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Herbivore-Dependent Induced Volatiles in Pear Plants Cause Differential Attractive Response by Lacewing Larvae

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Abstract

Biological control may benefit from the behavioral manipulation of natural enemies using volatile organic compounds (VOCs). Among these, herbivore-induced plant volatiles (HIPVs) provide potential tools for attracting or retaining predators and parasitoids of insect pests. This work aimed to characterize the VOCs emitted by pear plants in response to attack by Cacopsylla bidens (Hemiptera: Psyllidae), a major pest in pear orchards, to compare these with VOCs induced by a leaf chewing insect, Argyrotaenia sphaleropa (Lepidoptera: Tortricidae), and to evaluate the behavioral response of Chrysoperla externa (Neuroptera: Chrysopidae) to HIPVs from pear plants damaged by either herbivore. The results demonstrated that plants damaged by the pear psylla emitted VOC blends with increased amounts of aliphatic aldehydes. Leafroller damage resulted in increased amounts of benzeneacetonitrile, (E)-4,8-dimethylnona-1,3,7-triene, β-ocimene and caryophyllene. In olfactometer bioassays, larvae of C. externa were attracted to herbivore-damaged plants when contrasted with undamaged plants. When plant odors from psylla-damaged were contrasted with those of leafroller-damaged plants, C.externa preferred the former, also showing shorter response lag-times and higher response rates when psylla-damaged plants were present. Our results suggest that pear plants respond to herbivory by modifying their volatile profile, and that psylla-induced volatiles may be used as prey-specific chemical cues by chrysopid larvae. Our study is the first to report HIPVs in pear plants attacked by C. bidens, as well as the attraction of C. externa to psyllid-induced volatiles.

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References

  • Aartsma Y, Bianchi FJ, van der Werf W, Poelman EH, Dicke M (2017) Herbivore-induced plant volatiles and tritrophic interactions across spatial scales. New Phytol 216:1054–1063. doi:https://doi.org/10.1111/nph.14475

    Article  PubMed  PubMed Central  Google Scholar 

  • Arimura G-i, Muroi A, Nishihara M (2012) Plant–plant–plant communications, mediated by (E)β-ocimene emitted from transgenic tobacco plants, prime indirect defense responses of lima beans. J Plant Interact 7:193–196. doi:https://doi.org/10.1080/17429145.2011.650714

    Article  CAS  Google Scholar 

  • Arimura G-i, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515. doi:https://doi.org/10.1038/35020072

    Article  CAS  PubMed  Google Scholar 

  • Ayelo PM, Pirk CW, Yusuf AA, Chailleux A, Mohamed SA, Deletre E (2021a) Exploring the kairomone-based foraging behaviour of natural enemies to enhance biological control: a review. Front Ecol Evol 9:641974. doi:https://doi.org/10.3389/fevo.2021.641974

    Article  Google Scholar 

  • Ayelo PM, Yusuf AA, Pirk CW, Chailleux A, Mohamed SA, Deletre E (2021b) Terpenes from herbivore-induced tomato plant volatiles attract Nesidiocoris tenuis (Hemiptera: Miridae), a predator of major tomato pests. Pest Manag Sci 77:5255–5267. doi:https://doi.org/10.1002/ps.6568

    Article  CAS  PubMed  Google Scholar 

  • Badra Z, Larsson Herrera S, Cappellin L, Biasioli F, Dekker T, Angeli S, Tasin M (2021) Species-specific induction of Plant Volatiles by two aphid species in Apple: real time measurement of Plant Emission and attraction of Lacewings in the wind tunnel. J Chem Ecol 47:653–663. doi:https://doi.org/10.1007/s10886-021-01288-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models using lme4. J Stat Softw 67:1–48. doi:https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  • Bell WJ (1990) Searching behavior patterns in insects. Ann Rev Entomol 35:447–467. doi:https://doi.org/10.1146/annurev.en.35.010190.002311

    Article  Google Scholar 

  • Berrada S, Fournier D, Cuany A, Nguyen T (1994) Identification of resistance mechanisms in a selected laboratory strain of Cacopsylla pyri (Homoptera: Psyllidae): altered acetylcholinesterase and detoxifying oxidases. Pestic Biochem Physiol 48:41–47. doi:https://doi.org/10.1006/pest.1994.1005

