Advertisement

Bottom-up effects of irrigation, fertilization and plant resistance on Tuta absoluta: implications for Integrated Pest Management

  • Peng HanEmail author
  • Nicolas Desneux
  • Christine Becker
  • Romain Larbat
  • Jacques Le Bot
  • Stéphane Adamowicz
  • Jiang Zhang
  • Anne-Violette Lavoir
Review
  • 208 Downloads

Abstract

Soil abiotic factors and plant traits are able to trigger bottom-up effects along the tri-trophic plant–herbivore–natural enemy interactions. The consequences could be useful for controlling the insect herbivores. The South American tomato pinworm, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), a devastating invasive leaf-mining pest on tomato and other solanaceous plants, is currently threatening the tomato production worldwide. Recent knowledge of bottom-up effects on this pest has been gained, with fertilization, irrigation, plant resistance traits, as well as their interactions, being the major sources of these effects. Evidence is now emerging on how they impact on the performance of the moth from the perspective of tri-trophic interactions. In this review, we summarize the essential experiments studying the bottom-up effects on T. absoluta and discuss the implications of those findings for the Integrated Pest Management programs. Future promising research directions are then proposed.

Keywords

Plant chemical defense Plant adaptation/tolerance Tri-trophic interactions Breeding Plastid genome transformation Agro-ecosystems 

Notes

Acknowledgements

We thank the Editor-in-Chief of Journal of Pest Science for the invitation to submit this review article fitting the special issue on Tuta absoluta in 2019.

