Advertisement

Relative importance of host and plant semiochemicals in the foraging behavior of Trichogramma achaeae, an egg parasitoid of Tuta absoluta

  • Lessando GontijoEmail author
  • Pasquale Cascone
  • Massimo Giorgini
  • Marco Michelozzi
  • Hígor S. Rodrigues
  • Giuseppe Spiezia
  • Luigi Iodice
  • Emilio Guerrieri
Original Paper
First Online:
  • 24 Downloads

Abstract

Herbivore-induced plant volatiles (HIPVs) and host sex pheromones are important semiochemicals used by natural enemies to locate prey or hosts. The egg parasitoid Trichogramma achaeae Nagaraja & Nagarkatti has recently shown potential for use as a biological control agent of Tuta absoluta (Meyrick), a key pest of tomato crops worldwide. In this study, we used olfactometer tests to examine the behavioral response of T. achaeae females to T. absoluta sex pheromone or to HIPVs produced by tomato plants infested with T. absoluta eggs or larvae. Our results showed that T. achaeae was attracted to T. absoluta sex pheromone. Parasitoids were also innately attracted to volatiles produced by tomato plants, whether uninfested or infested. However, parasitoids could not distinguish between volatiles from uninfested or T. absoluta-infested tomato plants. We characterized the headspace volatiles of tomato plants used in the olfactometer tests and found out that oviposition and larval feeding by T. absoluta significantly enhanced HIPV emission. This study suggests that the sex pheromone of T. absoluta is a potential tool to manipulate the behavior of T. achaeae and improve its attraction to the tomato crop. The analysis of volatiles released by tomato plants, either infested or uninfested, coupled with the response of T. achaeae in the olfactometer tests was consistent with what was expected in terms of the foraging behavior of a generalist parasitoid. The results and implications are further discussed in the context of sustainable T. absoluta management.

Keywords

Tomato South American tomato pinworm Sex pheromone Biocontrol Volatile organic compounds 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

This work has been supported by the EU FP7 project ‘Ameliorating the Sustainable Control of Invasive Insects’ (PIRSES 318246). The work was also supported by ‘Fundação de Amparo a Pesquisa do Estado de Minas Gerais’—FAPEMIG (grant FORTIS-TCT-10254/2014). The authors would like to show their gratitude to Gabriele Cencetti (IBBR-CNR, ARCA Laboratory) for helping with GC–MS analyses.

