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Chrysoperla externa (Hagen) (Neuroptera, Chrysopidae) is a good candidate for predation of Aleurodicus cocois (Curtis) (Hemiptera: Aleyrodidae) in cashew crop

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Abstract

A potential alternative to the use of chemicals for controlling phytophagous arthropods in agricultural environments is the use of biological control agents of natural occurrence. This study evaluated the functional response of first-instar larvae of Chrysoperla externa-fed eggs and nymphs of Aleurodicus cocois, as well as the olfactory response of the third-instar larvae of this predator to the volatiles of two genotypes (CCP 76 and PRO 143/7) of dwarf cashew induced by the herbivory of A. cocois. The volatile compounds emitted by the leaves of the two cashew genotypes, infested and non-infested by A. cocois, were analyzed by solid-phase microextraction coupled to GC–MS. Logistic regression indicated that first-instar larvae of C. externa exhibited a type II response when fed eggs and nymphs of A. cocois. The value of the attack rate (a') did not differ between prey, but the handling time (Th) was longer when the predator fed on nymphs. In the behavioral tests third-instar larvae of C. externa were able to distinguish and select the volatile signals emitted after the infestation of A. cocois, regardless of the cashew genotype evaluated. According to the volatile profiles of cashew genotypes infested by A. cocois, the compounds β-caryophyllene, allo-ocimene, neo-allo-ocimene, α-copaene, γ-muurolene, and δ-cadinene were released in large amounts by genotypes CCP 76 and PRO 143/7. Therefore, these compounds may be involved in the attractiveness of the predator. The results indicate that C. externa may be an effective biocontrol agent of A. cocois in cashew crop.

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References

  • Adams, R. P. (2007). Identification of essential oil components by gas chromatography/mass spectrometry (Vol. 456). Allured Publishing Corp.

  • Agrofit, 2022 - Sistema de Agrotróxicos Fitossanitários - Ministério da Agricultura, Pecuária e Abastecimento - Coordenação Geral de Agrotóxicos e Afins/DFIA/DAS.http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons (accessed 25 January 2022).

  • Albuquerque GS, Tauber CA, Tauber MJ (2001) Chrysoperla externa and Ceraeochrysa spp.: potential for biological control in the New World tropics and subtropics. In: McEwen PK, New TR, Whittington AE (eds) Lacewings in the crop environment. Cambridge University Press, Cambridge, pp 408–423

  • Alfaia JP, Melo LL, Monteiro NV, Lima DB, Melo JWS (2018) Functional response of the predaceous mites Amblyseius largoensis and Euseius concordis when feeding on eggs of the cashew tree giant whitefly Aleurodicus cocois. Syst Appl Acarol 23:1559–2156. https://doi.org/10.11158/saa.23.8.6

    Article  Google Scholar 

  • Auad AM, Freitas SD, Barbosa LR (2002) Tempo de busca e de manuseio de larvas de Chrysoperla externa (Hagen, 1861) (Neuroptera, Chrysopidae) alimentadas com Uroleucon ambrosiae (Thomas, 1878) (Hemiptera, Aphididae). Rev Bras Entomol 46:535–538. https://doi.org/10.1590/S0085-56262002000400007

    Article  Google Scholar 

  • Begon M, Harper J, Townsend C (1999) Ecologia: indivíduos, populações e comunidades (3ª edição). Brackwell, Oxford

    Google Scholar 

  • Birkett MA, Chamberlain K, Guerrieri E, Pickett JA, Wadhams LJ, 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  Google Scholar 

  • Castro L, Alejandra M, Martínez O, Wilson J, Dotor R, Yadira M (2016) Evaluation of the regulatory effect of Chrysoperla externa on whitefly Trialeurodes vaporariorum in tomato. Rev Cienc Agríc 33:43–54

    Google Scholar 

  • Castro GAPR, Siqueira Filho A (2006) Impactos da mosca-branca na cajucultura Sanjoanense. Relatório da Prefeitura de São João da Barra, RJ.

  • Costa SS, Broglio SM, Dias-Pini NS, Santos DS, Santos JM, Duque FJ, Saraiva WV (2020) Developmental biology and functional responses of Leucochrysa (Nodita) azevedoi fed with different prey. Biocontrol Sci Technol 30:42–50. https://doi.org/10.1080/09583157.2019.1687644

    Article  Google Scholar 

  • Darshanee HLC, Ren H, Ahmed N, Zhang ZF, Liu YH, Liu TX (2017) Volatile-mediated attraction of greenhouse whitefly Trialeurodes vaporariorum to tomato and eggplant. Front Plant Sci 8:1285. https://doi.org/10.3389/fpls.2017.01285

    Article  Google Scholar 

  • Fancelli M, Sousa MR, Silva TSM, Girardi EA, Laumann RA, Coelho Filho MA (2017) SOLF–System for data acquisition in olfactometry bioassays. Citrus Res Technol 38:95–98