    Article  CAS  Google Scholar 

  • Bidart-Bouzat MG, Kliebenstein D (2011) An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores. Oecologia 167:677–689

    Article  PubMed  Google Scholar 

  • Birkett M, Chamberlain K, Guerrieri E, Pickett J, Wadhams L, Yasuda T (2003) Volatiles from whitefly-infested plants elicit a host-locating response in the parasitoid, Encarsia formosa. J Chem Ecol 29:1589–1600

    Article  CAS  PubMed  Google Scholar 

  • Borrero-Echeverry F, Becher PG, Birgersson G, Bengtsson M, Witzgall P, Saveer AM (2015) Flight attraction of Spodoptera littoralis (Lepidoptera, Noctuidae) to cotton headspace and synthetic volatile blends. Front Ecol Evol 3. doi:https://doi.org/10.3389/fevo.2015.00056

  • Brambilla A et al (2022) Immunity-associated volatile emissions of β-ionone and nonanal propagate defence responses in neighbouring barley plants. J Exp Bot 73:615–630

    Article  CAS  PubMed  Google Scholar 

  • Buès R, Boudinhon L, Toubon JF (2003) Resistance of pear psylla (Cacopsylla pyri L.; Hom., Psyllidae) to deltamethrin and synergism with piperonyl butoxide. Journal of Applied Entomology 127:305–312

  • Burckhardt D, Hodkinson I (1986) A revision of the west Palaearctic pear psyllids (Hemiptera: Psyllidae). Bull Entomol Res 76:119–132

    Article  Google Scholar 

  • Cascone P, Iodice L, Maffei ME, Bossi S, Arimura G-i, Guerrieri E (2015) Tobacco overexpressing β-ocimene induces direct and indirect responses against aphids in receiver tomato plants. J Plant Physiol 173:28–32

    Article  CAS  PubMed  Google Scholar 

  • Civolani S (2012) The past and present of pear protection against the pear psylla, Cacopsylla pyri L. Insecticides Pest Eng 65:385–408

    Google Scholar 

  • Civolani S et al (2010) Survey of susceptibility to abamectin of pear psylla (Hemiptera: Psyllidae) in northern Italy. J Econ Entomol 103:816–822

    Article  CAS  PubMed  Google Scholar 

  • Conti E et al (2008) Changes in the volatile profile of Brassica oleracea due to feeding and oviposition by Murgantia histrionica (Heteroptera: Pentatomidae). Eur J Entomol 105:839

    Article  CAS  Google Scholar 

  • Danner H et al (2011) Four terpene synthases produce major compounds of the gypsy moth feeding-induced volatile blend of Populus trichocarpa. Phytochemistry 72:897–908

    Article  CAS  PubMed  Google Scholar 

  • Danner H, Desurmont GA, Cristescu SM, van Dam NM (2018) Herbivore-induced plant volatiles accurately predict history of coexistence, diet breadth, and feeding mode of herbivores. New Phytol 220:726–738

    Article  CAS  PubMed  Google Scholar 

  • Daugherty MP, Briggs CJ, Welter SC (2007) Bottom-up and top-down control of pear psylla (Cacopsylla pyricola): fertilization, plant quality, and the efficacy of the predator Anthocoris nemoralis. Biol Control 43:257–264

    Article  Google Scholar 

  • de Oliveira CM et al (2019) Associative learning in immature lacewings (Ceraeochrysa cubana). Entomol Exp Appl 167:775–783

    Article  Google Scholar 

  • Degenhardt J, Gershenzon J (2000) Demonstration and characterization of (E)-nerolidol synthase from maize: a herbivore-inducible terpene synthase participating in (3E)-4, 8-dimethyl-1, 3, 7-nonatriene biosynthesis. Planta 210:815–822

    Article  CAS  PubMed  Google Scholar 

  • Dicke M (1994) Local and systemic production of volatile herbivore-induced terpenoids: their role in plant-carnivore mutualism. J Plant Physiol 143:465–472