References

  1. Ahamdi S, Poorjavad M (2018) Behavioral and biological effects of exposure to Tuta absoluta (lepidoptera: gelechiidae) sex pheromone on several Trichogramma (hymenoptera: trichogrammatidae) populations. J Econ Entomol.  https://doi.org/10.1093/jee/toy212 (in press) Google Scholar
  2. Alsaedi G, Ashouri A, Talaei-Hassanloui R (2016) Behavioral responses of the three Trichogramma species to different odor sources. J Entomol Zool Stud 4(4):1924Google Scholar
  3. Anastasaki E, Drizou F, Milonas PG (2018) Electrophysiological and oviposition responses of Tuta absoluta females to herbivore-induced volatiles in tomato plants. J Chem Ecol.  https://doi.org/10.1007/s10886-018-0929-1 Google Scholar
  4. Arakaki N, Wakamura S, Yasuda T (1996) Phoretic egg parasitoid, Telenomus euproctidis (Hymenoptera: Scelionidae), uses sex pheromone of tussock moth Euproctis taiwana (Lepidoptera: Lymantriidae) as a kairomone. J Chem Ecol 22:1079–1085CrossRefGoogle Scholar
  5. Backer LD, Megido RC, Fouconnier ML, Brostaux Y, Francis F, Verheggen F (2015) Tuta absoluta-induced plant volatiles: attractiveness towards the generalist predator Macrolophus pygmaeus. Arthropod-Plant Interact 9:465–476.  https://doi.org/10.1007/s11829-015-9388-6 CrossRefGoogle Scholar
  6. Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, worldwide spread, and management of the invasive south american tomato pinworm, Tuta absoluta: past, present, and future. Annu Rev Entomol 63:239–258CrossRefGoogle Scholar
  7. Cabello T, Gallego JR, Vila E, Soler A, del Pino M, Carnero A et al (2009) Biological control of the South American tomato pinworm, Tuta absoluta (Lepidoptera: Gelechiidae), with releases of Trichogramma achaeae (Hym.: Trichogrammatidae) in tomato greenhouses of Spain. IOBC/WPRS Bull 49:225–230Google Scholar
  8. Cabello T, Gallego JR, Fernandez FJ, Gamez M, Vila E, del Pino M, Hernandez-Suarez E (2012) Biological control strategies for the South American tomato moth (Lepidoptera: Gelechiidae) in greenhouse tomatoes. J Econ Entomol 105(6):2085–2096CrossRefGoogle Scholar
  9. Cagnotti CL, Hernández CM, Andormo AV, Viscarret M, Riquelme M, Botto EN, López SN (2016) Acceptability and suitability of Tuta absoluta eggs from irradiated parents to parasitism by Trichogramma nerudai and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Agric For Entomol 18:198–205CrossRefGoogle Scholar
  10. Campos MR, Biondi A, Adiga A, Guedes RNC, Desneux N (2017) From the Western Palaearctic region to beyond: Tuta absoluta 10 years after invading Europe. J Pest Sci 90:787–796CrossRefGoogle Scholar
  11. Cascone P, Carpenito S, Slotsbo S, Iodice L, Sørensen GJ, Holmstrup M, Guerrieri E (2015) Improving the efficiency of Trichogramma achaeae to control Tuta absoluta. Biocontrol 60:761–771CrossRefGoogle Scholar
  12. Chailleux A, Desneux N, Seguret J, Do Thi Khanh H, Maignet P, Tabone E (2012) Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS ONE 7:e48068CrossRefGoogle Scholar
  13. Chailleux A, Biondi A, Han P, Tabone E, Desneux N (2013) Suitability of the pest–plant system Tuta absoluta (Lepidoptera: Gelechiidae)—tomato for Trichogramma (Hymenoptera: Trichogrammatidae) parasitoids and insights for biological control. J Econ Entomol 106:2310–2321CrossRefGoogle Scholar
  14. Cherif A, Mansour R, Attia-Barhoumi S, Zappalà L, Grissa-Lebdi K (2018) Effectiveness of different release rates of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae) against Tuta absoluta (Lepidoptera: Gelechiidae) in protected and open field tomato crops in Tunisia. Biocontrol Sci Technol.  https://doi.org/10.1080/09583157.2018.1542485 Google Scholar
  15. Cocco A, Deliperi S, Delrio G (2013) Control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in greenhouse tomato crops using the mating disruption technique. J Appl Entomol 137:16–28CrossRefGoogle Scholar
