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Journal of Chemical Ecology

, Volume 44, Issue 3, pp 288–298 | Cite as

Electrophysiological and Oviposition Responses of Tuta absoluta Females to Herbivore-Induced Volatiles in Tomato Plants

  • Eirini Anastasaki
  • Fryni Drizou
  • Panagiotis G. Milonas
Article

Abstract

In response to attack by herbivorous insects, plants produce semiochemicals for intra- and interspecific communication. The perception of these semiochemicals by conspecifics of the herbivore defines their choice for oviposition and feeding. We aimed to investigate the role of herbivore-induced plant volatiles (HIPVs) by Tuta absoluta larvae on the oviposition choice of conspecific females on tomato plants. We performed two- choice and non-choice bioassays with plants damaged by larvae feeding and intact control plants. We also collected headspace volatiles of those plants and tested the response of female antennae on those blends with Gas Chromatography- Electro-Antennographical Detection (GC-EAD). In total 55 compounds were collected from the headspace of T. absoluta larvae-infested plants. Our results show that female moths preferred to oviposit on intact control plants instead of damaged ones. Herbivory induced the emission of hexanal, (Ζ)-3-hexen-1-ol, (E)-β-ocimene, linalool, (Z)-3-hexenyl butanoate, methyl salicylate, indole, nerolidol, guaidiene-6,9, β-pinene, β-myrcene, α-terpinene, hexenyl hexanoate, β-elemene, β-caryophyllene and (Ε-Ε)- 4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), one unidentified sesquiterpene and three unknown compounds. In Electroantennographic (EAG) assays, the antennae of T. absoluta females responded to hexanal, (Ζ)-3-hexen-1-ol, methyl salicylate and indole. The antennae of T. absoluta females exhibited a dose-response in EAG studies with authentic samples. Strong EAG responses were obtained for compounds induced on damaged tomato plants, as well as in nonanal, a compound emitted by both infested and control plants. These compounds could be utilized in integrated pest management of T. absoluta.

Keywords

Oviposition Volatiles Tomato GC-EAD Host plant preference Tomato leaf miner 

Notes

Acknowledgements

We would like to thank two anonymous reviewers and the handling editor for their valuable comments that considerably improve the manuscript. We also thank Apostolos Kapranas for his comments and English language editing.