Compliance with ethical standards

Conflict of interest

Authors declare no conflict of interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abbes K, Biondi A, Kurtulus A, Ricupero M, Russo A, Siscaro G, Chermiti B, Zappalà L (2015) Combined non-target effects of insecticide and high temperature on the parasitoid Bracon nigricans. PLoS ONE 10:e0138411CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abenavoli MR, Leone M, Sunseri F, Bacchi M, Sorgonà A (2016) Root phenotyping for drought tolerance in bean landraces From Calabria (Italy). J Agron Crop Sci 202:1–12CrossRefGoogle Scholar
  3. Amtmann A, Troufflard S, Armengaud P (2008) The effect of potassium nutrition on pest and disease resistance in plants. Physiol Plant 133:682–691CrossRefPubMedGoogle Scholar
  4. Arnò J, Gabarra R (2011) Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). J Pest Sci 84:513–520CrossRefGoogle Scholar
  5. Ballhorn DJ, Elias JD (2014) Salinity-mediated cyanogenesis in white clover (Trifolium repens) affects trophic interactions. Ann Bot 114:357–366CrossRefPubMedPubMedCentralGoogle Scholar
  6. Ballhorn DJ, Kautz S, Jensen M, Schmitt I, HeilM Hegeman AD (2011) Genetic and environmental interactions determine plant defences against herbivores. J Ecol 99:313–326CrossRefGoogle Scholar
  7. Bawin T, Dujeu D, De Backer L, Francis F, Verheggen FJ (2016) Ability of Tuta absoluta (Lepidoptera: Gelechiidae) to develop on alternative host plant species. Can Entomol 148:434–442CrossRefGoogle Scholar
  8. Becker C, Desneux N, Monticelli L, Fernandez X, Michel T, Lavoir AV (2015) Effects of abiotic factors on HIPV-mediated interactions between plants and parasitoids. Biomed Res Int 2015:342982CrossRefPubMedPubMedCentralGoogle Scholar
  9. Benrey B, Denno RF (1997) The slow-growth–high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78:987–999Google Scholar
  10. Bentz J, Reeves J III, Barbosa P, Francis B (1995) Nitrogen fertilizer effect on selection, acceptance, and suitability of Euphorbia pulcherrima (Euphorbiaceae) as a host plant to Bemisia tabaci (Homoptera: Aleyrodidae). Environ Entomol 24:40–45CrossRefGoogle Scholar
  11. Bergougnoux V (2014) The history of tomato: from domestication to biopharming. Biotechnol Adv 32:170–189CrossRefPubMedGoogle Scholar
  12. Bi JL, Toscano NC, Madore MA (2003) Effect of urea fertilizer application on soluble protein and free amino acid content of cotton petioles in relation to silverleaf whitefly (Bemisia argentifolii) populations. J Chem Ecol 29:747–761CrossRefPubMedGoogle Scholar
  13. Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8:e76548CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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 63:239–258CrossRefPubMedGoogle Scholar
  15. Blazhevski S, Kalaitzaki AP, Tsagkarakis AE (2018) Impact of nitrogen and potassium fertilization regimes on the biology of the tomato leaf miner Tuta absoluta. Entomol Gen 37:157–174CrossRefGoogle Scholar
  16. Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A, Kant MR, Prins M, de Vos M, Haring MA, Schuurink RC (2012) Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proc Natl Acad Sci USA 109:20124–20129CrossRefPubMedGoogle Scholar
  17. Bock (2015) Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Annu Rev Plant Biol 66:211–241CrossRefPubMedGoogle Scholar
  18. Bottega DB, de Souza BHS, Rodrigues NEL, Eduardo WI, Barbosa JC, Boica AL (2017) Resistant and susceptible tomato genotypes have direct and indirect effects on Podisus nigrispinus preying on Tuta absoluta larvae. Biol Control 106:27–34CrossRefGoogle Scholar
  19. Bruce TJA (2015) Interplay between insects and plants: dynamics and complex interactions that have coevolved over millions of years but act in milliseconds. J Exp Bot 66:455–465CrossRefPubMedGoogle Scholar
  20. Calvo FJ, Soriano JD, Stansly PA, Belda JE (2016) Can the parasitoid Necremnus tutae (Hymenoptera: Eulophidae) improve existing biological control of the tomato leafminer Tuta aboluta (Lepidoptera: Gelechiidae)? Bull Entomol Res 106:502–511CrossRefPubMedGoogle Scholar
