Behavioral response of the generalist predator Orius insidiosus to single and multiple herbivory by two cell content-feeding herbivores on rose plants

  • Ana Luiza V. Sousa
  • Diego B. Silva
  • Guilherme G. Silva
  • José Mauricio S. Bento
  • Maria Fernanda G. V. PenãflorEmail author
  • Brígida Souza
Original Paper


Multiple herbivory by arthropods with distinct feeding modes often reduces the attractiveness of herbivore-induced plant volatiles to the third trophic level, while herbivory by two species with the same feeding mode yields variable effects. So far, only few studies have examined multiple herbivory with two cell-content feeders. Here, we addressed the effect of multiple herbivory in rose plants by two cell-content feeders, Tetranychus urticae Koch (Acari: Tetranychidae) and Frankliniella insularis (Franklin) (Thysanoptera: Thripidae), on the olfactory preference of the minute pirate bug Orius insidiosus (Say) (Hemiptera: Anthocoridae), a generalist predator, to herbivore-induced plant volatiles (HIPVs). Additionally, we investigated whether the predator’s olfactory preference for HIPVs emitted by rose plants is associated with its feeding preference and prey quality. Y-tube olfactometer assays revealed that O. insidiosus was equally attracted to volatiles emitted by mite- or thrips-infested roses. Although HIPV blends from single-infested and multiple-infested rose plants differed in qualitative and quantitative terms, the minute pirate bug did not discriminate the odors of thrips- or mite-infested plants from multiple-infested plants. Congruent to the olfactory preference toward HIPVs, O. insidiosus did not show preference for either prey species, but consumed larger numbers of spider mites than thrips to complete its development. Therefore, our results showed that multiple herbivory by two cell-content feeders do not change the attractiveness of HIPV emissions compared to those of single-infested rose plants, and that lack of preference of the minute pirate bug to HIPV emissions induced by either spider mites or thrips favors the location of suitable prey.


Anthocoridae Flower thrips Minute pirate bug Spider mite Tetranychidae Thripidae 



We thank Arodi Prado Favaris for technical assistance, Dr. Jordano Salamanca for helping with data analysis, and Luís Carlos da Silva (Flora Minas—Itapeva, MG, Brazil) for supplying rose seedlings. This study was financially supported by the National Institute of Science and Technology (INCT) Semiochemicals in Agriculture (Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq, Process 465511/2014-7, and Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP, Process 2014/50871-0). A.L.V.S was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), B.S. by CNPq (PQ 310971-2013-6), and D.B.S. by FAPESP (Process 2016/12771-0).

Supplementary material

11829_2019_9729_MOESM1_ESM.docx (17 kb)
Electronic supplementary material 1 (DOCX 17 kb)