Funding

The present study was funded by the General Secretariat Research and Technology of the Greek Ministry of Education within the action “EXCELLENCE II” under the Operational Programme “Education and Lifelong Learning” 2007–2013 that is co-funded by the European Social Fund and National funds.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Adams R (2007) Identification of essential oil components by gas-chromatography/mass spectrometry, 4th edn. Allured Business Media, IllinoisGoogle Scholar
  2. Allmann S et al (2013) Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition. elife 2:e00421.  https://doi.org/10.7554/eLife.00421 PubMedPubMedCentralGoogle Scholar
  3. Anastasaki E, Balayannis G, Papanikolaou NE, Michaelakis AN, Milonas PG (2015) Oviposition induced volatiles in tomato plants. Phytochem Lett 13:262–266.  https://doi.org/10.1016/j.phytol.2015.07.007 CrossRefGoogle Scholar
  4. Angeles Lopez YI, Martinez-Gallardo NA, Ramirez-Romero R, Lopez MG, Sanchez-Hernandez C, Delano-Frier JP (2012) Cross-kingdom effects of plant-plant signaling via volatile organic compounds emitted by tomato (Solanum lycopersicum) plants infested by the greenhouse whitefly (Trialeurodes vaporariorum). J Chem Ecol 38:1376–1386.  https://doi.org/10.1007/s10886-012-0201-z CrossRefPubMedGoogle Scholar
  5. Ataide LMS, Arce CCM, Curtinhas JN, da Silva DJH, DeSouza O, Lima E (2017) Flight behavior and oviposition of Tuta absoluta on susceptible and resistant genotypes of Solanum lycopersicum. Arthropod-Plant Inte 11:567–575.  https://doi.org/10.1007/s11829-017-9500-1 CrossRefGoogle Scholar
  6. Awmark C, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844CrossRefGoogle Scholar
  7. Bawin T, De Backer L, Dujeu D, Legrand P, Megido RC, Francis F, Verheggen FJ (2014) Infestation level influences oviposition site selection in the tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae). Insects 5:877–884.  https://doi.org/10.3390/insects5040877 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bawin T, Collard F, De Backer L, Yarou BB, Compere P, Francis F, Verheggen FJ (2017) Structure and distribution of the sensilla on the antennae of Tuta absoluta (Lepidoptera: Gelechiidae). Micron 96:16–28.  https://doi.org/10.1016/j.micron.2017.01.008 CrossRefPubMedGoogle Scholar
  9. Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, worldwide wpread and management of the invasive south American tomato pinworm, Tuta absoluta: past, present, and future. Annu Rev Entomol 63.  https://doi.org/10.1146/annurev-ento-031616-034933
  10. Birkett MA et al (2000) New roles for cis-jasmone as an insect semiochemical and in plant defense. P Natl Acad Sci USA 97:9329–9334CrossRefGoogle Scholar
  11. Bruce TJ, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274.  https://doi.org/10.1016/j.tplants.2005.04.003 CrossRefPubMedGoogle Scholar
  12. Caparros Megido R et al (2014) Role of larval host plant experience and solanaceous plant volatile emissions in Tuta absoluta (Lepidoptera: Gelechiidae) host finding behavior. Arthropod-Plant Inte.  https://doi.org/10.1007/s11829-014-9315-2
  13. Cook SM, Khan ZR, Pickett JA (2007) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400CrossRefPubMedGoogle Scholar
  14. Copolovici L, Kännaste A, Pazouki L, Niinemets U (2012) Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J Plant Physiol 169:664–672.  https://doi.org/10.1016/j.jplph.2011.12.019 CrossRefPubMedGoogle Scholar
  15. De Backer L, Megido RC, Fauconnier M-L, Brostaux Y, Francis F, Verheggen F (2015) Tuta absoluta-induced plant volatiles: attractiveness towards the generalist predator Macrolophus pygmaeus. Arthropod-Plant Inter 9:465–476.  https://doi.org/10.1007/s11829-015-9388-6 CrossRefGoogle Scholar
  16. De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel nonspecific females. Nature 410:577–580CrossRefPubMedGoogle Scholar
  17. Dicke M (2000) Chemical ecology of host plant selection by herbivorous arhtopods: a multitrophic perpective. Biochem Syst Ecol 28:601–617CrossRefPubMedGoogle Scholar
  18. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. Trends Plant Sci 15:167–175.  https://doi.org/10.1016/j.tplants.2009.12.002 CrossRefPubMedGoogle Scholar
  19. Dicke M, van Poecke RMP, de Boer JG (2003) Inducible indirect defence of plants: from mechanisms to ecological functions. Basic Appl Ecol 4:27–42.  https://doi.org/10.1078/1439-1791-00131 CrossRefGoogle Scholar
  20. Erb M, Veyrat N, Robert CA, Xu H, Frey M, Ton J, Turlings TC (2015) Indole is an essential herbivore-induced volatile priming signal in maize. Nat Commun 6:6273.  https://doi.org/10.1038/ncomms7273 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fatouros NE et al (2012) Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS One 7:e43607.  https://doi.org/10.1371/journal.pone.0043607 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fatouros NE, Cusumano A, Danchin EGJ, Colazza S (2016) Prospects of herbivore egg-killing plant defenses for sustainable crop protection. Ecol Evol 6:6906–6918.  https://doi.org/10.1002/ece3.2365 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Furtado FB et al (2014) Seasonal variation of the chemical composition and antimicrobial and cytotoxic activities of the essential oils from Inga laurina (Sw.) Willd. Molecules 19:4560–4577.  https://doi.org/10.3390/molecules19044560 CrossRefPubMedGoogle Scholar
  24. Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecol Lett 13.  https://doi.org/10.1111/j.1461-0248.2009.01433.x
  25. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61.  https://doi.org/10.1111/j.1469-8137.2007.02330.x CrossRefPubMedGoogle Scholar
  26. 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
  27. IOFI (2011) Guidelines for the quantitative gas chromatography of volatile flavouring substances, from the working group on Methods of analysis of the International Organization of the Flavor Industry (IOFI). Flavour Frag J 26:297–299.  https://doi.org/10.1002/ffj.2061 Google Scholar
