leon-Reyes A, van der Ent S, van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316PubMedCrossRefGoogle Scholar
  43. Poch TJ, Simonetti JA (2013) Ecosystem services in human-dominated landscapes: insectivory in agroforestry systems. Agroforest Syst 87:871–879CrossRefGoogle Scholar
  44. Roper TJ (1999) Olfaction in birds. Adv Stud Behav 28:247–332CrossRefGoogle Scholar
  45. Schiebe C, Hammerbacher A, Birgersson G, Witzell J, Brodelius PE, Gershenzon J, Hansson BS, Krokene P, Schlyter F (2012) Inducibility of chemical defenses in Norway spruce bark is correlated with unsuccessful mass attacks by the spruce bark beetle. Oecologia 170:183–198PubMedCrossRefGoogle Scholar
  46. Steiger SS, Fidler AE, Valcu M, Kempenaers B (2008) Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds? Proc R Soc B 275:2309–2317PubMedCentralPubMedCrossRefGoogle Scholar
  47. Stroup WW (2013) Generalized linear mixed models: modern concepts, methods and applications. CRC Press, Boca RatonGoogle Scholar
  48. Thaler JS, Stout MJ, Karban R, Duffey SS (1996) Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 22:1767–1781PubMedCrossRefGoogle Scholar
  49. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270PubMedCrossRefGoogle Scholar
  50. Turlings TCJ, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-injured corn. Proc Natl Acad Sci USA 89:8399–8402PubMedCentralPubMedCrossRefGoogle Scholar
  51. Van Bael SA, Philpott SM, Greenberg R, Bichier P, Barber NA, Mooney KA, Gruner DS (2008) Birds as predators in tropical agroforestry systems. Ecology 89:928–934PubMedCrossRefGoogle Scholar
  52. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle RiverGoogle Scholar
  53. Zhang Y, Xie Y, Xue J, Peng G, Wang X (2009) Effect of volatile emissions, especially α-pinene, from persimmon trees infested by Japanese wax scales or treated with methyl jasmonate on recruitment of ladybeetle predators. Environ Entomol 38:1439–1445PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Elina Mäntylä
    • 1
    • 2
  • James D. Blande
    • 3
  • Tero Klemola
    • 1
  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland
  2. 2.Institute of BiologyFreie Universität BerlinBerlinGermany
  3. 3.Department of Environmental ScienceUniversity of Eastern FinlandKuopioFinland

Personalised recommendations