    Article  CAS  Google Scholar 

  • Dicke M (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? In: Proceedings of the 10th international symposium on insect-plant relationships, Springer, pp 131–142

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175

    Article  CAS  PubMed  Google Scholar 

  • Drukker B, Bruin J, Sabelis MW (2000) Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiol Entomol 25:260–265

    Article  CAS  Google Scholar 

  • Drukker B, Scutareanu P, Sabelis M (1995) Do anthocorid predators respond to synomones from psylla-infested pear trees under field conditions? Entomol Exp Appl 77:193–203

    Article  Google Scholar 

  • Du Y-W, Shi X-B, Zhao L-C, Yuan G-G, Zhao W-W, Huang G-H, Chen G (2022) Chinese Cabbage Changes its release of Volatiles to defend against Spodoptera litura. Insects 13:73

    Article  PubMed  PubMed Central  Google Scholar 

  • Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. CRC Crit Rev Plant Sci 25:417–440

    Article  CAS  Google Scholar 

  • El-Sayed A, Knight A, Basoalto E, Suckling D (2018) Caterpillar‐induced plant volatiles attract conspecific herbivores and a generalist predator. J Appl Entomol 142:495–503

    Article  CAS  Google Scholar 

  • Farré-Armengol G, Filella I, Llusià J, Peñuelas J (2017) β-Ocimene, a Key Floral and Foliar Volatile involved in multiple interactions between plants and other organisms. Molecules 22:1148

    Article  PubMed  PubMed Central  Google Scholar 

  • Fellowes MDE, van Alphen JJM, Jervis MA (2005) Foraging Behaviour. In: Jervis MA (ed) Insects as natural enemies: a practical perspective. Springer Netherlands, Dordrecht, pp 1–71. doi:https://doi.org/10.1007/978-1-4020-2625-6_1

    Chapter  Google Scholar 

  • Flint H, Salter S, Walters S (1979) Caryophyllene: an attractant for the green lacewing. Environ Entomol 8:1123–1125

    Article  CAS  Google Scholar 

  • Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169

    Article  CAS  PubMed  Google Scholar 

  • Godard K-A, White R, Bohlmann J (2008) Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69:1838–1849

    Article  CAS  PubMed  Google Scholar 

  • Görg LM, Gallinger J, Gross J (2021) The phytopathogen ‘Candidatus Phytoplasma mali’alters apple tree phloem composition and affects oviposition behavior of its vector Cacopsylla picta. Chemoecology 31:31–45

    Article  Google Scholar 

  • Gross J, Jorge BCd, Gallinger J, Görg L, Maurer D, Rid M (2019) The chemistry of multitrophic interactions in phytoplasma disease systems and advances in control of psyllid vectors with semiochemicals. Phytopathogenic Mollicutes 9:157–158

    Article  Google Scholar 

  • Guo H, Wang C-Z (2019) The ethological significance and olfactory detection of herbivore-induced plant volatiles in interactions of plants, herbivorous insects, and parasitoids. Arthropod-Plant Interact 13:161–179

    Article  Google Scholar 

  • Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61

    Article  CAS  PubMed  Google Scholar 

  • Heimpel GE, Asplen MK (2011) A ‘Goldilocks’ hypothesis for dispersal of biological control agents. Biocontrol 56:441–450

    Article  Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398

    Article  Google Scholar 

  • Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184

    Article  CAS  PubMed  Google Scholar 

  • Horton DR (1999) Monitoring of pear psylla for pest management decisions and research. Integr Pest Manag Rev 4:1–20

    Article  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  CAS  PubMed  Google Scholar 

  • James DG (2003) Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing, Chrysopa nigricornis. J Chem Ecol 29:1601–1609

    Article  CAS  PubMed  Google Scholar 

  • Jayanthi PK, Subramoniam A, Kumar PS, Jayanthimala B, Rekha A (2021) Do conspecific herbivores track resource depletion through host phenology-specific HIPVs? Curr Sci 121:286

    Article  CAS  Google Scholar 

  • Jones VP et al (2016) Evaluating plant volatiles for monitoring natural enemies in apple, pear and walnut orchards. Biol Control 102:53–65

