Botanical insecticide and natural enemies: a potential combination for pest management against Tuta absoluta

A Correction to this article is available

This article has been updated

Abstract

The development of new strategies to control pest insects is required, in combination with conventional pesticides or replacing them. Essential oils produced from botanical extracts used in management programs should be effective against pests and selective to natural enemies. Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is one of the most destructive pests of solanaceous crops in the world, and a possible management strategy consists of releases of the predator Nesidiocoris tenuis (Hemiptera: Miridae), along with botanical applications. The objective of this study was to evaluate the effects of Prev-am® oil on T. absoluta offspring, either with or without the predator N. tenuis, as well as the oil’s effects on N. tenuis predatory behavior and longevity. The oil’s effects were compared with distilled water (control) and a synthetic pesticide (lambda-cyhalothrin). The response of populations to lambda-cyhalothrin was similar to that with Prev-am®, compared to the control, showing that N. tenuis had higher capacity to reduce T. absoluta populations. The survival analysis of predators exposed to Prev-am® indicates that none of the concentrations differed significantly from the control. In addition, the canonical variate analysis indicated significant overall differences in the predator behavior submitted to different treatments, suggesting that synthetic pesticide treatment affected predator behavior when compared to control and Prev-am®. Reduction in predatory voracity of N. tenuis adults exposed to leaves treated with pesticide and biopesticide was significant compared to the control treatment. The results obtained could improve IPM programs against T. absoluta through the Prev-am® applications and N. tenuis releases.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Change history

  • 06 March 2019

    In the original publication of the article, the authors have inadvertently missed to include a statement in the Acknowledgement section and the corrected version is given below.

References

  1. Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134

    Article  Google Scholar 

  2. Asplen MK, Anfora G, Biondi A et al (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494

    Article  Google Scholar 

  3. Barnier F, Valeix M, Duncan P (2014) Diet quality in a wild grazer declines under the threat of an ambush predator. Proc R Soc B 281:20140446

    Article  PubMed  Google Scholar 

  4. Biondi A, Desneux N, Siscaro G et al (2012) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803–812

    Article  CAS  PubMed  Google Scholar 

  5. Biondi A, Zappalà L, Stark J et al (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8(9):e76548

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Biondi A, Zappalà L, Di Mauro A et al (2016) Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis? Biocontrol 61:79–90

    Article  Google Scholar 

  7. Biondi A, Guedes RNC, Wan FH et al (2018) Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Annu Rev Entomol 63:239–258

    Article  CAS  PubMed  Google Scholar 

  8. Blaeser P, Sengonca C, Zegula T (2004) The potential use of different predatory bug species in the biological control of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). J Pest Sci 77:211–219

    Article  Google Scholar 

  9. Calvo FJ, Bolckmans K, Belda JE (2012) Release rate for a pre-plant application of Nesidiocoris tenuis for Bemisia tabaci control in tomato. Biocontrol 57:809–817

    Article  Google Scholar 

  10. Campolo O, Cherif A, Ricupero M et al (2017) Citrus peel essential oil nanoformulations to control the tomato borer, Tuta absoluta: chemical properties and biological activity. Sci Rep 7:13036

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Campos MR, Rodrigues ARS, Silva WM et al (2014) Spinosad and the tomato borer Tuta absoluta: a bioinsecticide, an invasive pest threat, and high insecticide resistance. PLoS ONE 9:e103235

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Campos MR, Biondi A, Adiga A et al (2017) From the Western Palaearctic region to beyond: Tuta absoluta ten years after invading Europe. J Pest Sci 90:787–796

    Article  Google Scholar 

  13. Chaieb I, Zarrad K, Sellam R et al (2018) Chemical composition and aphicidal potential of Citrus aurantium peel essential oils. Entomol Gen 37:63–75

    Article  Google Scholar 

  14. Ciriminna R, Lomeli-Rodriguez M, Cara PD (2014) Limonene: a versatile chemical of the bioeconomy. Chem Commun 50:15288–15296

    Article  CAS  Google Scholar 

  15. Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–297

    Article  CAS  PubMed  Google Scholar 

  16. Cordeiro EMG, Corrêa AS, Venzon M et al (2010) Insecticide survival and behavioural avoidance in the lacewings Chrysoperla externa and Ceraeochrysa cubana. Chemosphere 81:1352–1357