  21. Camargo RA, Herai RH, Santos LN, Bento FM, Lima JE, Marques-Souza H, Figueira A (2015) De novo transcriptome assembly and analysis to identify potential gene targets for RNAi-mediated control of the tomato leafminer (Tuta absoluta). BMC Genom 16:635CrossRefGoogle Scholar
  22. Camargo RA, Barbosa GO, Possignolo IP, Peres LE, Lam E, Lima JE, Figueira A, Marques-Souza H (2016) RNA interference as a gene silencing tool to control Tuta abosuta in tomato (Solanum lycopersicum). PeeJ 4:e2673Google Scholar
  23. Campos MR, Rodrigues ARS, Silva WM, Silva TBM, Silva VRF, Guedes RNC, Siqueira HAA (2014) Spinosad and the tomato borer Tuta absoluta: a bioinsecticide, an invasive pest threat, and high insecticide resistance. PLoS ONE 9:e103235CrossRefPubMedPubMedCentralGoogle Scholar
  24. Campos MR, Silva TBM, Silva WM, Silva JE, Siqueira HAA (2015) Spinosyn resistance in the tomato borer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J Pest Sci 88:405–412CrossRefGoogle Scholar
  25. 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
  26. Caparros Megido R, Haubruge E, Verheggen FJ (2012) First evidence of deuterotokous parthenogenesis in the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J Pest Sci 85:409–412CrossRefGoogle Scholar
  27. Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM, Francia E, Marèa C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crop Res 105:1–14CrossRefGoogle Scholar
  28. Chen Y, Ruberson JR, Olson DM (2008) Nitrogen fertilization rate affects larval performance and feeding, and oviposition preference of the beet armyworm, Spodoptera exigua, on cotton. Entomol Exp Appl 126:244–255CrossRefGoogle Scholar
  29. Chen Y, Olson DM, Ruberson JR (2010) Effects of nitrogen fertilization on tritrophic interactions. Arthropod-Plant Interact 4:81–94CrossRefGoogle Scholar
  30. 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
  31. Coqueret V, Le Bot J, Larbat R, Desneux N, Robin C, Adamowicz S (2017) Nitrogen nutrition of tomato plant alters leafminer dietary intake dynamics. J Insect Physiol 99:130–138CrossRefPubMedGoogle Scholar
  32. Cuartero J, Fernández-Muñoz R (1999) Tomato and salinity. Sci Hortic 78:83–125CrossRefGoogle Scholar
  33. De Azevedo SM, de Faria MV, Maluf WR, Acbde O, Jade F (2003) Zingiberene-mediated resistance to the South American tomato pinworm derived from Lycopersicon hirsutum var. hirsutum. Euphytica 134:347–351CrossRefGoogle Scholar
  34. De Backer L, Megido RC, Fauconnier ML, Brostaux Y, Francis F, Verheggen F (2015) Tuta absoluta-induced plant volatiles: attractiveness towards the generalist predator Macrolophus pygmaeus. Arthropod-Plant Interact 9:465–476CrossRefGoogle Scholar
  35. De Backer L, Bawin T, Schott M, Gillard L, Marko IE, Francis F, Verheggen F (2017) 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 11:111–120CrossRefGoogle Scholar
  36. Debouba M, Gouia H, Suzuki A, Ghorbel MH (2006) NcCl stress effects on enzymes involved in nitrogen assimilation pathway in tomato “Lycopersicon esculentun” seedlings. J Plant Physiol 163:1247–1258CrossRefPubMedGoogle Scholar
  37. Denno RF, Gratton C, Peterson MA, Langellotto GA, Finke DL, Huberty AF (2002) Bottom-up forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83:1443–1458CrossRefGoogle Scholar
  38. Desneux N, Decourtye A, Delpuech J (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106CrossRefPubMedGoogle Scholar
  39. 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
  40. Desneux N, Luna MG, Guillemaud T, Urbaneja A (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 84:403–408CrossRefGoogle Scholar
  41. 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
  42. Dong YC, Han P, Niu CY, Zappalà L, Amiens-Desneux E, Bearez P, Lavoir AV, Biondi A, Desneux N (2018) Nitrogen and water inputs to tomato plant do not trigger bottom-up effects on a leafminer parasitoid through host and non-host exposures. Pest Manag Sci 74:516–522CrossRefPubMedGoogle Scholar
  43. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212CrossRefGoogle Scholar
  44. Feng Y, Cao LY, Wu WM, Shen XH, Zhan XD, Zhai RR, Wang RC, Chen DB, Cheng SH (2010) Mapping QTLs for nitrogen-deficiency tolerance at seedling stage in rice (Oryza sativa L.). Plant Breed 129:652–656CrossRefGoogle Scholar
