Arthropod-Plant Interactions

, Volume 11, Issue 2, pp 121–131 | Cite as

Olfactory response of the zoophytophagous mirid Nesidiocoris tenuis to tomato and alternative host plants

  • Mario Naselli
  • Lucia Zappalà
  • Antonio Gugliuzzo
  • Giovanna Tropea Garzia
  • Antonio Biondi
  • Carmelo Rapisarda
  • Fabrizio Cincotta
  • Concetta Condurso
  • Antonella Verzera
  • Gaetano SiscaroEmail author
Original Paper


It has been proved that the omnivorous predator Nesidiocoris tenuis (Hemiptera: Miridae) is attracted to and can develop successfully on sesame (Sesamum indicum). In this study, the potential of this plant, compared with Dittrichia viscosa and tomato (Solanum lycopersicum), to attract the mirid bug was assessed. A Y-tube olfactometer was used to test the olfactory preference of the mirid in dual-choice bioassays comparing healthy tomato, S. indicum, and D. viscosa plants, and tomato plants infested by eggs and larvae of Tuta absoluta (Lepidoptera: Gelechiidae). To understand the biochemical basis of the attraction of the omnivorous predator toward the alternative plants, headspace solid-phase microextraction combined with gas chromatography–mass spectrometry was performed, with the aim of identifying potential volatiles responsible for mirid attraction. S. indicum was the most attractive plant; T. absoluta infestation did not significantly increase N. tenuis attraction. We identified 57 volatiles belonging to the classes of hydrocarbon and oxygenated monoterpenes, sesquiterpenes, C13-norisoprenoids, aliphatic aldehydes, esters, alcohols, and hydrocarbons. Sesame plants emitted the lowest amount of hydrocarbon monoterpenes but a higher rate of oxygenated terpenes. Green leaf volatiles, known for attracting mirids, were emitted at higher levels by sesame plants, whereas tomato plants infested by T. absoluta larvae showed the highest levels of monoterpene hydrocarbons. The potential applications of plant volatiles in integrated management of tomato pests are discussed in the framework of mirid ecology.


Plant volatiles HS-SPME–GC-MS Olfactometer Generalist predator Functional biodiversity Banker plant 



This research was partially funded by the Italian Ministry of Education, University and Research (PRIN project “Insects and globalization: sustainable control of exotic species in agro-forestry ecosystems” GEISCA, 2010CXXHJE_004). The PhD of M.N. was funded by a grant from the University of Catania.