    Article  CAS  Google Scholar 

  17. Crispim Junior CF, Pederiva CN, Bose RC et al (2012) ETHOWATCHER: validation of a tool for behavioral and video-tracking analysis in laboratory animals. Comput Biol Med 42:257–264

    Article  PubMed  Google Scholar 

  18. De Clercq P (2002) Dark clouds and their silver linings: exotic generalist predators in augmentative biological control. Neotrop Entomol 31:169–176

    Article  Google Scholar 

  19. Desneux N, Pham-Delègue MH, Kaiser L (2004a) Effects of sub-lethal and lethal doses of lambda-cyhalothrin on oviposition experience and host-searching behaviour of a parasitic wasp, Aphidius ervi. Pest Manag Sci 60:381–389

    Article  CAS  PubMed  Google Scholar 

  20. Desneux N, Rafalimanana H, Kaiser L (2004b) Dose–response relationship in lethal and behavioural effects of different insecticides on the parasitic wasp Aphidius ervi. Chemosphere 54:619–627

    Article  CAS  PubMed  Google Scholar 

  21. Desneux N, Fauvergue X, Dechaume-Moncharmont FX et al (2005) Diaeretiella rapae limits Myzus persicae populations following applications of deltamethrin in oilseed rape. J Econ Entomol 98:9–17

    Article  PubMed  Google Scholar 

  22. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  Google Scholar 

  23. 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 83:197–215

    Article  Google Scholar 

  24. Desneux N, Luna MG, Guillemaud T et al (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408

    Article  Google Scholar 

  25. Devi PK, Yadav DN, Anand J (2002) Role of Nesidiocoris tenuis Reuter (Hemiptera: Miridae) in natural suppression of tomato fruit borer, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). Pest Manag Hortic Ecosyst 8:109–113

    Google Scholar 

  26. Drobnjaković T, Marčić D, Prijović M et al (2016) Life history traits and population growth of Encarsia formosa Gahan (Hymenoptera: Aphelinidae) local population from Serbia. Entomol Gen 35:281–295

    Article  Google Scholar 

  27. El Hajj AK, Rizk H, Gharib M et al (2017) Management of Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) using biopesticides on tomato crop under greenhouse conditions. J Agric Sci 9:123

    Google Scholar 

  28. Guedes R, Picanço M (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bull 42:211–216

    Article  Google Scholar 

  29. Haddi K, Berger M, Bielza P et al (2012) Identification of mutations associated with pyrethroid resistance in the voltage-gated sodium channel of the tomato leaf miner (Tuta absoluta). Insect Biochem Mol Biol 42:506–513

    Article  CAS  PubMed  Google Scholar 

  30. Hafsi A, Abbes K, Chermiti B et al (2012) Response of the tomato miner Tuta absoluta (Lepidoptera: Gelechiidae) to thirteen insecticides in semi-natural conditions in Tunisia. EPPO Bull 42:312–316

    Article  Google Scholar 

  31. Han P, Zhang YN, Lu ZZ et al (2018) Are we ready for the invasion of Tuta absoluta? Unanswered key questions for elaborating an Integrated Pest Management package in Xinjiang, China. Entomol Gen 38:113–125

    Article  Google Scholar 

  32. He Y, Zhao J, Zheng Y, Desneux N et al (2012) Lethal effect of imidacloprid on the coccinellid predator Serangium japonicum and sublethal effects on predator voracity and on functional response to the whitefly Bemisia tabaci. Ecotoxicology 21:1291–1300

    Article  CAS  PubMed  Google Scholar 

  33. Herbert IN, Svendsen C, Hankard PK et al (2004) Comparison of instantaneous rate of population increase and critical-effect estimates in Folsomia candida exposed to four toxicants. Ecotoxicol Environ Saf 57:175–183

    Article  CAS  PubMed  Google Scholar 

  34. Isman MB (2000) Plant essential oils for pest and disease management. Crop Prot 19:603–608

    Article  CAS  Google Scholar 

  35. Köhler HR, Triebskorn R (2013) Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science 341:759–765

    Article  CAS  Google Scholar 

  36. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  37. Lu YH, Wu KM, Jiang YY et al (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365