  45. Fernandes MES, Fernandes FL, Silva DJ, Picanço MC, Jhamc GN, Carneiro PC, Queiroz RB (2012) Trichomes and hydrocarbons associated with the tomato plant antixenosis to the leafminer. An Acad Bras Cienc 84:201–209CrossRefPubMedGoogle Scholar
  46. Flores P, Hernández V, Hellín P, Fenoll J, Cava J, Mestre T, Martínez V (2015) Metabolite profile of the tomato dwarf cultivar Micro-Tom and comparative response to saline and nutritional stresses with regard to a commercial cultivar. J Sci Food Agric 96:1562–1570CrossRefPubMedGoogle Scholar
  47. Gharekhani GH, Salek-Ebrahimi H (2014) Life table parameters of Tuta absoluta (Lepidoptera: Gelechiidae) on different varieties of tomato. J Econ Entomol 107:1765–1770CrossRefPubMedGoogle Scholar
  48. Gillespie DR, McGregor RR (2000) The functions of plant feeding in the omnivorous predator Dicyphus hesperus: water places limits on predation. Ecol Entomol 25:380–386CrossRefGoogle Scholar
  49. Greenway H, Munns R (1980) Mechanisms of salt tolerance in Nonhalophytes. Ann Rev Plant Physiol 31:149–190CrossRefGoogle Scholar
  50. Guedes RNC, Picanco MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bull 42:211–216CrossRefGoogle Scholar
  51. Guillemaud T, Blin A, Le Goff I et al (2015) The tomato borer, Tuta absoluta, invading the Mediterranean Basin, originates from a single introduction from Central Chile. Sci Rep 5:8371CrossRefPubMedPubMedCentralGoogle Scholar
  52. Gutbrodt B, Mody K, Dorn S (2011) Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores. Oikos 120:1732–1740CrossRefGoogle Scholar
  53. Han P, Lavoir AV, Le Bot J, Amiens-Desneux E, Desneux N (2014) Nitrogen and water availability to tomato plants triggers bottom-up effects on the leafminer Tuta absoluta. Sci Rep 4:4455CrossRefPubMedPubMedCentralGoogle Scholar
  54. Han P, Bearez P, Adamowicz S, Lavoir AV, Desneux N (2015a) Nitrogen and water limitations in tomato plants trigger negative bottom-up effects on the omnivorous predator Macrolophus pygmaeus. J Pest Sci 88:685–691CrossRefGoogle Scholar
  55. Han P, Dong YC, Lavoir AV, Adamowicz S, Bearez P, Wajnberg E, Desneux N (2015b) Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod. Ecol Evol 5:5468–5477CrossRefPubMedPubMedCentralGoogle Scholar
  56. Han P, Desneux N, Amiens-Desneux E, Le Bot J, Bearez P, Lavoir AV (2016a) Does plant cultivar difference modify the bottom-up effects of resource limitation on plant–herbivorous insect interactions? J Chem Ecol 42:1293–1303CrossRefPubMedGoogle Scholar
  57. Han P, Wang ZJ, Lavoir AV, Michel T, Seassau A, Zheng WY, Niu CY, Desneux N (2016b) Increased water salinity applied to tomato plants accelerates the development of the leaf miner Tuta absoluta through bottom-up effects. Sci Rep 6:32403CrossRefPubMedPubMedCentralGoogle Scholar
  58. Han P, Zhang YN, Lu ZZ, Wang S, Biondi A, Desneux N (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 38:113–125CrossRefGoogle Scholar
  59. Hufbauer RA, Torchin ME (2007) Integrating ecological and evolutionary theory of biological invasions. In: Nentwig W (ed) biological invasions. Springer, Berlin, pp 79–96CrossRefGoogle Scholar
  60. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732Google Scholar
  61. Inbar M, Doostdar H, Mayer R (2001) Suitability of stressed and vigorous plants to various insect herbivores. Oikos 94:228–235CrossRefGoogle Scholar
  62. Janssen A, Willemse E, Van Der Hammen T (2003) Poor host plant quality causes omnivore to consume predator eggs. J Anim Ecol 72:478–483CrossRefGoogle Scholar
  63. Kaplan I, Thaler JS (2011) Do plant defenses enhance or diminish prey suppression by omnivorous Heteroptera? Biol Control 59:53–60CrossRefGoogle Scholar
  64. Kohandani F, Le Goff GJ, Hance T (2017) Does insect mother know under what conditions it will make their offspring live? Insect Sci 24:141–149CrossRefPubMedGoogle Scholar
  65. Larbat R, Adamowicz S, Robin C, Han P, Desneux N, Le Bot J (2016) Interrelated responses of tomato plants and the leaf miner Tuta absoluta to nitrogen supply. Plant Biol 18:495–504CrossRefPubMedGoogle Scholar
  66. Le Bot J, Adamowicz S (2005) Nitrogen nutrition and use in horticultural crops. J Crop Improv 15:323–367CrossRefGoogle Scholar
  67. Le Bot J, Adamowicz S, Robin P (1998) Modelling plant nutrition of horticultural crops: a review. Sci Hortic 74:47–82CrossRefGoogle Scholar