  28. Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135:483–495.  https://doi.org/10.1104/pp.103.038315 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Karban R (2011) The ecology and evolution of induced resistance against herbivores. Funct Ecol 25:339–347.  https://doi.org/10.1111/j.1365-2435.2010.01789.x CrossRefGoogle Scholar
  30. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144.  https://doi.org/10.1126/science.291.5511.2141 CrossRefPubMedGoogle Scholar
  31. Khan ZR, James DG, Midega CAO, Pickett JA (2008) Chemical ecology and conservation biological control. Biol Control 45:210–224.  https://doi.org/10.1016/j.biocontrol.2007.11.009 CrossRefGoogle Scholar
  32. Pashalidou FG, Lucas-Barbosa D, van Loon JJA, Dicke M, Fatouros NE (2013) Phenotypic plasticity of plant response to herbivore eggs: effects on resistance to caterpillars and plant development. Ecology 94:702–713CrossRefPubMedGoogle Scholar
  33. Pereyra PC, Sánchez NE (2006) Effect of two solanaceous plants on developmental and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 35:565–574CrossRefGoogle Scholar
  34. Pinto-Zevallos DM, Strapasson P, Zarbin PHG (2016) Herbivore-induced volatile organic compounds emitted by maize: electrophysiological responses in Spodoptera frugiperda females. Phytochem Lett 16:70–74.  https://doi.org/10.1016/j.phytol.2016.03.005 CrossRefGoogle Scholar
  35. Poelman EH, Broekgaarden C, van Loon JJA, Dicke M (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 17:3352–3365.  https://doi.org/10.1111/j.1365-294X.2008.03838.x CrossRefPubMedGoogle Scholar
  36. Ponzio C et al (2016) Volatile-mediated foraging behaviour of three parasitoid species under conditions of dual insect herbivore attack. Anim Behav 111:197–206.  https://doi.org/10.1016/j.anbehav.2015.10.024 CrossRefGoogle Scholar
  37. Proffit M, Birgersson G, Bengtsson M, Reis R Jr, Witzgall P, Lima E (2011) Attraction and oviposition of Tuta absoluta females in response to tomato leaf volatiles. J Chem Ecol 37:565–574.  https://doi.org/10.1007/s10886-011-9961-0 CrossRefPubMedGoogle Scholar
  38. Raitanen J, Forsman JT, Kivela SM, Maenpaa MI, Valimaki P (2014) Attraction to conspecific eggs may guide oviposition site selection in a solitary insect. Behav Ecol 25:110–116.  https://doi.org/10.1093/beheco/art092 CrossRefGoogle Scholar
  39. 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.  https://doi.org/10.1007/s10886-012-0228-1 CrossRefPubMedGoogle Scholar
  40. Renwick JAA, Chew FS (1994) Species-specific effects of herbivory on the oviposition behavior of the moth Manduca sexta. J Chem Ecol 39:377–400Google Scholar
  41. Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC (2013) Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens. Int J Mol Sci 14:17781–17811.  https://doi.org/10.3390/ijms140917781 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Shiojiri K, Takabayashi J, Yano S, Takafuji A (2002) Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecol Lett 5:186–192CrossRefGoogle Scholar
  43. Silva DB, Bueno VHP, Lins JC Jr, van Lenteren JC (2015) Life history data and population growth of Tuta absoluta at constant and alternating temperatures on two tomato lines. B Instectol 68:223–232Google Scholar
  44. Silva DB, Weldegergis BT, Van Loon JJ, Bueno VH (2017) Qualitative and quantitative differences in herbivore-induced plant volatile blends from tomato plants infested by either Tuta absoluta or Bemisia tabaci. J Chem Ecol 43:53–65.  https://doi.org/10.1007/s10886-016-0807-7 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Smith RM, Marshall JA, Davey MR, Lowe KC, Power JB (1996) Comparison of volatiles and waxes in leaves of genetically engineered tomatoes. Phytochemistry 43:753–758CrossRefGoogle Scholar
  46. Sokal RR, Rohlf FJ (2012) Biometry: the principles and practice of statistics in biological research. 4 edn. W. H. Freeman and Co, New YorkGoogle Scholar
  47. Song C, Lai WC, Reddy KM, Wei B (2003) Temperature-programmed retention indices for GC and GC-MS of hydrocarbon fuels and simulateddistillation of GC of heavy oils. In: Hsu CS (ed) Analytical advances for hydrocarbon research, 1st edn. Springer Science & Business Media, New York, pp 147–210CrossRefGoogle Scholar
  48. Stenberg JA, Heil M, Åhman I, Björkman C (2015) Optimizing crops for biocontrol of pests and disease. Trends Plant Sci 20:698–712.  https://doi.org/10.1016/j.tplants.2015.08.007 CrossRefPubMedGoogle Scholar
  49. Strapasson P, Pinto-Zevallos DM, Paudel S, Rajotte EG, Felton GW, Zarbin PH (2014) Enhancing plant resistance at the seed stage: low concentrations of methyl jasmonate reduce the performance of the leaf miner Tuta absoluta but do not alter the behavior of its predator Chrysoperla externa. J Chem Ecol 40:1090–1098.  https://doi.org/10.1007/s10886-014-0503-4 CrossRefPubMedGoogle Scholar
  50. Teles Pontes WJ, Lima ER, Cunha EG, TDA PM, Lôbo AP, Barros R (2010) Physical and chemical cues affect oviposition by Neoleucinodes elegantalis. Physiol Entomol 35:134–139.  https://doi.org/10.1111/j.1365-3032.2010.00720.x CrossRefGoogle Scholar
  51. Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol exp appl 47:3–14CrossRefGoogle Scholar
  52. Ulland S, Ian E, Mozuraitis R, Borg-Karlson AK, Meadow R, Mustaparta H (2008) Methyl salicylate, identified as primary odorant of a specific receptor neuron type, inhibits oviposition by the moth Mamestra brassicae L. (Lepidoptera, noctuidae). Chem Senses 33:35–46.  https://doi.org/10.1093/chemse/bjm061 CrossRefPubMedGoogle Scholar
  53. Zhuang X, Fiesselmann A, Zhao N, Chen H, Frey M, Chen F (2012) Biosynthesis and emission of insect herbivory-induced volatile indole in rice. Phytochemistry 73:15–22.  https://doi.org/10.1016/j.phytochem.2011.08.029 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Biological Control, Department of EntomologyBenaki Phytopathological InstituteKifissiaGreece
  2. 2.Division of Plant and Crop Sciences, School of BiosciencesThe University of NottinghamLoughboroughUK

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