    Article  CAS  PubMed  Google Scholar 

  38. Mansour R, Suma P, Mazzeo G, Lebdi KG et al (2011) Evaluating side effects of newer insecticides on the vine mealybug parasitoid Anagyrus sp. near pseudococci, with implications for integrated pest management in vineyards. Phytoparasitica 39:369–376

    Article  CAS  Google Scholar 

  39. Mansour R, Brévault T, Chailleux A et al (2018) Occurrence, biology, natural enemies and management Tuta absoluta in Africa. Entomol Gen 38:83–111

    Article  Google Scholar 

  40. Martins JC, Picanço MC, Bacci L et al (2016) Life table determination of thermal requirements of the tomato borer Tuta absoluta. J Pest Sci 89:897–908

    Article  Google Scholar 

  41. McNair JB, Goulden CE, Ziegenfuss MC (1995) Is there a place for ecotoxicology? SETAC News 15:18–21

    Google Scholar 

  42. Miresmailli S, Isman MB (2014) Botanical insecticides inspired by plant–herbivore chemical interactions. Trends Plant Sci 19:29–35

    Article  CAS  PubMed  Google Scholar 

  43. Mohammed AAH, Desneux N, Fan YJ et al (2018) Impact of imidacloprid and natural enemies on cereal aphids: integration or ecosystem service disruption? Entomol Gen 37:47–61

    Article  Google Scholar 

  44. Mossa ATH (2016) Green pesticides: essential oils as biopesticides in insect- pest management. Environ Sci Technol 9:354–378

    Article  CAS  Google Scholar 

  45. Nelder JA, Wedderburn RWM (1972) Generalized linear models. J R Stat Soc Ser A 135:370–384

    Article  Google Scholar 

  46. Nollet LM, Rathore HS (2017) Orange oil. In: Ciriminna R, Meneguzzo F, Pagliaro M (eds) Green pesticides handbook: essential oils for pest control, 1st edn. CRC Press, Ghent, pp 291–300

    Google Scholar 

  47. Passos LC, Soares MA, Costa MA et al (2017) Physiological susceptibility of the predator Macrolophus basicornis (Hemiptera: Miridae) to pesticides used to control of Tuta absoluta (Lepidoptera: Gelechiidae). Biocontrol Sci Technol 27:1082–1095

    Article  Google Scholar 

  48. Passos LC, Soares MA, Collares LJ et al (2018) Lethal, sublethal and transgenerational effects of insecticides on Macrolophus basicornis, predator of Tuta absoluta. Entomol Gen 38:127–143

    Article  Google Scholar 

  49. Pavela R, Benelli G (2016) Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21:1000–1007

    Article  CAS  Google Scholar 

  50. 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 35:297–306

    Google Scholar 

  51. Perdikis DC, Lykouressis DP (2002) Life table and biological characteristics of Macrolophus pygmaeus when feeding on Myzus persicae and Trialeurodes vaporariorum. Entomol Exp Appl 102:261–272

    Article  Google Scholar 

  52. Perdikis DC, Lykouressis DP (2004) Myzus persicae (Homoptera: Aphididae) as suitable prey for Macrolophus pygmaeus (Hemiptera: Miridae) population increase on pepper plants. Environ Entomol 33:499–505

    Article  Google Scholar 

  53. Pérez-Aguilar DA, Soares MA, Passos LC et al (2018) Lethal and sublethal effects of insecticides on Engytatus varians (Heteroptera: Miridae), a predator of Tuta absoluta (Lepidoptera: Gelechiidae). Ecotoxicology 27:719–728

    Article  CAS  PubMed  Google Scholar 

  54. Ragsdale DW, Landis DA, Brodeur J et al (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399

    Article  CAS  PubMed  Google Scholar 

  55. R Core Team (2016) R: a language and environment for statistical computing (Version 3.3.1). R Foundation for Statistical Computing, Vienna. https://www.r-project.org/

  56. Regnault-Roger C, Vincent C, Arnasson JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annu Rev Entomol 57:405–425

    Article  CAS  PubMed  Google Scholar 

  57. Relyea RA, Auld JR (2005) Predator- and competitor-induced plasticity: how changes in foraging morphology affect phenotypic tradeoffs. Ecology 86:1723–1729