  1. Abe H, Shimoda T, Ohnishi J, Kugimiya S, Narusaka M, Seo S, Narusaka Y, Tsuda S, Kobayashi M (2009) Jasmonate-dependent plant defense restricts thrips performance and preference. BMC Plant Biol 9:97PubMedPubMedCentralCrossRefGoogle Scholar
  2. Allison JD, Hare JD (2009) Learned and naïve natural enemy responses and the interpretation of volatile organic compounds as cues or signals. New Phytol 184:768–782PubMedCrossRefPubMedCentralGoogle Scholar
  3. Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135:2025–2037PubMedPubMedCentralCrossRefGoogle Scholar
  4. Arab A, Trigo JR, Lourenção AL, Peixoto AM, Ramos F, Bento JMS (2007) Differential attractiveness of potato tuber volatiles to Phthorimaea operculella (Gelechiidae) and the predator Orius insidiosus (Anthocoridae). J Chem Ecol 33:1845–1855PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bueno VHP (2009) Desenvolvimento e criação massal de percevejos predadores Orius. In: Bueno VHP (ed) Controle Biológico de Pragas: produção massal e controle de qualidade, 2nd edn. Editora UFLA, LavrasGoogle Scholar
  6. Bueno VHP, Mendes SM, Carvalho LM (2006) Evaluation of a rearing-method for the predator Orius insidiosus. Bull Insectol 59:1–6Google Scholar
  7. Bueno VHP, Silva AR, Carvalho LM, Moura N (2009) Control of thrips with Orius insidiosus in greenhouse cut roses: use of a banker plant improves the performance of the predator. IOBC/WPRS Bull 49:183–187Google Scholar
  8. Bukovinszky T, Poelman EH, Kamp A, Hemerik L, Prekatsakis G, Dicke M (2012) Plants under multiple herbivory: consequences for parasitoid search behaviour and foraging efficiency. Anim Behav 83:501–509CrossRefGoogle Scholar
  9. Carvalho LM, Bueno VHP, Mendes SM (2006) Ocorrência e flutuação populacional de tripes, pulgões e inimigos naturais em crisântemo de corte em casa de vegetação. Bragantia 65:139–146CrossRefGoogle Scholar
  10. Carvalho LM, Bueno VHP, Almeida EFA, Reis SN, Lessa MA (2013) Principais pragas em cultivo de roseira: reconhecimento e controle. Circ Técnica 157:1–7Google Scholar
  11. Cloutier C, Johnson SG (1993) Predation by Orius tristicolor (Hemiptera: Anthocoridae) on Phytoseiulus persimilis (Acarina: Phytoseiidae): testing for compatibility between biocontrol agents. Environ Entomol 22:477–482CrossRefGoogle Scholar
  12. Cook D, Herbert A, Akin DS, Reed J (2011) Biology, crop injury, and management of thrips (Thysanoptera: Thripidae) infesting cotton seedlings in the United States. J Integ Pest Mngmt 2(2):B1–B9. CrossRefGoogle Scholar
  13. De Boer JG (2004) Carnivore attraction to herbivore-induced plant volatiles: effects of mixing volatile blends and multiple infestation of plants. PhD Thesis, Wageningen University, The NetherlandsGoogle Scholar
  14. De Boer JG, Hordijk CA, Posthumus MA, Dicke M (2008) Prey and non- prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J Chem Ecol 34:281–290PubMedPubMedCentralCrossRefGoogle Scholar
  15. Delphia CM, Mescher MC, De Moraes CM (2007) Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33:997–1012PubMedCrossRefPubMedCentralGoogle Scholar
  16. Dicke M, Hilker M (2003) Induced plant defenses: from molecular biology to evolutionary ecology. Basic Appl Ecol 4:3–14CrossRefGoogle Scholar
  17. Dicke M, van Loon JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249CrossRefGoogle Scholar
  18. Dicke M, van Beek TA, Posthumus MA, Ben Dom N, van Bokhoven H, De Groot AE (1990) Isolation and identification of volatile kairomone that affects acarine predator–prey interactions. Involvement of host plant in its production. J Chem Ecol 16:381–396PubMedCrossRefPubMedCentralGoogle Scholar
  19. Dicke M, van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324PubMedCrossRefPubMedCentralGoogle Scholar
  20. Drukker B, Bruin J, Sabelis MW (2000) Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiol Entomol 25:260–265CrossRefGoogle Scholar
  21. Escobar-Bravo R, Klinkhamer PG, Leiss KA (2017) Induction of jasmonic acid-associated defenses by thrips alters host suitability for conspecifics and correlates with increased trichome densities in tomato. Plant Cell Physiol 58:622–634PubMedPubMedCentralCrossRefGoogle Scholar