  1. Abbas S, Perez-Hedo M, Colazza S, Urbaneja A (2014) The predatory mirid Dicyphus maroccanus as a new potential biological control agent in tomato crops. Biocontrol 59:565–574CrossRefGoogle Scholar
  2. Abbes K, Biondi A, Kurtulus A, Ricupero M, Russo A, Siscaro G, Chermiti B, Zappala L (2015) Combined non-target effects of insecticide and high temperatures on the parasitoid Bracon nigricans. PLoS ONE 10(9):e0138411CrossRefPubMedPubMedCentralGoogle Scholar
  3. Agrawal AA, Klein CN (2000) What omnivores eat: direct effects of induced plant resistance on herbivores and indirect consequences for diet selection by omnivores. J Anim Ecol 69:525–535CrossRefGoogle Scholar
  4. Ahirwar RM, Gupta MP, Banerjee S (2010) Field efficacy of natural and indigenous products on sucking pests of sesame. Indian J Nat Prod Resour 1:221–226Google Scholar
  5. Allmann S, Baldwin IT (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329:1075–1078CrossRefPubMedGoogle Scholar
  6. Alomar O, Goula M, Albajes R (2002) Colonisation of tomato fields by predatory mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agric Ecosyst Environ 89(1–2):105–115CrossRefGoogle Scholar
  7. Anastasaki E, Balayannis G, Papanikolaou NE, Michaelakis AN, Milonas PG (2015) Oviposition induced volatiles in tomato plants. Phytochem Lett 13:262–266CrossRefGoogle Scholar
  8. Besser K, Harper A, Welsby N, Schauvinhold I, Slocombe S, Li Y, Dixon RA, Broun P (2009) Divergent regulation of terpenoid metabolism in the trichomes of wild and cultivated tomato species. Plant Physiol 149:499–514CrossRefPubMedPubMedCentralGoogle Scholar
  9. Biondi A, Mommaerts V, Smagghe G, Vinuela E, Zappalà L, Desneux N (2012) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68:1523–1536CrossRefPubMedGoogle Scholar
  10. Biondi A, Zappalà L, Stark JD, Desneux N (2013a) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8(9):e76548. doi: 10.1371/journal.pone.0076548 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Biondi A, Chaillieux A, Lambion J, Han P, Zappalà L, Desneux N (2013b) Indigenous natural enemies attacking Tuta absoluta (Lepidoptera: Gelechiidae) in southern France. Egypt J Biol Pest Control 23:117–121Google Scholar
  12. Biondi A, Desneux N, Amiens-Desneux E, Siscaro G, Zappalà L (2013c) Biology and developmental strategies of the Palaearctic parasitoid Bracon nigricans (Hymenoptera: Braconidae) on the Neotropical moth Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 106:1638–1647CrossRefPubMedGoogle Scholar
  13. Biondi A, Zappalà L, Desneux N, Aparo A, Siscaro G, Rapisarda C, Martin T, Tropea Garzia G (2015) Potential toxicity of α-cypermethrin-treated net on Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 108(3):1191–1197CrossRefPubMedGoogle Scholar
  14. Biondi A, Zappalà L, Di Mauro A, Tropea Garzia G, Russo A, Desneux N, Siscaro G (2016) Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis? Biocontrol 61:79–90CrossRefGoogle Scholar
  15. Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol 55:433–440CrossRefGoogle Scholar
  16. Bonaventure G, Van Doorn A, Baldwin IT (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci 16(6):294–299CrossRefPubMedGoogle Scholar
  17. Bruessow F, Gouhier-Darimont C, Buchala A, Metraux JP, Reymond P (2010) Insect eggs suppress plant defence against chewing herbivores. Plant J 62(5):876–885CrossRefPubMedGoogle Scholar
  18. Bukovinszky T, Gols R, Posthumus MA, Vet LEM, Van Lenteren JC (2005) Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellen). J Chem Ecol 31(3):461–480CrossRefPubMedGoogle Scholar
  19. Calvo FJ, Soriano J, Bolckmans K, Belda JE (2012) A successful method for whitefly and Tuta absoluta control in tomato. Evaluation after two years of application in practice. IOBC/WPRS Bull 80:237–244Google Scholar
  20. Campos MR, Silva TB, Silva WM, Silva JE, Siqueira HA (2015) Spinosyn resistance in the tomato borer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J Pest Sci 88:405–412CrossRefGoogle Scholar
  21. Cano M, Vila E, Janssen D, Bretones G, Salvador E, Lara L, Tellez M (2009) Selection of refuges for Nesidiocoris tenuis (Het.: Miridae) and Orius laevigatus (Het.: Anthocoridae): virus reservoir risk assessment. IOBC/WPRS Bull 49:281–286Google Scholar
  22. Castañé C, Arnó J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29CrossRefGoogle Scholar
  23. De Backer L, Caparros Megido R, Haubruge E, Verheggen F (2014) Macrolophus pygmaeus (Rambur) as an efficient predator of the tomato leafminer Tuta absoluta (Meyrick) in Europe. A review. Biotechnol Agron Soc Environ 18:536–543Google Scholar
  24. De Backer L, Caparros Megido R, Fauconnier ML, Brostaux Y, Francis F, Verheggen F (2015) Tuta absoluta-induced plant volatiles: attractiveness towards the generalist predator Macrolophus pygmaeus. Arthropod Plant Interact 9(5):465–476CrossRefGoogle Scholar
