Skip to main content
SpringerLink
Log in

What signals do herbivore-induced plant volatiles provide conspecific herbivores?

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Herbivore-induced plant volatiles (HIPVs) have been opined as ‘indirect or direct defenses’ of plants and are extensively studied. In contrast, HIPVs may also indicate that plant defenses have been overcome by herbivores infesting the plant; however, studies on this aspect have so far received little attention. Using the interaction of Capsicum annum (Bell pepper) with its pest Scirtothrips dorsalis (Chilli thrips) as a model system, we studied the role of HIPVs in this selected insect–plant interaction. Multiple-choice olfactometer assays with headspace volatiles collected from different growth stages of un-infested C. annum plants represented by pre-flowering (PF), flowering (FL) and fruiting stages (FR) proved FR volatiles to be highly attractive to S. dorsalis. Further, FR plants were infested with S. dorsalis adults and HIPVs released by infested plants were collected and subjected to multiple-choice olfactometer bioassays. Thrips were significantly attracted to HIPVs than to headspace volatiles of un-infested FR plants or thrips body odour. Coupled GC-EAG with S. dorsalis and HIPVs or FR plant volatile revealed specific compounds that elicited an EAG response. Individual EAG-active compounds were less attractive to thrips, however, synthetic blends of EAG-active compounds at the ratio similar to headspace samples were found to be highly attractive. However, when given a choice between synthetic blends of HIPVs and FR, thrips were significantly attracted to synthetic blend of HIPVs. Our study provides empirical data on signals HIPVs may provide to conspecific herbivores and suggests that the role of HIPVs, mostly generalized as defense, may vary based on the interaction and must be studied closely to understand their ecological functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ananthakrishnan T (1993) Bionomics of thrips. Annu Rev Entomol 38:71–92

    Article  Google Scholar 

  • Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50(5):911–923

    Article  CAS  PubMed  Google Scholar 

  • Bernasconi ML, Turlings TCJ, Ambrosetti L, Bassetti P, Dorn S (1998) Herbivore induced emissions of maize volatiles repel the corn leaf aphid Rhopalosiphum maidis. Entomol Exp Appl 87:133–142

    Article  CAS  Google Scholar 

  • Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman and Hall, New York, pp 1–312

  • Bolter CJ, Dicke M, Van Loon JJA, Visser JH, Posthumus MA (1997) Attraction of Colorado potato beetle to herbivore-damaged plants during herbivory and after its termination. J Chem Ecol 23:1003–1023

    Article  CAS  Google Scholar 

  • Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects-finding the right mix. Phytochem 72:1605–1611

    Article  CAS  Google Scholar 

  • Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    Article  CAS  PubMed  Google Scholar 

  • Cardoza YJ, Tumlinson JH (2006) Compatible and incompatible Xanthomonas infections differentially affect herbivore-induced volatile emission by pepper plants. J Chem Ecol 32:1755–1768

    Article  CAS  PubMed  Google Scholar 

  • Carroll MJ, Schmelz EA, Meagher RL, Teal PEA (2006) Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. J Chem Ecol 32:1911–1924

    Article  CAS  PubMed  Google Scholar 

  • Carroll MJ, Schmelz EA, Teal PEA (2008) The attraction of Spodoptera frugiperda neonates to cowpea seedlings is mediated by volatiles induced by conspecific herbivory and the elicitor inceptin. J Chem Ecol 34:291–300

    Article  CAS  PubMed  Google Scholar 

  • Clavijo McCormick A, Irmisch S, Reinecke A, Boeckler GA, Veit D, Reichelt M, Hansson BS, Gershenzon J, Kollner TG, Unsicker SB (2014) Herbivore-induced volatile emission in black poplar: regulation and role in attracting herbivore enemies. Plant Cell Environ 37(8):1909–1923

    Article  PubMed  Google Scholar 

  • Clavijo McCormick A, Reinecke A, Gershenzon J, Unsicker SB (2016) Feeding experience affects the behavioral response of polyphagous gypsy moth caterpillars to herbivore-induced poplar volatiles. J Chem Ecol 42:382–393

    Article  Google Scholar 

  • D’Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J (2007) Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J 49:194–207

  • De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH (1998) Herbivore infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • De Moraes CM, Mescheer MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel nonspecific females. Nature 410:577–580

    Article  PubMed  Google Scholar 

  • Delphia CM, Mescher MC, De Moraes CM (2007) Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33:997–1012

    Article  CAS  PubMed  Google Scholar 

  • Dethier VG (1982) Mechanisms of host plant recognition. Entomol Exp Appl 31:49–56