  68. Le Bot J, Bénard C, Robin C, Bourgaud F, Adamowicz S (2009) The “trade-off” between synthesis of primary and secondary compounds in young tomato leaves is altered by nitrate nutrition: experimental evidence and model consistency. J Exp Bot 60:4301–4314CrossRefPubMedGoogle Scholar
  69. Leite GLD, Picanço M, Jham GN, Marquini F (2004) Intensity of Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) and Liriomyza spp. (Diptera: Agromyzidae) attacks on Lycopersicum esculentum Mill. Leaves. Ciência e Agrotecnologia 28:42–48CrossRefGoogle Scholar
  70. Lu YH, Wu KM, Jiang YY, Guo YY, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365CrossRefPubMedGoogle Scholar
  71. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158CrossRefPubMedGoogle Scholar
  72. Maluf WR, Barbosa LV, Santa-Cecília LVC (1997) 2-Tridecanone-mediated mechanisms of resistance to the South American tomato pinworm Scrobipalpuloides absoluta (Meyrick, 1917) (Lepidoptera-Gelechiidae) in Lycopersicon spp. Euphytica 93:189–194CrossRefGoogle Scholar
  73. Maluf WR, de Silva VF, Cardoso M, Gomes LAA, Neto ACG, Maciel GM, Nízio DAC (2010) Resistance to the South American tomato pinworm Tuta absoluta in high acylsugar and/or high zingiberene tomato genotypes. Euphytica 176:113–123CrossRefGoogle Scholar
  74. Manaa A, Ben Ahmed H, Valot B, Bouchet JP, Aschi-Smiti S, Causse M, Faurobert M (2011) Salt and genotype impact on plant physiology and root proteome variations in tomato. J Exp Bot 62:2797–2813CrossRefPubMedGoogle Scholar
  75. Mansour R, Brévault T, Chailleux A et al (2018) Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomol Gen 38:83–111CrossRefGoogle Scholar
  76. Mohamadi P, Razmjou J, Naseri B, Hassanpour M (2017) Humic fertilizer and vermicompost applied to the soil can positively affect population growth parameters of Trichogramma brassicae (Hymenoptera: Trichogrammatidae) on eggs of Tuta absoluta (Lepidoptera: Gelechiidae). Neotrop Entomol 46:678–684CrossRefPubMedGoogle Scholar
  77. Naselli M, Zappalà L, Gugliuzzo A et al (2017a) Olfactory response of the zoophytophagous mirid Nesidiocoris tenuis to tomato and alternative host plants. Arthropod-Plant Interact 11:121–131CrossRefGoogle Scholar
  78. Naselli M, Biondi A, Tropea Garzia G, Desneux N, Russo A, Siscaro G, Zappalà L (2017b) Insights into food webs associated with the South American tomato pinworm. Pest Manag Sci 73:1352–1357CrossRefPubMedGoogle Scholar
  79. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotox Environ Safe 60:324–349CrossRefGoogle Scholar
  80. Passos LC, Soares MA, Collares LJ, Malagoli I, Desneux N, Carvalho GA (2018) Lethal, sublethal and transgenerational effects caused by insecticides on Macrolophus basicornis, predator of Tuta absoluta. Entomol Gen 38:127–143CrossRefGoogle Scholar
  81. Pérez-Aguilar DA, Araújo Soares M, Passos LC, Martínez AM, Pineda S, Carvalho GA (2018) Lethal and sublethal effects of insecticides on Engytatus varians (Heteroptera: Miridae), a predator of Tuta absoluta (Lepidoptera: Gelechiidae). Ecotoxicology 27:719–728CrossRefGoogle Scholar
  82. Poelman EH, Dicke M (2014) Plant-mediated interactions among insects within a community ecological perspective. In: Voelckel C, Jander G (eds) Annual plant reviews insect plant interactions, vol 47. Wiley, New York, pp 309–338CrossRefGoogle Scholar
  83. Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251CrossRefGoogle Scholar
  84. 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 37:565–574CrossRefPubMedGoogle Scholar
  85. Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Ann Rev Entomol 56:375–399CrossRefGoogle Scholar
  86. Rakha M, Zekeya N, Sevgan S, Musembi M, Ramasamy S, Hanson P, Havey M (2017) Screening recently identified whitefly/spider mite—resistant wild tomato accessions for resistance to Tuta absoluta. Plant Breed 136:562–568CrossRefGoogle Scholar
  87. Resende JTV, de Maluf WR, Faria MV, Pfann Z, Nascimento IR (2006) Acylsugars in tomato leaflets confer resistance to the South American tomato pinworm, Tuta absoluta. Meyr Sci Agric 63:20–25CrossRefGoogle Scholar