    Article  Google Scholar 

  58. Roditakis E, Skarmoutsou C, Staurakaki M (2013) Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest Manag Sci 69:834–840

    Article  CAS  PubMed  Google Scholar 

  59. Roditakis E, Vasakis E, Grispou M et al (2015) First report of Tuta absoluta resistance to diamide insecticides. J Pest Sci 88:9–16

    Article  Google Scholar 

  60. Roditakis E, Vasakis E, García-Vidal L et al (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

    Article  Google Scholar 

  61. Sankarganesh E, Firake DM, Sharma B et al (2017) Invasion of the South American Tomato Pinworm, Tuta absoluta, in northeastern India: a new challenge and biosecurity concerns. Entomol Gen 36:335–345

    Article  Google Scholar 

  62. SAS Institute (2008) SAS/STAT®, Release 9.2: User’s Guide. Cary, NC, USA

  63. Silva GA, Picanço MC, Bacci L et al (2011) Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag Sci 67:913–920

    Article  CAS  PubMed  Google Scholar 

  64. Siqueira HAA, Guedes RNC, Picanço MC (2000) Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae). Agric For Entomol 2:147–153

    Article  Google Scholar 

  65. Slos S, Meester LD, Stoks R (2009) Behavioural activity levels and expression of stress proteins under predation risk in two damselfly species. Ecol Entomol 34:297–303

    Article  Google Scholar 

  66. Sosa ME, Tonn CE (2008) Plant secondary metabolites from Argentinean semiarid lands: bioactivity against insects. Phytochem Rev 7:3–24

    Article  CAS  Google Scholar 

  67. Stark JD, Tanigoshi L, Bounfour M et al (1997) Reproductive potential: its influence on the susceptibility of a species to pesticides. Ecotoxicol Environ Saf 37:273–279

    Article  CAS  PubMed  Google Scholar 

  68. Stark JD, Banks JE, Acheampong S (2004) Estimating susceptibility of biological control agents to pesticides: influence of life history strategies and population structure. Biol Control 29:392–398

    Article  Google Scholar 

  69. Stenersen J (2004) Chemical pesticides mode of action and toxicology. CRC Press, Ghent

    Google Scholar 

  70. Sylla S, Brévault T, Bal AB et al (2017) Rapid spread of the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), an invasive pest in Sub-Saharan Africa. Entomol Gen 36:269–283

    Article  Google Scholar 

  71. Walthall WK, Stark JD (1997) Comparison of two population-level ecotoxicological endpoints: the intrinsic (rm) and instantaneous (ri) rates of increase. Environ Toxicol Chem 16:1068–1073

    CAS  Google Scholar 

  72. Wan FH, Yang NW (2016) Invasion and management of agricultural alien insects in China. Annu Rev Entomol 61:77–98

    Article  CAS  PubMed  Google Scholar 

  73. Xian X, Han P, Wang S et al (2017) The potential invasion risk and preventive measures against the tomato leafminer Tuta absoluta in China. Entomol Gen 36:319–333

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Philippe Bearez, Edwige Amiens-Desneux and Christiane Metay-Merrien from INRA for technical assistance and the Coordination of Superior Level Staff Improvement (Capes), Minas Gerais State Foundation for Research (FAPEMIG) and CNPq (National Council for Scientific and Technological Development) for provide funding to MAS (Ph.D. fellowship), the project EUCLID (H2020-SFS-2014, grant number: 633999) for funding to ND, and the project STomP (ARIMnet2, grant agreement: 618127) for funding to ND, A-VL, AB and LZ.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marianne A. Soares.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

This article does not contain any studies with human participants or animals (other than insects) performed by any of the authors.

Additional information

Communicated by M. Traugott.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Soares, M.A., Campos, M.R., Passos, L.C. et al. Botanical insecticide and natural enemies: a potential combination for pest management against Tuta absoluta. J Pest Sci 92, 1433–1443 (2019). https://doi.org/10.1007/s10340-018-01074-5

Download citation

Keywords

  • Natural product
  • Predatory mirid
  • South American tomato pinworm
  • Ecotoxicology
  • Biological control