  16. Coppola M, Cascone P, Madonna V, Di Lelio I, Esposito F, Avitabile C, Romanelli A, Guerrieri E, Vitiello A, Pennacchio F, Rao R, Corrado G (2017) Plant-to-plant communication triggered by systemin primes anti-herbivore resistance in tomato. Sci Rep.  https://doi.org/10.1038/s41598-017-15481-8 Google Scholar
  17. Degenhardt J, Kollner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621–1637CrossRefGoogle Scholar
  18. Degenhardt DC, Refi-Hind S, Stratmann JW, Lincoln DE (2010) Systemin and jasmonic acid regulate constitutive and herbivore-induced systemic volatile emissions in tomato, Solanum lycopersicum. Phytochemistry 71:2024–2037CrossRefGoogle Scholar
  19. Desneux N, Wajnberg E, Wyckhuys KAG et al (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
  20. Dicke M (1994) Local and systemic production of volatile herbivore-induced terpenoids: their role in plant-carnivore mutualism. J Plant Physiol 143:465–472CrossRefGoogle Scholar
  21. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175CrossRefGoogle Scholar
  22. Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440CrossRefGoogle Scholar
  23. El-Arnaouty SA, Pizzol J, Galal HH, Kortam MN, Afifi AI et al (2014) Assessment of two Trichogramma species for the control of Tuta absoluta in North African tomato greenhouses. Afr Entomol 22:801–809CrossRefGoogle Scholar
  24. Farag MA, Paré PW (2002) C6 green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61:545–554CrossRefGoogle Scholar
  25. Faria CA, Torres JB, Fernandes AMV, Farias AMI (2008) Parasitism of Tuta absoluta in tomato plants by Trichogramma pretiosum Riley in response to host density and plant structures. Cienc Rural 38:1504–1509CrossRefGoogle Scholar
  26. 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.  https://doi.org/10.1371/journal.pone.0043607 CrossRefGoogle Scholar
  27. Giorgini M, Guerrieri E, Cascone P, Gontijo L (2019) Current strategies and future outlook for managing the Neotropical tomato pest Tuta absoluta (Meyrick) in the Mediterranean Basin. Neotrop Entomol.  https://doi.org/10.1007/s13744-018-0636-1 Google Scholar
  28. Guedes RNC, Picanço MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bull 42:211–216CrossRefGoogle Scholar
  29. Han P, Bayram Y, Shaltiel-Harpaz L, Sohrabi F, Saji A, Esenali UT, Jalilov A, Ali A, Shashank PR, Ismoilov K, Lu ZZ, Wang S, Zhang GF, Wan FH, Biondi A, Desneux N (2019) Tuta absoluta continues to disperse in Asia: damage, ongoing management and future challenges. J Pest Sci.  https://doi.org/10.1007/s10340-018-1062-1 Google Scholar
  30. Hervé M (2017) RVAideMemoire: testing and plotting procedures for biostatistics. https://CRAN.R-project.org/package=RVAideMemoire. Accessed 2 Aug 2018
  31. Hilker M, Meiners T (2011) Plants and insect eggs: how do they affect each other? Phytochemistry 72:1612–1623CrossRefGoogle Scholar
  32. Huigens ME, Woelk JB, Pashalidou FG, Bukovinszky T, Smid HM, Fatouros NE (2010) Chemical espionage on species-specific butterfly anti-aphrodisiacs by hitchhiking Trichogramma wasps. Behav Ecol 21:470–478CrossRefGoogle Scholar
  33. Kopke D, Schröder R, Fischer HM, Gershenzon G, Hilker M, Schmidt A (2008) Does egg deposition by herbivorous pine sawflies affect transcription of sesquiterpene synthases in pine? Planta 22:427–438CrossRefGoogle Scholar
  34. Kortam MN, El Arnaouty SA, Fatnassi H, Afifi AI, Pizzol J, Suloma A, Poncet C (2017) The effect of microclimatic parameters on two Trichogramma species used to control Tuta absoluta. IOBC-WPRS Bull 124(131):137Google Scholar
  35. Lewis WJ, Nordlund DA, Gueldne RC, Teal PEA, Tumlinson JH (1982) Kairomones and their use for management of entomophagous insects: XIII. Kairomonal activity for Trichogramma spp. of abdominal tips, excretion, and a synthetic sex pheromone blend of Heliothis zea (Boddie) moths. J Chem Ecol 8:1323–1331CrossRefGoogle Scholar