  88. Roditakis E, Steinbach D, Moritz G et al (2017) Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Insect Biochem Mol Biol 80:11–20CrossRefPubMedGoogle Scholar
  89. Roditakis E, Vasakis E, Garcia-Vidal L, Martínez-Aguirre MR, 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 91:421–435CrossRefGoogle Scholar
  90. Romero-Aranda R, Soria T, Cuartero J (2001) Tomato plant–water and plant–water relationships under saline growth conditions. Plant Sci 160:265–272CrossRefPubMedGoogle Scholar
  91. Rostami E, Madadi H, Abbasipour H, Allahyari H, Cuthbertson AGS (2017) Life table parameters of the tomato leaf miner Tuta absoluta (Lepidoptera: Gelechiidae) on different tomato cultivars. J Appl Entomol 141:88–96CrossRefGoogle Scholar
  92. Royer M, Larbat R, Le Bot J, Adamowicz S, Robin C (2013) Is the C:N ratio a reliable indicator of C allocation to primary and defence-related metabolisms in tomato? Phytochemistry 88:25–33CrossRefPubMedGoogle Scholar
  93. Ruelas C, Tiznado-Hernández ME, Sánchez-Estrada A, Robles-Burgueño MR, Troncoso-Rojas R (2006) Changes in phenolic acid content during alternaria alternata infection in tomato fruit. J Phytopathol 154:236–244CrossRefGoogle Scholar
  94. Ruf S, Hermann M, Berger IJ, Carrer H, Bock R (2001) Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat Biotechnol 19:870–875CrossRefPubMedGoogle Scholar
  95. Salehi Z, Yarahmadi F, Rasekh A, Sohani NZ (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
  96. Sankarganesh E, Firake DM, Sharma Verma VK, Behere GT (2017) Invasion of the South American Tomato Pinworm, Tuta absoluta, in northeastern India: a new challenge and biosecurity concerns. Entomol Gen 36:335–345CrossRefGoogle Scholar
  97. Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology. Oxford University Press, OxfordGoogle Scholar
  98. Seagraves MP, Riedell WE, Lundgren JG (2011) Oviposition preference for water-stressed plants in Orius insidiosus (Hemiptera: Anthocoridae). J Insect Behav 24:132–143CrossRefGoogle Scholar
  99. Selale H, Dagli F, Mutlu N, Doğanlar S, Frary A (2017) Cry1Ac-mediated resistance to tomato leaf miner (Tuta absoluta) in tomato. Plant Cell Tiss Org 131:65–73CrossRefGoogle Scholar
  100. Silva JE, Assis CPO, Ribeiro LMS, Siqueira HAA (2016) Field evolved resistance and cross-resistance of Brazilian Tuta absoluta (Lepidoptera: Gelechiidae) populations to diamide insecticides. J Econ Entomol 109:2190–2195CrossRefGoogle Scholar
  101. 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 43:53–65CrossRefPubMedPubMedCentralGoogle Scholar
  102. Silva DB, Bueno VHP, Loon JJAV, Peñaflor MFGV, Bento JMS, Lenteren JCV (2018) Attraction of three Mirid Predators to tomato infested by both the tomato leaf mining moth Tuta absoluta and the whitefly Bemisia tabaci. J Chem Ecol 44:29–39CrossRefPubMedGoogle Scholar
  103. Sinia A, Roitberg B, McGregor RR, Gillespie DR (2004) Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus. Entomol Exp Appl 110:243–248CrossRefGoogle Scholar
  104. Siqueira HAA, Guedes RNC, Picanço MC (2000) Cartap resistance and synergism in populations of Tuta absoluta (Lepidoptera: Gelechiidae). J Appl Entomol 124:233–238CrossRefGoogle Scholar
  105. Siqueira HAA, Guedes RNC, Fragoso DB, Magalhaes LC (2001) Abamectin resistance and synergism in Brazilian populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Int J Pest Manag 47:247–251CrossRefGoogle Scholar
  106. Slansky F Jr, Scriber JM (1985) Food consumption and utilization. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology. Pergamon Press, Oxford, pp 87–163Google Scholar
  107. Snoeren TAL, Sitbon E, Levy D (2017) Resistance to arthropod pest in tomatoes. United States Patent Application Publication. Pub. No: US2017/0240910 A1Google Scholar
  108. Sohrabi F, Nooryazdan H, Gharati B, Saeidi Z (2016) Evaluation of ten tomato cultivars for resistance against tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under field infestation conditions. Entomol Gen 36:163–175CrossRefGoogle Scholar
  109. Sohrabi F, Nooryazdan HR, Gharati B, Saeidi Z (2017) Plant Resistance to the moth Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato cultivars. Neotrop Entomol 46:203–209CrossRefPubMedGoogle Scholar