  25. De Backer L, Bawin T, Schott M, Gillard L, Markó IE, Francis F, Verheggen F (2016) Betraying its presence: identification of the chemical signal released by Tuta absoluta-infested tomato plants that guide generalist predators toward their prey. Arthropod Plant Interact. doi: 10.1007/s11829-016-9471-7 Google Scholar
  26. De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Métraux JP, Van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18(9):923–937CrossRefPubMedGoogle Scholar
  27. Desneux N, Wajinberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narvaez-Vasquez CA, Gonzalez-Cabrera J, Catalan Ruescas D, Tabone E, Frandon J (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215CrossRefGoogle Scholar
  28. Dicke M (2009) Behavioural and community ecology of plants that cry for help. Plant, Cell Environ 32:654–665CrossRefGoogle Scholar
  29. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175CrossRefPubMedGoogle Scholar
  30. Dicke M, Sabelis MW (1988) How plants obtain predatory mites as bodyguards. Neth J Zool 38:148–165CrossRefGoogle Scholar
  31. Fatouros NE, Lucas-Barbosa D, Weldegergis BT, Pashalidou FG, van Loon JJA et al (2012) Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS ONE 7(8):e43607. doi: 10.1371/journal.pone.0043607 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Gols R, Bullock JM, Dicke M, Bukovinszky T, Harvey JA (2011) Smelling the wood from the trees: non-linear parasitoid responses to volatile attractants produced by wild and cultivated cabbage. J Chem Ecol 37(8):795–807CrossRefPubMedPubMedCentralGoogle Scholar
  33. Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT (2008) Shared signals—‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol Lett 11:24–34PubMedGoogle Scholar
  34. Hassan MN, Zainal Z, Ismail I (2015) Green leaf volatiles: biosynthesis, biological functions and their applications in biotechnology. Plant Biotechnol J 13:727–739CrossRefGoogle Scholar
  35. Ingegno BL, Pansa MG, Tavella L (2011) Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biol Control 58:174–181CrossRefGoogle Scholar
  36. Ingegno BL, Ferracini C, Gallinotti D, Alma A, Tavella L (2013) Evaluation of the effectiveness of Dicyphus errans (Wolff) as predator of Tuta absoluta (Meyrick). Biol Control 67:246–252CrossRefGoogle Scholar
  37. Ingegno BL, La-Spina M, Jordan MJ, Tavella L, Sanchez JA (2016) Host plant perception and selection in the sibling species Macrolophus melanotoma and Macrolophus pygmaeus (Hemiptera: Miridae). J Insect Behav. doi: 10.1007/s10905-016-9549-1 Google Scholar
  38. Kang JH, Shi F, Jones AD, Marks MD, Howe GA (2010) Distortion of trichome morphology by the hairless mutation of tomato affects leaf surface chemistry. J Exp Bot 61:1053–1064CrossRefPubMedGoogle Scholar
  39. Lins JCJ, van Loon JJA, Bueno VHP, Lucas-Barbosa D, Dicke M, van Lenteren JC (2014) Response of the zoophytophagous predators Macrolophus pygmaeus and Nesidiocoris tenuis to volatiles of uninfested plants and to plants infested by prey or conspecifics. Biocontrol 59(6):707–718CrossRefGoogle Scholar
  40. McGregor RR, Gillespie DR (2004) Olfactory responses of the omnivorous generalist predator Dicyphus hesperus to plant and prey odours. Entomol Exp Appl 112:201–205CrossRefGoogle Scholar
  41. Mollá O, Gonzalez-Cabrera J, Urbaneja A (2011) The combined use of Bacillus thuringiensis and Nesidiocoris tenuis against the tomato borer Tuta absoluta. Biocontrol 56(6):883–891CrossRefGoogle Scholar
  42. Mollá O, Biondi A, Alonso-Valiente M, Urbaneja A (2014) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. Biocontrol 59:175–183CrossRefGoogle Scholar
  43. Nakaishi K, Fukui Y, Arakawa R (2011) Reproduction of Nesidiocoris tenuis (Reuter) on sesame. J Appl Entomol Zool 55:199–205CrossRefGoogle Scholar
  44. Naselli M, Urbaneja A, Siscaro G, Jaques JA, Zappalà L, Flors V, Pérez-Hedo M (2016) Stage-related defense response induction in tomato plants by Nesidiocoris tenuis. Int J Mol Sci 17:1210. doi: 10.3390/ijms17081210 CrossRefPubMedCentralGoogle Scholar
  45. Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101:372CrossRefPubMedGoogle Scholar
  46. Pan H et al (2015) Volatile fragrances associated with flowers mediate host plant alternation of a polyphagous mirid bug. Sci Rep 5:14805. doi: 10.1038/srep14805 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Parolin P, Bresch C, Poncet C, Desneux N (2014) Introducing the term ‘Biocontrol Plants’ for integrated pest management. Sci Agric 71:77–80CrossRefGoogle Scholar
  48. Perdikis D, Arvaniti K (2016) Nymphal development on plant vs. leaf with and without prey for two omnivorous predators: Nesidiocoris tenuis (Reuter, 1895) (Hemiptera: Miridae) and Dicyphus errans (Wolff, 1804) (Hemiptera: Miridae). Entomol Gen 35:297–306CrossRefGoogle Scholar