    Article  CAS  Google Scholar 

  • Jones VP, Steffan SA, Wiman NG, Horton DR, Miliczky E, Zhang Q-H, Baker CC (2011) Evaluation of herbivore-induced plant volatiles for monitoring green lacewings in Washington apple orchards. Biol Control 56:98–105

    Article  Google Scholar 

  • Kaplan I (2012) Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire? Biol Control 60:77–89. doi:https://doi.org/10.1016/j.biocontrol.2011.10.017

    Article  Google Scholar 

  • Kelly JL, Hagler JR, Kaplan I (2014) Semiochemical lures reduce emigration and enhance pest control services in open-field predator augmentation. Biol Control 71:70–77. doi:https://doi.org/10.1016/j.biocontrol.2014.01.010

    Article  CAS  Google Scholar 

  • Koski TM et al (2015) Do insectivorous birds use volatile organic compounds from plants as olfactory foraging cues? Three experimental tests. Ethology 121:1131–1144

    Article  Google Scholar 

  • Knight AL, Mujica V, Larsson Herrera S, Tasin M (2019) Monitoring codling moth (Lepidoptera: Tortricidae) with a four-component volatile blend compared to a sex pheromone‐based blend. J Appl Entomol 143(9):942–947

    Article  CAS  Google Scholar 

  • Knight AL, Light DM, Trimble RM (2011) Identifying (E)-4, 8-dimethyl-1, 3, 7-nonatriene plus acetic acid as a new lure for male and female codling moth (Lepidoptera: Tortricidae). Environ Entomol 40(2):420–430

    Article  CAS  Google Scholar 

  • Li T, Blande JD (2017) Volatile-mediated within-plant signaling in hybrid aspen: required for systemic responses. J Chem Ecol 43:327–338

    Article  CAS  PubMed  Google Scholar 

  • Lim UT, Ben-Yakir D (2020) Visual sensory systems of predatory and parasitic arthropods. Biocontrol Sci Technol 30:728–739. doi:https://doi.org/10.1080/09583157.2020.1752362

    Article  Google Scholar 

  • Lucchi A, Loni A, Gandini LM, Scaramozzino P, Ioriatti C, Ricciardi R, Schearer PW (2017) Using herbivore-induced plant volatiles to attract lacewings, hoverflies and parasitoid wasps in vineyards: achievements and constraints. Bull Insectol 70:273–282

    Google Scholar 

  • Majithia D, Metrani R, Dhowlaghar N, Crosby KM, Patil BS (2021) Assessment and classification of volatile profiles in melon breeding lines using headspace solid-phase microextraction coupled with gas chromatography-mass spectrometry. Plants 10:2166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayer CJ, Vilcinskas A, Gross J (2011) Chemically mediated multitrophic interactions in a plant-insect vector-phytoplasma system compared with a partially nonvector species. Agricultural and Forest Entomology 13: 25-35 

    Article  Google Scholar 

  • Mayer CJ, Vilcinskas A, Gross J (2008a) Phytopathogen Lures Its Insect Vector by Altering Host Plant Odor. Journal of Chemical Ecology 34: 1045-1049 

  • Mayer CJ, Vilcinskas A, Gross J (2008b) Pathogen-induced Release of Plant Allomone Manipulates Vector Insect Behavior. Journal of Chemical Ecology 34: 1518-1522 

  • Midon P, Idalicia E (2021) Preferencia de tamaño de presa y respuesta funcional de Chrysoperla externa (Neuroptera: Chrysopidae) sobre Diaphorina citri (Hemiptera: Psyllidae). Dissertation, Universidad de La Republica, Uruguay

  • Mills NJ, Heimpel GE (2018) Could increased understanding of foraging behavior help to predict the success of biological control? Curr Opin Insect Sci 27:26–31. doi:https://doi.org/10.1016/j.cois.2018.02.013

    Article  PubMed  Google Scholar 

  • Moayeri HR, Ashouri A, Brødsgaard HF, Enkegaard A (2007) Males of the predatory mirid bug Macrolophus caliginosus exploit plant volatiles induced by conspecifics as a sexual synomone. Entomol Exp Appl 123:49–55