  22. Gebreziher HF, Nakamuta K (2016) A mixture of herbivore-induced plant volatiles from multiple host plant species enhances the attraction of a predatory bug under field-cage conditions. Arthropod-Plant Interact 10:507–515CrossRefGoogle Scholar
  23. Gols R, Veenemans C, Potting RPJ, Smid HM, Dicke M, Harvey JA, Bukovinszky T (2012) Variation in the specificity of plant volatiles and their use by a specialist and a generalist parasitoid. Anim Behav 83:1231–1242CrossRefGoogle Scholar
  24. Herbert HJ (1981) Biology, life tables, and innate capacity for increase of the twospotted spider mite, Tetranychus urticae (Acarina: Tetranychidae). Can Entomol 113:371–378CrossRefGoogle Scholar
  25. James DG (2003) Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ Entomol 32:977–982CrossRefGoogle Scholar
  26. James DG (2005) Further evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. J Chem Ecol 31:493–507CrossRefGoogle Scholar
  27. James DG, Price TS (2004) Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 30:1613–1628PubMedCrossRefPubMedCentralGoogle Scholar
  28. Jander R (1963) Insect orientation. Ann Rev Entomol 8:95–114CrossRefGoogle Scholar
  29. 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 135:483–495PubMedPubMedCentralCrossRefGoogle Scholar
  30. Kawazu K, Mochizuki A, Sato Y et al (2012) Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod-Plant Interact 6:221–230CrossRefGoogle Scholar
  31. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144PubMedCrossRefPubMedCentralGoogle Scholar
  32. Kroes A, Stam JM, David A et al (2016) Plant-mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage. Plant Biol 18:981–991PubMedCrossRefPubMedCentralGoogle Scholar
  33. Li CY, Williams MM, Loh YT, Lee GI, Howe GA (2002) Resistance of cultivated tomato to cell content-feeding herbivores is regulated by octadecanoid-signaling pathway. Plant Physiol 130:494–503PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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 59:707–718CrossRefGoogle Scholar
  35. Mallinger RE, Hogg DB, Gratton C (2011) Methyl salicylate attracts natural enemies and reduces populations of soybean aphids (Hemiptera: Aphididae) in soybean agroecosystems. J Econ Entomol 104:115–124PubMedCrossRefPubMedCentralGoogle Scholar
  36. McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310CrossRefGoogle Scholar
  37. Mendes SM, Bueno VHP, Argolo VM, Silveira LCP (2002) Type of prey influences biology and consumption rate of Orius insidiosus (Say) (Hemiptera, Anthocoridae). Rev Bras Entomol 46:99–103CrossRefGoogle Scholar
  38. Moayeri HRS, Ashouri A, Brødsgaard HF, Enkegaard A (2006) Odour-mediated preference and prey preference of Macrolophus caliginosus between spider mites and green peach aphids. J Appl Entomol 130:504–508CrossRefGoogle Scholar
  39. Mochizuki M, Yano E (2007) Olfactory response of the anthocorid predatory bug Orius sauteri to thrips-infested eggplants. Entomol Exp Appl 123:57–62CrossRefGoogle Scholar
  40. Mumm R, Dicke M (2010) Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can J Zool 88:628–667CrossRefGoogle Scholar
  41. Oliveira MS, Pareja M (2014) Attraction of a ladybird to sweet pepper damaged by two aphid species simultaneously or sequentially. Arthropod-Plant Interact 8:547–555CrossRefGoogle Scholar
  42. Pareja M, Pinto-Zevallos DM (2016) Impacts of induction of plant volatiles by individual and multiple stresses across trophic levels. In: Blande JD, Glinwood R (eds) Signaling and communication in plants, 1st edn. Springer, New YorkGoogle Scholar
  43. Peñaflor MFGV, Gonçalves FG, Colepicolo C, Sanches PA, Bento JMS (2017) Effects of single and multiple herbivory by host and non-host caterpillars on the attractiveness of herbivore-induced volatiles of sugarcane to the generalist parasitoid Cotesia flavipes. Entomol Exp Appl 165:83–93CrossRefGoogle Scholar
  44. Reis PR, Alves EB, Souza EO (1997) Biologia do ácaro-vermelho do cafeeiro Oligonychus ilicis (McGregor, 1917). Ciênc Tecnol 21:260–266Google Scholar
  45. Rodriguez-Saona C, Crafts-Brandner SJ, Cañas L (2003) Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J Chem Ecol 29:2521–2532CrossRefGoogle Scholar