  36. Lietti MMM, Botto E, Alzogaray RA (2005) Insecticide resistance in argentine populations of Tuta absoluta. Neotrop Entomol 34:113–119CrossRefGoogle Scholar
  37. López E (1991) Polilla del tomate: problema crítico para la rentabilidad del cultivo de verano. Empresa y Avance Agrícola 1:6–7Google Scholar
  38. Mansour R, Brévault T, Chailleux A, Cherif A, Grissa-Lebdi K, Haddi K, Mohamed SA, Nofemela RS, Oke A, Sylla S, Tonnang HEZ, Zappalà L, Kenis M, Desneux N, Biondi A (2018) Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomol Gen 38(2):83–112CrossRefGoogle Scholar
  39. Mumm R, Dicke M (2010) Variation in natural plant products and the attraction of bodyguards for indirect plant defense. Can J Zool 88:628–667CrossRefGoogle Scholar
  40. Mumm R, Schrank K, Wegener R, Schulz S, Hilker M (2003) Chemical analysis of volatiles emitted by Pinus sylvestris after induction by insect oviposition. J Chem Ecol 29:1235–1252CrossRefGoogle Scholar
  41. Naselli M, Zappalà L, Gugliuzzo A, Tropea Garzia G, Biondi A, Rapisarda C, Cincotta F, Condurso C, Verzera A, Siscaro G (2017) Olfactory response of the zoophytophagous mirid Nesidiocoris tenuis to tomato and alternative host plants. Arthropod–Plant Interact 11:121–131CrossRefGoogle Scholar
  42. Noldus LPJJ, van Lenteren JC, Lewis WJ (1991) How Trichogramma parasitoids use moth sex pheromones as kairomones: orientation behaviour in a wind tunnel. Physiol Entomol 16:313–327CrossRefGoogle Scholar
  43. Nordlund DA, Chalfant RB, Lewis WJ (1985) Response of Trichogramma pretiosum females to volatile synomones from tomato plants. J Entomol Sci 20(3):372–376CrossRefGoogle Scholar
  44. Oliveira L, Durão AC, Fontes J, Roja IS, Tavares J (2017) Potential of Trichogramma achaeae (Hymenoptera: Trichogrammatidae) in biological control of Tuta absoluta (Lepidoptera: Gelechiidae) in Azorean greenhouse tomato crops. J Econ Entomol 110:2010–2015CrossRefGoogle Scholar
  45. Parra JRP, Zucchi RA (2004) Trichogramma in Brazil: feasibility of use after twenty years of research. Neotrop Entomol 33:271–281CrossRefGoogle Scholar
  46. Pashalidou FG, Huigens ME, Dicke M, Fatouros NE (2010) The use of oviposition-induced plant cues by Trichogramma egg parasitoids. Ecol Entomol 35:748–753CrossRefGoogle Scholar
  47. Perez-Hedo M, Suay R, Alonso M, Ruocco M, Giorgini M, Poncet C, Urbaneja A (2017) Resilience and robustness of IPM in protected horticulture in the face of potential invasive pests. Crop Prot 97:119–127CrossRefGoogle Scholar
  48. Picanço MC, Leite GLD, Guedes RNC, Silva EA (1998) Yield loss in trellised tomato affected by insecticidal sprays and plant spacing. Crop Prot 17:447–452CrossRefGoogle Scholar
  49. Polaszek A, Rugman-Jones PF, Stouthamer R, Hernandez-Suarez E, Cabello T (2012) Molecular and morphological diagnoses of five species of Trichogramma: biological control agents of Chrysodeixis chalcites (Lepidoptera: Noctuidae) and Tuta absoluta (Lepidoptera: Gelechiidae) in the Canary Islands. Biocontrol 57:21–36CrossRefGoogle Scholar
  50. Pratissoli D, Thuler RT, Andrade GS, Zanotti LCM, Silva AF (2005) Estimate of Trichogramma pretiosum to control Tuta absoluta in stalked tomato. Pesqui Agropecu Bras 40:715–718CrossRefGoogle Scholar
  51. Proffit M, Birgersson G, Bengtsson M, Reis R, Witzgall P, Lima E (2011) Attraction and oviposition of Tuta absoluta females in response to tomato leaf volatiles. J Chem Ecol 37:565–574CrossRefGoogle Scholar
  52. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 2 Aug 2018
  53. Rani PU, Sandhyarani K (2012) Specificity of systemically released rice stem volatiles on egg parasitoid, Trichogramma japonicum Ashmead behavior. J Appl Entomol 136:749–760CrossRefGoogle Scholar