    Article  CAS  Google Scholar 

  • Mohammed K, Agarwal M, Li B, Newman J, Liu T, Ren Y (2020) Evaluation of d-Limonene and β-Ocimene as Attractants of Aphytis melinus (Hymenoptera: Aphelinidae), a parasitoid of Aonidiella aurantii (Hemiptera: Diaspididae) on Citrus spp. Insects 11:44

    Article  PubMed  PubMed Central  Google Scholar 

  • Muroi A, Ramadan A, Nishihara M, Yamamoto M, Ozawa R, Takabayashi J, Arimura G-i (2011) The composite effect of transgenic plant volatiles for acquired immunity to herbivory caused by inter-plant communications. PLoS ONE 6:e24594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Núñez S, Scatoni I (2013) Tecnología disponible para el manejo de plagas en frutales de hoja caduca. INIA, Montevideo, Uruguay

    Google Scholar 

  • Oksanen J et al (2022) Vegan: Community Ecology Package. R package version 26 – 2

  • Pålsson J, Porcel M, Dekker T, Tasin M (2022) Attract, reward and disrupt: responses of pests and natural enemies to combinations of habitat manipulation and semiochemicals in organic apple. J Pest Sci 95:619–631

    Article  Google Scholar 

  • Pappas ML et al (2017) Induced plant defences in biological control of arthropod pests: a double-edged sword. Pest Manag Sci 73:1780–1788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson HM, Ray S, Ali JG, Krawczyk G (2022) Feeding and oviposition by the brown marmorated stink bug, Halyomorpha halys (Stål) induce direct and systemic changes in volatile compound emissions from potted peach and tree of heaven. Arthropod-Plant Interact 16:227–247. doi:https://doi.org/10.1007/s11829-022-09893-1

    Article  CAS  Google Scholar 

  • Piesik D, Wenda-Piesik A (2015) Sitophilus granarius responses to blends of five groups of cereal kernels and one group of plant volatiles. J Stored Prod Res 62:36–39

    Article  Google Scholar 

  • Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Preti M, Knight AL, Favaro R, Basoalto E, Tasin M, Angeli S (2021) Comparison of new kairomone-based lures for Cydia pomonella (Lepidoptera: Tortricidae) in Italy and USA. Insects 12(1):72

    Article  PubMed  PubMed Central  Google Scholar 

  • Rehermann G, Altesor P, McNeil JN, González A (2016) Conspecific females promote calling behavior in the noctuid moth, Pseudaletia adultera. Entomologia Experimentalis et Applicata 159:362-369 

    Article  Google Scholar 

  • R Core Team (2022) R: A language and environment for statistical computing. Vienna, Austria

  • Rid M, Mesca C, Ayasse M, Gross J (2016) Apple proliferation phytoplasma influences the pattern of plant volatiles emitted depending on pathogen virulence. Front Ecol Evol 3:152

    Article  Google Scholar 

  • Riffel A et al (2021) Exposure to sugarcane borer-induced plant volatile (E)‐caryophyllene enhances parasitoid recruitment. Entomol Exp Appl 169:937–946

    Article  CAS  Google Scholar 

  • Rott A, Häckermann J, Brand N, Vallat A, Dorn S (2005) Parasitoid exploitation of the seasonal variation in host plant volatile emission for herbivore location. Entomol Exp Appl 115:199–205

    Article  CAS  Google Scholar 

  • Rowen E, Kaplan I (2016) Eco-evolutionary factors drive induced plant volatiles: a meta‐analysis. New Phytol 210:284–294

    Article  CAS  PubMed  Google Scholar 

  • Sanchez JA, Carrasco-Ortiz A, López‐Gallego E, Ramírez‐Soria MJ, La Spina M, Ortín‐Angulo MC, Ibáñez‐Martínez H (2022) Density thresholds and the incorporation of biocontrol into decision‐making to enhance the control of Cacopsylla pyri in pear (cv. Ercolini) orchards. Pest Manag Sci 78:116–125