  110. Soria T, Cuartero J (1997) Tomato fruit yield and water consumption with salty water irrigation. Acta Hortic 458:215–219Google Scholar
  111. Strapasson P, Pinto-Zevallos DM, Paudel S, Rajotte EG, Felton GW, Zarbin PHG (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 40:1090–1098CrossRefPubMedGoogle Scholar
  112. Sung J, Lee S, Lee Y, Ha S, Son B, Kim T, Waters BM, Krishnan HB (2015) Metabolomic profiling from leaves and roots of tomato (Solanum lycopersicum L.) plants grown under nitrogen, phosphorus or potassium-deficient condition. Plant Sci 241:55–64CrossRefPubMedGoogle Scholar
  113. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Ann Rev Entomol 47:561–594CrossRefGoogle Scholar
  114. Tan CW, Chiang SY, Ravuiwasa KT, Yadav J, Hwang SY (2012) Jasmonate-induced defenses in tomato against Helicoverpa armigera depend in part on nutrient availability, but artificial induction via methyl jasmonate does not. Arthropod-Plant Interact 6:531–541CrossRefGoogle Scholar
  115. Tariq M, Wrignt DJ, Rossiter JT, Staly JT (2012) Aphids in a changing world: testing the plant stress, plant vigour and pulsed stress hypotheses. Agr Forest Entomol 14:177–185CrossRefGoogle Scholar
  116. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251CrossRefPubMedGoogle Scholar
  117. Vacas S, Alfaro C, Primo J, Navarro-Llopis V (2011) Studies on the development of a mating disruption system to control the tomato leafminer, Tuta absoluta Povolny (Lepidoptera: Gelechiidae). Pest Manag Sci 67:1473–1480CrossRefPubMedGoogle Scholar
  118. Wan FH, Yang NW (2016) Invasion and management of agricultural alien insects in China. Ann Rev Entomol 61:77–98CrossRefGoogle Scholar
  119. Wheeler JAG, Krimmel BA (2015) Mirid (Hemiptera: Heteroptera) specialists of sticky plants: adaptations. Interact Ecol Implic 60:393–414Google Scholar
  120. White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, BerlinCrossRefGoogle Scholar
  121. Xian XQ, Han P, Wang S, Zhang GF, Liu WX, Desneux N, Wan FH (2017) The potential invasion risk and preventive measures against the tomato leafminer Tuta absoluta in China. Entomol Gen 36:319–333CrossRefGoogle Scholar
  122. Ximénez-Embún MG, Ortego F, Castañera P (2016) Drought-stressed tomato plants trigger bottom-up effects on the invasive Tetranychus evansi. PLoS ONE 11:e0145275CrossRefPubMedPubMedCentralGoogle Scholar
  123. Zappalà L, Siscaro G, Biondi A, Mollà O, Gonzàlez-Cabrera J, Urbaneja A (2012) Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. J Appl Entomol 136:401–409CrossRefGoogle Scholar
  124. Zappalà L, Biondi A, Alma A 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
  125. Zaugg I, Benrey B, Bacher S (2013) Bottom-up and top-down effects influence Bruchid beetle individual performance but not population densities in the field. PLoS ONE 8:e55317CrossRefPubMedPubMedCentralGoogle Scholar
  126. Zhang J, Khan SA, Hasse C, Ruf S, Heckel DG, Bock R (2015) Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347:911–914Google Scholar
  127. Zhang J, Khan SA, Heckel DG, Bock R (2017) Next generation insect-resistant plants: RNAi-mediated crop protection. Trends Biotechnol 8:871–882CrossRefGoogle Scholar
  128. Zhong ZW, Li XF, Pearson D, Wang DL, Sanders D, Zhu Y, Wang L (2017) Ecosystem engineering strengthens bottom-up and weakens top-down effects via trait-mediated indirect interactions. Proc R Soc B 284:20170475CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Peng Han
    • 1
    Email author
  • Nicolas Desneux
    • 2
  • Christine Becker
    • 3
  • Romain Larbat
    • 4
  • Jacques Le Bot
    • 5
  • Stéphane Adamowicz
    • 5
  • Jiang Zhang
    • 6
  • Anne-Violette Lavoir
    • 2
  1. 1.CAS Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and GeographyChinese Academy of SciencesÜrümqiChina
  2. 2.INRA (French National Institute for Agricultural Research)University Côte d’Azur, CNRS, UMR 1355-7254Sophia AntipolisFrance
  3. 3.Department of Crop ProtectionHochschule Geisenheim UniversityGeisenheimGermany
  4. 4.UMR 1121 UL-INRA Agronomie et EnvironnementVandoeuvre-lès-NancyFrance
  5. 5.UR1115 PSH, INRAAvignonFrance
  6. 6.State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life SciencesHubei UniversityWuhanChina

Personalised recommendations