  49. Perdikis D, Favas C, Lykouressis D, Fantinou A (2007) Ecological relationships between non cultivated plants and insect predators in agroecosystems: the case of Dittrichia viscosa (Asteraceae) and Macrolophus melanotoma (Hemiptera: Miridae). Acta Oecol 31:299–306CrossRefGoogle Scholar
  50. Pérez-Alonso MJ, Velasco-Negueruela A, Duru ME, Harmandar M, García Vallejo MC (1996) Composition of the volatile oil from the aerial parts of Inula viscosa (L.) Aiton. Flavour Fragr J 11:349–351CrossRefGoogle Scholar
  51. Pérez-Hedo M, Urbaneja A (2015) Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci 88:65–73CrossRefGoogle Scholar
  52. Pérez-Hedo M, Urbaneja-Bernat P, Jaques JA, Urbaneja A (2015) Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants. J Pest Sci 88:543–554CrossRefGoogle Scholar
  53. Ponzio C, Gols R, Pieterse CMJ, Dicke M (2013) Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Funct Ecol 27:587–598CrossRefGoogle Scholar
  54. Roditakis E, Vasakis E, Grispou M, Stavrakaki M, Nauen R, Gravouil M, Bassi A (2015) First report of Tuta absoluta resistance to diamide insecticides. J Pest Sci 88:9–16CrossRefGoogle Scholar
  55. Sánchez JA, Lacasa A (2008) Impact of the zoophytophagous plant bug Nesidiocoris tenuis (Heteroptera: Miridae) on tomato yield. J Econ Entomol 101(6):1864–1870CrossRefPubMedGoogle Scholar
  56. Sugiura S, Yamazaki K (2006) Consequences of scavenging behaviour in a plant bug associated with a glandular plant. Biol J Linn Soc 88:593–602CrossRefGoogle Scholar
  57. Thaler JS, Farag MA, Paré PW, Dicke M (2002) Jasmonate deficient plants have reduced direct and indirect defences against herbivores. Ecol Lett 5(6):764–774CrossRefGoogle Scholar
  58. Tropea Garzia G, Siscaro G, Biondi A, Zappalà L (2012) Tuta absoluta, an exotic invasive pest from South America now in the EPPO region: biology, distribution and damage. Bull EPPO 42:205–210CrossRefGoogle Scholar
  59. Urbaneja A, Gonzalez-Cabrera J, Arno J, Gabarra R (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Manag Sci 68:1215–1222CrossRefPubMedGoogle Scholar
  60. van Damme V, Berkvens N, Moerkens R, Berckmoes E, Wittemans L et al (2015) Overwintering potential of the invasive leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) as a pest in greenhouse tomato production in Western Europe. J Pest Sci 88(3):533–541CrossRefGoogle Scholar
  61. Wang Y, Kays SJ (2002) Sweetpotato volatile chemistry in relation to sweet potato weevil (Cylas formicarius) behavior. J Am Soc Hortic Sci 127:656–662Google Scholar
  62. Wheeler AG Jr, Krimmel BA (2015) Mirid (Hemiptera: Heteroptera) specialists of sticky plants: adaptations, interactions, and ecological implications. Annu Rev Entomol 60:393–414CrossRefPubMedGoogle Scholar
  63. Williams L III, Blackmer JL, Rodriguez-Saona C, Zhu S (2010) Plant volatiles influence electrophysiological and behavioral responses of Lygus hesperus. J Chem Ecol 36:467–478CrossRefPubMedGoogle Scholar
  64. Zappalà L, Siscaro G, Biondi A, Mollá O, Gonzalez-Cabrera J, Urbaneja A (2012a) Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. J Appl Entomol 136:401–409CrossRefGoogle Scholar
  65. Zappalà L, Bernardo U, Biondi A, Cocco A, Deliperi S, Delrio G, Giorgini M, Pedata P, Rapisarda C, Tropea Garzia G, Siscaro G (2012b) Recruitment of native parasitoids by the exotic pest Tuta absoluta in Southern Italy. Bull Insectol 65(1):51–61Google Scholar
  66. Zappalà L, Biondi A, Alma A, Al-Jboory IJ, Arnó J et al (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle-East, and their potential use in pest control strategies. J Pest Sci 86:635–647CrossRefGoogle Scholar
  67. Zhu P, Lu Z, Heong K, Chen G, Zheng X et al (2014) Selection of nectar plants for use in ecological engineering to promote biological control of rice pests by the predatory bug, Cyrtorhinus lividipennis, (Heteroptera: Miridae). PLoS ONE 9(9):e108669CrossRefPubMedPubMedCentralGoogle Scholar
  68. Zohreh S, Fatemeh Y, Arash R, Zandi SN (2016) Functional responses of Orius albidipennis Reuter (Hemiptera, Anthocoridae) to Tuta absoluta Meyrick (Lepidoptera, Gelechiidae) on two tomato cultivars with different leaf morphological characteristics. Entomol Gen 36:127–136CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Mario Naselli
    • 1
  • Lucia Zappalà
    • 1
  • Antonio Gugliuzzo
    • 1
  • Giovanna Tropea Garzia
    • 1
  • Antonio Biondi
    • 1
  • Carmelo Rapisarda
    • 1
  • Fabrizio Cincotta
    • 2
  • Concetta Condurso
    • 3
  • Antonella Verzera
    • 2
  • Gaetano Siscaro
    • 1
    Email author
  1. 1.Department of Agriculture, Food and Environment (Di3A)University of CataniaCataniaItaly
  2. 2.Department of Veterinary ScienceUniversity of MessinaMessinaItaly
  3. 3.Department of Chemical, Biological, Pharmaceutical and Environmental ScienceUniversity of MessinaMessinaItaly

Personalised recommendations