    Article  Google Scholar 

  • Dicke J, van Beek TA, Posthumus MA, Ben Dom N, Van Bokhoven H, De Groot AE (1990) 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

    Article  CAS  PubMed  Google Scholar 

  • Dickens JC (2002) Behavioral responses of larvae of Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) to host plant volatile blends attractive to adults. Agric Entomol 4:309–314

    Article  Google Scholar 

  • Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156(2):145–169

    Article  CAS  Google Scholar 

  • Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera: Sphingidae) and its natural host, Nicotiana attenuata. III Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harari AR, Yakir DB, Rosen D (1994) Mechanism of aggregation behavior in Maladera matrida Argaman (Coleoptera: Scarabidae). J Chem Ecol 20:361–371

    Article  CAS  PubMed  Google Scholar 

  • Horiuchi JI, Arimura GI, Ozawa R, Shimoda T, Takabayashi J, Nishioka T (2003) A comparison of the responses of Tetranychus urticae (Acari: Tetranychidae) and Phytoseiulus persimilis (Acari: Phytoseiidae) to volatiles emitted from lima bean leaves with different levels of damage made by T. urticae or Spodoptera exigua (Lepidoptera: Noctuidae). Appl Entomol Zool 38:109–116

    Article  Google Scholar 

  • Huang CH, Yan FM, Byers JA, Wang RJ, Xu CR (2009) Volatiles induced by the larvae of the Asian corn borer (Ostrinia furnacalis) in maize plants affect behavior of conspecific larvae and female adults. Insect Sci 16:311–320

    Article  CAS  Google Scholar 

  • Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273

    Article  Google Scholar 

  • Jan De Kogel W (2001) Preference and performance of western flower thrips. Thrips and tospoviruses: Proceedings of the 7th international symposium on Thysanoptera, pp 181–183

  • Kalberer NM, Turlings TCJ, Rahier M (2001) Attraction of a leaf beetle (Oreina cacaliae) to damaged host plants. J Chem Ecol 27:647–661

    Article  CAS  PubMed  Google Scholar 

  • Kamala Jayanthi PD, Woodcock CM, Caulfield J, Birkett MA, Bruce TJA (2012) Isolation and identification of host cues from mango, Mangifera indica that attract gravid female oriental fruit fly, Bactrocera dorsalis. J Chem Ecol 38:361–369

    Article  CAS  Google Scholar 

  • Kamala Jayanthi PD, Kempraj V, Aurade RM, Venkataramanappa RK, Nandagopal B, Verghese A, Bruce TJA (2014) Oviposition site-selection by Bactrocera dorsalis is mediated through an innate recognition template tuned to γ-Octalactone. PLoS ONE 9:1–6

    Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    Article  CAS  PubMed  Google Scholar 

  • Kirk WDJ (1985) Effect of some floral scents on host finding by thrips. J Chem Ecol 11:35–43

    Article  CAS  PubMed  Google Scholar 

  • Landolt PJ, Tumlinson JH, Alborn DH (1999) Attraction of Colorado potato beetle (Coleoptera: Chrysomelidae) to damaged and chemically induced potato plants. Environ Entomol 28:973–978

    Article  Google Scholar 

  • Landolt PJ, Brumley JA, Smithhisler CL, Biddick LL, Hofstetter RW (2000) Apple fruit infested with codling moth are more attractive to neonate codling moth larvae and possess increased amounts of (E,E)-alpha-farnesene. J Chem Ecol 26:1685–1699

    Article  CAS  Google Scholar 

  • Loughrin JH, Manukian A, Heath RR, Turlings TCJ, Tumlinson JH (1994) Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plants. Proc Natl Acad Sci USA 91:11836–11840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loughrin JH, Potter DA, Kemp TRH (1995) Volatile compounds induced by herbivory act as aggregation kairomones for the Japanese beetle (Popilia japonica Newman). J Chem Ecol 21:1457–1467

    Article  CAS  PubMed  Google Scholar 

  • Palmer JM, Mound LA (1983) The Scirtothrips species of Australia and New Zealand (Thysonaptera: Thripidae). J Nat Hist 17(4):507–518

    Article  Google Scholar 

  • Pare PW, Tumlinson JH (1997) Induced synthesis of plant volatiles. Nature 385:30–31

    Article  CAS  Google Scholar 

  • Pettersson J (1970) An aphid sex attractant. Entomol Scand 1:63–73

    Article  Google Scholar 

  • Pickett JA, Wadhams LJ, Woodcock CM (1998) Insect supersense: mate and host location by insects as model systems for exploiting olfactory interactions. Biochemist 20:8–13