    Article  CAS  PubMed  Google Scholar 

  • Sarkar N, Karmakar A, Barik A (2016) Volatiles of Solena amplexicaulis (Lam.) Gandhi leaves influencing attraction of two generalist insect herbivores. J Chem Ecol 42:1004–1015

    Article  CAS  PubMed  Google Scholar 

  • Scutareanu P, Drukker B, Bruin J, Posthumus M, Sabelis M (1996) Leaf volatiles and polyphenols in pear trees infested by psylla pyricola. Evidence of simultaneously induced responses. Chemoecology 7:34–38

    Article  CAS  Google Scholar 

  • Scutareanu P, Drukker B, Bruin J, Posthumus MA, Sabelis MW (1997) Volatiles from psylla-infested pear trees and their possible involvement in attraction of anthocorid predators. J Chem Ecol 23:2241–2260

    Article  CAS  Google Scholar 

  • Seemüller E, Schneider B (2004) ‘Candidatus Phytoplasma mali’,‘Candidatus Phytoplasma pyri’and ‘Candidatus Phytoplasma prunorum’, the causal agents of apple proliferation, pear decline and European stone fruit yellows, respectively. International Journal of Systematic and Evolutionary Microbiology 54:1217–1226

  • Silva DB, Weldegergis BT, Van Loon JJ, Bueno VH (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 43:53–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sigsgaard L, Esbjerg P, Philipsen H (2006) Experimental releases of Anthocoris nemoralis F. and Anthocoris nemorum (L.)(Heteroptera: Anthocoridae) against the pear psyllid Cacopsylla pyri L.(Homoptera: Psyllidae) in pear. Biol Control 39:87–95

    Article  Google Scholar 

  • Simpson M et al (2011) Attract and reward: combining chemical ecology and habitat manipulation to enhance biological control in field crops. J Appl Ecol 48:580–590

    Article  Google Scholar 

  • 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 20:1329–1354

    Article  CAS  PubMed  Google Scholar 

  • Takabayashi J, Shiojiri K (2019) Multifunctionality of herbivory-induced plant volatiles in chemical communication in tritrophic interactions. Curr Opin Insect Sci 32:110–117. doi:https://doi.org/10.1016/j.cois.2019.01.003

    Article  PubMed  Google Scholar 

  • Tooker JF, O’Neal ME, Rodriguez-Saona C (2020) Balancing disturbance and conservation in agroecosystems to improve biological control. Ann Rev Entomol 65:81–100

    Article  CAS  Google Scholar 

  • Tóth M, Bozsik A, Szentkirályi F, Letardi A (2006) Phenylacetaldehyde: a chemical attractant for common green lacewings (Chrysoperla carnea sl, Neuroptera: Chrysopidae). Eur J Entomol 103:267

    Article  Google Scholar 

  • Tóth M, Szentkirályi F, Vuts J, Letardi A, Tabilio MR, Jaastad G, Knudsen GK (2009) Optimization of a phenylacetaldehyde-based attractant for common green lacewings (Chrysoperla carnea sl). J Chem Ecol 35:449–458

    Article  PubMed  Google Scholar 

  • Tougeron K, Iltis C, Renoz F, Albittar L, Hance T, Demeter S, Le Goff GJ (2021) Ecology and biology of the parasitoid Trechnites insidiosus and its potential for biological control of pear psyllids. Pest Manag Sci 77:4836–4847

    Article  CAS  PubMed  Google Scholar 

  • Turlings TC, Lengwiler UB, Bernasconi ML, Wechsler D (1998) Timing of induced volatile emissions in maize seedlings. Planta 207:146–152

    Article  CAS  Google Scholar 

  • Valle D, Burckhardt D, Mujica V, Zoppolo R, Morelli E (2017) The occurrence of the pear psyllid, Cacopsylla bidens (Šulc, 1907)(Insecta: Hemiptera: Psyllidae), in Uruguay. Check List 13:2088–2088

    Article  Google Scholar 

  • Valle D, Mujica V, Silvera M, Borges A, Zoppolo R, Morelli E (2021) Effect of the ground cover management on Cacopsylla bidens (Šulc, 1907) populations in pear orchards. In: XIII International Pear Symposium 1303, 2018. pp 375–380 doi: https://doi.org/10.17660/ActaHortic.2021.1303.52