  46. Rodriguez-Saona C, Kaplan I, Braasch J, Chinnasamy D, Williams L (2011) Field responses of predaceous arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biol Control 59:294–303CrossRefGoogle Scholar
  47. Salamanca J, Pareja M, Rodriguez-Saona C, Resende ALS, Souza B (2015) Behavioral responses of adult lacewings, Chrysoperla externa, to a rose-aphid-coriander complex. Biol Control 80:103–112CrossRefGoogle Scholar
  48. Santos RC, Peñaflor MFGV, Sanches PA, Nardi C, Bento JMS (2016) The effects of Gibberella zeae, Barley Yellow Dwarf Virus, and co-infection on Rhopalosiphum padi olfactory preference and performance. Phytoparasitica 44:47–54CrossRefGoogle Scholar
  49. Schausberger P (2018) Herbivore-associated bacteria as potential mediators and modifiers of induced plant defense against spider mites and thrips. Front Plant Sci 9:1107. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Shalileh S, Ogada PA, Moualeu DP, Poehling HM (2016) Manipulation of Frankliniella occidentalis (Thysanoptera: Thripidae) by tomato spotted wilt virus (tospovirus) via the host plant nutrients to enhance its transmission and spread. Environ Entomol 45:1235–1242PubMedPubMedCentralCrossRefGoogle Scholar
  51. Shiojiri K, Takabayashi J, Yano S, Takafuji A (2000) Flight response of parasitoids toward plant-herbivore complexes: a comparative study of two parasitoid-herbivore systems on cabbage plants. Appl Entomol Zool 35:87–92CrossRefGoogle Scholar
  52. Shiojiri K, Takabayashi J, Yano S, Takafuji A (2001) Infochemically mediated tritrophic interaction webs on cabbage plants. Popul Ecol 43:23–29CrossRefGoogle Scholar
  53. 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 7:1–13Google Scholar
  54. Silveira LCP, Bueno VHP, van Lenteren JC (2004) Orius insidiosus as biological control agent of Thrips in greenhouse chrysanthemums in the tropics. Bull Insectol 57:103–109Google Scholar
  55. Steenbergen M, Abd-el-Haliem A, Bleeker P et al (2018) Thrips advisor: exploiting thrips-induced defences to combat pests on crops. J Exp Bot 69:1837–1848PubMedCrossRefPubMedCentralGoogle Scholar
  56. Stepanycheva EA, Petrova MO, Chermenskaya TD et al (2014) The behavioral response of the predatory bug Orius laevigatus Fieber (Heteroptera, Anthocoridae) to Synthetic Volatiles. Entomol Rev 94:510–517CrossRefGoogle Scholar
  57. Stepanycheva EA, Petrova MO, Chermenskaya TD, Shamshev IV (2016) Effect of methyl salicylate on behavioral responses of insects in a forest park. Entomol Rev 96:295–300CrossRefGoogle Scholar
  58. Stout MJ, Workman KV, Bostock RM, Duffey SS (1998) Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74–81CrossRefGoogle Scholar
  59. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 30:1251–1253CrossRefGoogle Scholar
  60. Turlings TCJ, Tumlinson JH, Heath RR, Proveaux AT, Doolittle RE (1991) Isolation and identification of allelochemicals that attract the larval parasitoid Cotesia marginiventris (Cresson) to the micro-habitat of one of its hosts. J Chem Ecol 17:2235–2251PubMedCrossRefPubMedCentralGoogle Scholar
  61. van Oudenhove L, Mailleret L, Fauvergue X (2017) Infochemical use and dietary specialization in parasitoids: a meta-analysis. Ecol Evol 7:4804–4811PubMedPubMedCentralCrossRefGoogle Scholar
  62. Villarroel CA, Jonckheere W, Alba JM et al (2016) Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction. Plant J 86:119–131PubMedCrossRefPubMedCentralGoogle Scholar
  63. Xu X, Borgemeister C, Poehling HM (2006) Interactions in the biological control of western flower thrips Frankliniella occidentalis (Pergande) and two-spotted spider mite Tetranychus urticae Koch by the predatory bug Orius insidiosus Say on beans. Biol Control 36:57–64CrossRefGoogle Scholar
  64. Zhang PJ, Zheng SJ, van Loon JJA, Boland W, David A, Mumm R, Dicke M (2009) Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proc Natl Acad Sci USA 106:21202–21207PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Laboratory of Chemical Ecology of Insect-Plant Interactions (LEQIIP), Department of EntomologyFederal University of Lavras (UFLA)LavrasBrazil
  2. 2.Department of Entomology and AcarologyUniversity of São Paulo, “Luiz de Queiroz” College of Agriculture (ESALQ/USP)PiracicabaBrazil

Personalised recommendations