    CAS  Google Scholar 

  • Pow EM, Bennison JA, Birkett MA, Luszniak MJ, Manjunatha M, Pickett JA, Segers IS, Wadhams LJ, Wardlow LR, Woodcock CM (1999) Behavioural responses of western flower thrips (Frankliniella occidentalis) to host plant volatiles. In: Vierbergen G, Tune 1 (eds) Proceedings sixth international symposium on thysanoptera, Akdeniz University, Antalya, Turkey, April 27–May 1, 1988, pp 121–128

  • Reisenman CE, Riffell JA, Duffy K, Pesque A, Mikles D, Goodwin B (2013) Species-specific effects of herbivory on the oviposition behavior of the moth Manduca sexta. J Chem Ecol 39:76–89

    Article  CAS  PubMed  Google Scholar 

  • Robert CA, Erb M, Duployer M, Zwahlen C, Doyen GR, Turlings TC (2012) Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytol 194(4):1061–1069

    Article  CAS  PubMed  Google Scholar 

  • Stamps JA, Krishnan VV (2005) Nonintuitive cue use in habitat selection. Ecology 86:2860–2867

    Article  Google Scholar 

  • Stamps JA, Krishnan VV, Reid ML (2005) Search costs and habitat selection by dispersers. Ecology 86:510–518

    Article  Google Scholar 

  • Sugimoto K, Matsui K, Iijima Y, Akakabe Y, Muramoto S, Ozawa R, Uefune M, Sasaki R, Alamgir KM, Akitake S, Nobuke T, Galis I, Aoki K, Shibata D, Takabayashi J (2014) Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense. Proc Natl Acad Sci USA 111(19):7144–7149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JN, Pellmyr O (1991) Evolution of oviposition behaviour and host preferences in Lepidoptera. Annu Rev Entomol 65:65–89

    Article  Google Scholar 

  • Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253

    Article  CAS  PubMed  Google Scholar 

  • Ulland S (2007) Functional characterization of olfactory receptor neurons in the cabbage moth Mammestra brassicae L (Lepidoptera: Noctuidae) Gas chromatography linked to single cell recordings and mass spectrometry Doctoral thesis submitted to Norwegian University of Science and Technology

  • Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485

    Article  CAS  PubMed  Google Scholar 

  • Visser JH (1986) Host odor perception in phytophagous insects. Annu Rev Entomol 31:121–144

    Article  Google Scholar 

  • Visser JH (1988) Host-plant finding by insects: orientation sensory input and search patterns. J Insect Physiol 34:259–268

    Article  Google Scholar 

  • War AR, Sharma HC, Paulraj MG, War MY, Ignacimuthu S (2011) Herbivore induced plant volatiles—their role in plant defense for pest management. Plant Signal Behav 6(12):1973–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webster B, Bruce TJA, Hardie J, Pickett JA (2010) Volatiles functioning as host cues in a blend become non-host cues when presented alone to the black bean aphid. Anim Behav 79:451–457

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by Grants from the Indian Council for Agricultural Research [ICAR] through National Fellow Project.

Author information

Authors and Affiliations

  1. Department of Entomology, University of Agricultural Sciences, GKVK, Bangalore, 560 065, India

    Subhash Shivaramu

  2. National Fellow Laboratory, Division of Entomology and Nematology, ICAR-Indian Institute of Horticultural Research, Hesseraghatta, Bangalore, 560 089, India

    Pagadala Damodaram Kamala Jayanthi, Vivek Kempraj & Akshay Kumar Chakravarty

  3. Division of Insect Ecology, ICAR-National Bureau of Agricultural Important Resources, Hebbal, Bangalore, 560 031, India

    Raghavendra Anjinappa & Bakthavatsalam Nandagopal

Authors
  1. Subhash Shivaramu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pagadala Damodaram Kamala Jayanthi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vivek Kempraj
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Raghavendra Anjinappa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bakthavatsalam Nandagopal
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Akshay Kumar Chakravarty
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pagadala Damodaram Kamala Jayanthi.

Additional information

Handling Editor: Jarmo Holopainen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (EPS 217 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shivaramu, S., Jayanthi, P.D.K., Kempraj, V. et al. What signals do herbivore-induced plant volatiles provide conspecific herbivores?. Arthropod-Plant Interactions 11, 815–823 (2017). https://doi.org/10.1007/s11829-017-9536-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-017-9536-2

Keywords

Search

Navigation