Experimental and Applied Acarology

, Volume 59, Issue 3, pp 263–273 | Cite as

Do plants use airborne cues to recognize herbivores on their neighbours?

  • Yasuyuki Choh
  • Rika Ozawa
  • Junji Takabayashi


Plants show defensive responses after exposure to volatiles from neighbouring plants infested by herbivores. When a plant’s neighbours host only species of herbivores that do not feed on the plant itself, the plant can conserve energy by maintaining a low defence level. An intriguing question is whether plants respond differently to volatiles from plants infested by herbivores that pose greater or lesser degrees of danger. We examined the secretion of extrafloral nectar (EFN) in lima bean plants exposed to volatiles from cabbage plants infested by common cutworm, two-spotted spider mites, or diamondback moth larvae. Although the first two herbivore species feed on lima bean plants, diamondback moth larvae do not. As a control, lima bean plants were exposed to volatiles from uninfested cabbage plants. Only when exposed to volatiles from cabbage plants infested by spider mites did lima bean plants significantly increase their EFN secretion compared with the control. Increased EFN secretion can function as an indirect defence by supplying the natural enemies of herbivores with an alternative food source. Of the three herbivore species, spider mites were the most likely to move from cabbage plants to lima bean plants and presumably posed the greatest threat. Although chemical analyses showed differences among treatments in volatiles produced by herbivore-infested cabbage plants, which compounds or blends triggered the increased secretion of EFN by lima bean plants remains unclear. Thus, our results show that plants may tune their defence levels according to herbivore risk level.


Extrafloral nectar Indirect defence Induced response Plant communication Recognition Herbivore-induced plant volatiles 



This research was financially supported by the Global Center of Excellence Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” of the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan; a Grant-in-Aid for Scientific Research (S) from MEXT, Japan (No. 19101009), and a Core-to-Core project from the Japan Science and Technology Agency.