  54. Reddy GVP, Holopainen JK, Guerrero A (2002) Olfactory responses of Plutella xylostella natural enemies to host pheromone, larval frass, and green leaf cabbage volatiles. J Chem Ecol 28:131–143CrossRefGoogle Scholar
  55. Roditakis E, Vasakis E, García-Vidal L, Martínez-Aguirre MDR, Rison JL, Haxaire-Lutun MO, Nauen R, Tsagkarakou A, Bielza P (2018) A four-year survey on insecticide resistance and likelihood of chemical control failure for tomato leaf miner Tuta absoluta in the European/Asian region. J Pest Sci 91:421–435.  https://doi.org/10.1007/s10340-017-0900-x CrossRefGoogle Scholar
  56. Rohart F, Gautier B, Singh A, Lê Cao K-A (2017) mixOmics: An R package for ‘omics feature selection and multiple data integration. PLoS Comput Biol 13(11):e1005752.  https://doi.org/10.1371/journal.pcbi.1005752 CrossRefGoogle Scholar
  57. Sacchettini JC, Poulter CD (1997) Biochemistry-creating isoprenoid diversity. Science 277:1788–1789CrossRefGoogle Scholar
  58. Silva GA, Picanço MC, Bacci L, Crespo ALB, Rosado JF, Guedes RNC (2011) Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag Sci 67:913–920CrossRefGoogle Scholar
  59. Silva DB, Weldegergis BT, Van Loon JJA, Bueno VHP (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 43:53–65CrossRefGoogle Scholar
  60. Silva JE, Ribeiro LMS, Vinasco N, Guedes RNC, Siqueira HAA (2019) Field-evolved resistance to chlorantraniliprole in the tomato pinworm Tuta absoluta: inheritance, cross-resistance profile, and metabolism. J Pest Sci.  https://doi.org/10.1007/s10340-018-1064-z Google Scholar
  61. Siqueira HAA, Guedes RNC, Picanco MC (2000) Insecticide resistance in populations of Tuta absoluta (Lepidoptera:Gelechiidae). Agric For Entomol 2:147–153CrossRefGoogle Scholar
  62. Takabayashi J, Dicke M, Posthumus MA (1994) Volatile herbivore-induced terpenoids in plant-mite interactions: variation caused by biotic and abiotic factors. J Chem Ecol 20:1329–1354CrossRefGoogle Scholar
  63. Tropea Garzia G, Siscaro G, Biondi A, Zappalà L (2012) Tuta absoluta, a South American pest of tomato now in the EPPO region: biology, distribution and damage. EPPO Bull 42:205–210CrossRefGoogle Scholar
  64. Turlings TCJ, Wackers FI, Vet LEM, Lewis WJ, Tumlinson JH (1993) Learning of host-finding cues by hymenopterous parasitoids. In: Papaj DR, Lewis WJ (eds) Insect learning. Chapman and Hall, New York, pp 51–78CrossRefGoogle Scholar
  65. Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485CrossRefGoogle Scholar
  66. Urbaneja A, González-Cabrera J, Arnó J, Gabar R (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Manag Sci 68:1215–1222CrossRefGoogle Scholar
  67. van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63:39–59CrossRefGoogle Scholar
  68. Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Ann Rev Entomol 37:141–172CrossRefGoogle Scholar
  69. Wilson JK, Woods HA (2016) Innate and learned olfactory responses in a wild population of the egg parasitoid Trichogramma (Hymenoptera: Trichogrammatidae). J Insect Sci 16(1):1–8CrossRefGoogle Scholar
  70. Wright MG, Stouthamer R (2011) First report of Trichogramma achaeae (Hymenoptera: Trichogrammatidae) from Hawaii. Proc Hawaii Entomol Soc 43:67Google Scholar
  71. Zappalà L, Biondi A, Alma A, Al-Jboory IJ, Arnò J, Bayram A, Chailleux A, El-Arnaouty A, Gerling D, Guenaoui Y, Shaltiel-Harpaz L, Siscaro G, Stavrinides M, Tavella L, Aznar RV, Urbaneja A, Desneux N (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(4):635–647CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Management and Conservation of Natural and Agricultural EcosystemsFederal University of Viçosa - Campus FlorestalFlorestalBrazil
  2. 2.CNR - Istituto per la Protezione Sostenibile delle PiantePorticiItaly
  3. 3.CNR - Istituto di Bioscenze e BiorisorseSesto FiorentinoItaly
  4. 4.Department of EntomologyFederal University of ViçosaViçosaBrazil

Personalised recommendations

Cite article

Buy options