  • Valle D, Cabrera N, Clavijo F, Mujica V, Gonzalez A, Siri M, Lavandero B (2022) Who is feeding on the pear psylla? Applying molecular ecology for the biological control of Cacopsylla bidens. Int J Pest Manage 68:390–401. doi:https://doi.org/10.1080/09670874.2022.2135181

    Article  Google Scholar 

  • Van Poecke RM, Posthumus MA, Dicke M (2001) Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol 27:1911–1928

    Article  PubMed  Google Scholar 

  • Vet LE, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Ann Rev Entomol 37:141–172

    Article  Google Scholar 

  • War AR, Sharma HC, Paulraj MG, War MY, Ignacimuthu S (2011) Herbivore induced plant volatiles: their role in plant defense for pest management. Plant Signal Behav 6:1973–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weissbecker B, Van Loon JJ, Dicke M (1999) Electroantennogram responses of a predator, Perillus bioculatus, and its prey, Leptinotarsa decemlineata, to plant volatiles. J Chem Ecol 25:2313–2325

    Article  CAS  Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  • Wyckhuys KA, Lu Y, Morales H, Vazquez LL, Legaspi JC, Eliopoulos PA, Hernandez LM (2013) Current status and potential of conservation biological control for agriculture in the developing world. Biol Control 65:152–167

    Article  Google Scholar 

  • Yang J-N, Wei J-N, Kang L (2021) Feeding of pea leafminer larvae simultaneously activates jasmonic and salicylic acid pathways in plants to release a terpenoid for indirect defense. Insect Sci 28:811–824. doi:https://doi.org/10.1111/1744-7917.12820

    Article  CAS  PubMed  Google Scholar 

  • Yi H-S, Heil M, Adame-Alvarez RM, Ballhorn DJ, Ryu C-M (2009) Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol 151:2152–2161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yi H-S, Ryu C-M, Heil M (2010) Sweet smells prepare plants for future stress: Airborne induction of plant disease immunity. Plant Signal Behav 5:528–531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu H, Zhang Y, Wu K, Gao XW, Guo YY (2008) Field-testing of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. Environ Entomol 37:1410–1415

    Article  CAS  PubMed  Google Scholar 

  • Zhang L et al (2020) Overexpression of the caryophyllene synthase gene GhTPS1 in cotton negatively affects multiple pests while attracting parasitoids. Pest Manag Sci 76:1722–1730

    Article  CAS  PubMed  Google Scholar 

  • Zoppolo R, Scatoni I, Duarte F, Mujica M, Gabard Z (2015) Area-wide pest management in deciduous fruits of southern Uruguay. In: International Symposium on Innovation in Integrated and Organic Horticulture (INNOHORT) 1137, pp 153–160

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Acknowledgements

The contribution of Carmen Rossini, Federico Rodrigo, Maria Eugenia Amorós, Hernan Groba, Anna Burgueño Paula Lagurara, Soledad Delgado and Evelin Pechi was particularly valued. The field and laboratory work of Mariana Silvera, Gaston Tejera, Gonzalo Vazquez, Jorge Secco, Jonathan Macchi and Peter Schlenzak was greatly appreciated. The involvement of Carolina Leoni, Diego Maeso and Roberto Zoppolo in all the stages of this work has been of great help in the development of this project.

Funding

This research was funded by Instituto Nacional de Investigación Agropecuaria, Project FR_21 (INIA Uruguay).

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All authors contributed to the study conception and design. D.V and V.M proceeded to collect the materials for the study. Statistical analyses were performed by D.V and chemical analysis were performed by A.G. All authors read and approved the final manuscript.

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Correspondence to D. Valle.

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Valle, D., Mujica, V. & Gonzalez, A. Herbivore-Dependent Induced Volatiles in Pear Plants Cause Differential Attractive Response by Lacewing Larvae. J Chem Ecol 49, 262–275 (2023). https://doi.org/10.1007/s10886-023-01403-8

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