  1. Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515PubMedCrossRefGoogle Scholar
  2. Arimura G, Ozawa R, Nishioka T, Boland W, Koch T, Kühnemann F, Takabayashi J (2002) Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J 29:87–98PubMedCrossRefGoogle Scholar
  3. Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Nat Acad Sci USA 95:8113–8118PubMedCrossRefGoogle Scholar
  4. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signalling in plant-plant interactions: “talking trees” in the genomics era. Science 311:812–815PubMedCrossRefGoogle Scholar
  5. Bruin J, Dicke M, Sabelis MW (1992) Plants are better protected against spider-mites after exposure to volatiles from infested conspecifics. Experientia 48:525–529CrossRefGoogle Scholar
  6. Bruin J, Sabelis MW, Dicke M (1995) Do plants tap SOS signals from their infested neighbours? Trends Ecol Evol 10:167–170PubMedCrossRefGoogle Scholar
  7. Bruinsma M, Posthumus MA, Mumm R, Mueller MJ, van Loon JJA, Dicke M (2009) Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. J Exp Bot 60:2575–2587PubMedCrossRefGoogle Scholar
  8. Choh Y (2006) Plant-plant interactions mediated by herbivore-induced plant volatiles. Kyoto University, PhD dissertationGoogle Scholar
  9. Choh Y, Takabayashi J (2006) Herbivore-induced extrafloral nectar production in lima bean plants enhanced by previous exposure to volatiles from infested conspecifics. J Chem Ecol 32:2073–2077PubMedCrossRefGoogle Scholar
  10. Choh Y, Shimoda T, Ozawa R, Dicke M, Takabayashi J (2004a) Exposure of lima bean leaves to volatiles from herbivore-induced conspecific plants results in emission of carnivore attractants: active or passive process? J Chem Ecol 30:1305–1317PubMedCrossRefGoogle Scholar
  11. Choh Y, Ozawa R, Takabayashi J (2004b) Effects of exogenous jasmonic acid and benzo (1,2,3) thiadazole-7-carbothionic acid S-methyl ester (BTH), a functional analogue of salicylic acid, on the eggs production of a herbivorous mite Tetranychus urticae (Acari: Tetranychidae). Appl Entomol Zool 39:311–314CrossRefGoogle Scholar
  12. Choh Y, Kugimiya S, Takabayashi J (2006) Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites. Oecologia 147:455–460PubMedCrossRefGoogle Scholar
  13. Choh Y, Uefune M, Takabayashi J (2008) Diamondback moth females oviposit more on plants infested by non-parasitized than by parasitized conspecifics. Ecol Entomol 33:565–568CrossRefGoogle Scholar
  14. de Boer JG, Posthumus MA, Dicke M (2004) Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J Chem Ecol 30:2215–2230PubMedCrossRefGoogle Scholar
  15. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573CrossRefGoogle Scholar
  16. De Moraes CM, Mescher C, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580PubMedCrossRefGoogle Scholar
  17. Dicke M (1999) Specificity of herbivore-induced plant volatiles. In: Insect-plant interactions and induced plant defence (Novartis Foundation). Wiley, Chichester, pp 43–54Google Scholar
  18. Dicke M, Baldwin IT (2010) Evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175PubMedCrossRefGoogle Scholar
  19. Dicke M, Sabelis MW, Takabayashi J, Bruin J, Posthumus MA (1990) Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. J Chem Ecol 16:3091–3118CrossRefGoogle Scholar
  20. Dicke M, Gols R, Ludeking D, Posthumus MA (1999) Jasmonic and herbivory differentially induce carnivore-attractanting plant volatiles in lima bean plants. J Chem Ecol 25:1907–1922CrossRefGoogle Scholar
  21. Dicke M, van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attacks. Nat Chem Biol 5:317–324PubMedCrossRefGoogle Scholar
  22. Dolch R, Tscharntke T (2000) Defoliation of alders (Alnus glutinosa) affects herbivory by leaf beetles on undamaged neighbours. Oecologia 125:504–511CrossRefGoogle Scholar
  23. Fatouros NE, van Loon JJA, Hordijk KA, Smid HM, Dicke M (2005) Herbivore-induced plant volatiles mediate in-flight host discrimination by parasitoids. J Chem Ecol 31:2033–2047PubMedCrossRefGoogle Scholar
  24. Frost CJ, Appel HM, Carlson JE, de Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498PubMedCrossRefGoogle Scholar
  25. Geervliet JBF, Posthumus MA, Vet LEM, Dicke M (1997) Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. J Chem Ecol 23:2935–2954CrossRefGoogle Scholar
  26. Gols R, Roosjen M, Dijkman H, Dicke M (2003) Induction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation. J Chem Ecol 29:2651–2666PubMedCrossRefGoogle Scholar
  27. Heil M (2004) Induction of two indirect defences benefits Lima bean (Phaseolus lunatus, Fabaceae) in nature. J Ecol 92:527–536CrossRefGoogle Scholar
  28. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61PubMedCrossRefGoogle Scholar
  29. Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144PubMedCrossRefGoogle Scholar
  30. Heil M, Kost C (2006) Priming of indirect defences. Ecol Lett 9:813–817PubMedCrossRefGoogle Scholar
  31. Heil M, Silva Bueno JC (2007) Within-plant signalling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Nat Acad Sci USA 104:5467–5472PubMedCrossRefGoogle Scholar
  32. Heil M, Lion U, Boland W (2008) Defense-inducing volatiles: in search of active motif. J Chem Ecol 34:601–604PubMedCrossRefGoogle Scholar
  33. Karban R, Shiojiri K (2009) Self recognition affects plant communication and defense. Ecol Lett 12:502–506PubMedCrossRefGoogle Scholar
  34. Karban R, Baldwin IT, Baxter IJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71CrossRefGoogle Scholar
  35. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emission innature. Science 291:2141–2144PubMedCrossRefGoogle Scholar
  36. Kikuta Y, Ueda H, Nakayama K, Katsuda Y, Ozawa R, Takabayashi J, Matsuda K (2011) Specific regulation of pyrethrin biosynthesis in Chrysanthemum cinerariaefolium by a blend of volatiles emitted from artificially damaged conspecific plants. Plant Cell Physiol 52:588–596PubMedCrossRefGoogle Scholar
  37. Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94:619–628CrossRefGoogle Scholar
  38. Li C, Williams MM, Loh YT, Lee GI, Howe GA (2002) Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiol 130:494–503PubMedCrossRefGoogle Scholar
  39. Ozawa R, Arimura G, Takabayashi J, Shimoda T, Nishioka T (2000) Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol 41:391–398PubMedCrossRefGoogle Scholar
  40. Pallini A, Janssen A, Sabelis MW (1997) Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors. Oecologia 110:179–185CrossRefGoogle Scholar
  41. Raine NE, Willmer P, Stone GN (2002) Spatial structuring and floral avoidance behavior prevent ant-pollinator conflict in Mexican ant-acacia. Ecology 83:3086–3096Google Scholar
  42. Shiojiri K, Takabayashi J, Yano S, Takafuji A (2001) Infochemically mediated tritrophic interaction webs on cabbage plants. Popul Ecol 43:23–29CrossRefGoogle Scholar
  43. Shiojiri K, Ozawa R, Kugimiya S, Uefune M, van Wijk M, Sabelis MW, Takabayashi J (2010) Herbivore-specific, density-dependent induction of plant volatiles: honest or “cry wolf” signals? PLoS ONE 5:1–11CrossRefGoogle Scholar
  44. Takabayashi J, Dicke M (1996) Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci 1:109–113CrossRefGoogle Scholar
  45. Tscharntke T, Thiessen S, Dolch R, Boland W (2001) Herbivory, induced resistance, and interplant signals transfer in Alnus glutinosa. Bioche Syst Ecol 29:1024–1047Google Scholar
  46. Turlings TCJ, Loughrin JH, McCall PJ, Röse USR, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Nat Acad Sci USA 92:4169–4174PubMedCrossRefGoogle Scholar
  47. Turlings TCJ, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habitats: possible consequences for their natural enemies. Biol Cont 11:122–129CrossRefGoogle Scholar
  48. Van Rijn PCJ, Tanigoshi LK (1999) The contribution of extrafloral nectar to survival and reproduction of the predatory mite Iphiseius degenerans and Ricinus communis. Exp Appl Acarol 23:281–296CrossRefGoogle Scholar
  49. Wäckers FL, Wunderlin R (1999) Induction of cotton extrafloral nectar production in response to herbivory does not require a herbivore-specific elicitor. Entomol Exp Appl 91:149–154CrossRefGoogle Scholar
  50. Wäckers FL, Zuber D, Wunderlin R, Keller F (2001) The effect of herbivory on temporal and spatial dynamics of foliar nectar production in cotton and castor. Ann Bot 87:365–370CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Center for Ecological ResearchKyoto UniversityOtsuJapan
  2. 2.Laboratory of Applied Entomology, Department of HorticultureChiba UniversityChibaJapan

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