    Article  Google Scholar 

  • Flint HM, Salter SS, Walters S (1979) Caryophyllene: an attractant for the green lacewing. Environ Entomol 6:1123–1125. https://doi.org/10.1093/ee/8.6.1123

    Article  Google Scholar 

  • Fonseca AR, Carvalho CF, Souza B (2000) Resposta funcional de Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae) alimentada com Schizaphis graminum (Rondani) (Hemiptera: Aphididae). An Soc Entomol Bras 29:309–317

    Article  Google Scholar 

  • Ganjisaffar F, Perring TM (2015) Prey stage preference and functional response of the predatory mite Galendromus flumenis to Oligonychus pratensis. Biol Control 82:40–45. https://doi.org/10.1016/j.biocontrol.2014.12.004

    Article  Google Scholar 

  • Goiana ES, Dias-Pini NS, Vidal Neto FDC, Maciel GPS, Pastori P, Melo J (2017b) Some biological parameters and colonization of Aleurodicus cocois on dwarf-cashew. Idesia 35:117–120

    Google Scholar 

  • Goiana ES, Dias-Pini NS, Muniz CR, Soares AA, Alves JC, Vidal-Neto FC, Bezerra CSS (2020) Dwarf-cashew resistance to whitefly (Aleurodicus cocois) linked to morphological and histochemical characteristics of leaves. Pest Manag Sci 76:464–471. https://doi.org/10.1002/ps.5531

    Article  CAS  Google Scholar 

  • Goiana ES, Dias-Pini NS, Gomes Filho AAH, Vidal Neto FDC, Barros LDM, Pastori PL, Sosa Duque FJ (2017a) Preferência de clones de cajueiro-anão à mosca-branca e distribuição temporal da praga e seu predador. Embrapa Agroindústria Tropical-Boletim de Pesquisa e Desenvolvimento (INFOTECA-E). http://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1068665 (accessed 28 December 2021)

  • Hassanpour M, Mohaghegh J, Iranipour S, Nouri-Ganbalani G, Enkegaard A (2011) Functional response of Chrysoperla carnea (Neuroptera: Chrysopidae) to Helicoverpa armigera (Lepidoptera: Noctuidae): effect of prey and predator stages. Insect Science 18:217–224

    Article  Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:85–398. https://doi.org/10.4039/Ent91385-7

    Article  Google Scholar 

  • Holling CS (1966) The functional response of invertebrate predators to prey density. Mem Ent Soc Can 48:1–78. https://doi.org/10.4039/entm9848fv

    Article  Google Scholar 

  • Horowitz AR, Ishaaya I (2014) Dynamics of biotypes B and Q of the whitefly Bemisia tabaci and its impact on insecticide resistance. Pest Manag Sci 70:1568–1572

    Article  CAS  Google Scholar 

  • SAS Institute. 2018. SAS/STAT User’s guide, version 8.02, TS level 2 MO. SAS Institute Inc., Cary, North Carolina.

  • Juliano SA (2001) Nonlinear curve fitting: predation and functional response curves. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn. Chapman and Hall, New York, pp 159–182

    Google Scholar 

  • Jumbo LOV, Teodoro AV, Rêgo AS, Haddi K, Galvão AS, Oliveira EE (2019) The lacewing Ceraeochrysa caligata as a potential biological agent for controlling the red palm mite Raoiella indica. PeerJ 7:e7123. https://doi.org/10.7717/peerj.7123

    Article  Google Scholar 

  • Laws AN (2017) Climate change effects on predator–prey interactions. Curr Opin Insect Sci 23:28–34. https://doi.org/10.1016/j.cois.2017.06.010

    Article  Google Scholar 

  • Laznik Ž, Trdan S (2018) Are synthetic volatiles, typically emitted by insect-damaged peach cultivars, navigation signals for two-spotted lady beetle (Adalia bipunctata L.) and green lacewing (Chrysoperla carnea [Stephens]) larvae? J Plant Dis Prot 125:529–538. https://doi.org/10.1007/s41348-018-0172-6

    Article  Google Scholar 

  • Leman A, Ingegno BL, Tavella L, Janssen A, Messelink GJ (2019) The omnivorous predator Macrolophus pygmaeus, a good candidate for the control of both greenhouse whitefly and poinsettia thrips on gerbera plants. Insect Sci.

  • Li SJ, Ren SL, Xue X, Ren SX, Cuthbertson AG, Van Dam NM, Qiu BL (2014) Efficiency of plant induced volatiles in attracting Encarsia formosa and Serangium japonicum, two dominant natural enemies of whitefly Bemisia tabaci in China. Pest Manag Sci 70:1604–1610

    Article  CAS  Google Scholar 

  • Li ZQ, Zhang S, Cai XM, Luo JY, Dong SL, Cui JJ, Chen ZM (2018) Instinct binding affinities of odorant-binding proteins from the natural predator Chrysoperla sinica suggest different strategies to hunt prey. J Insect Physiol 111:25–31

    Article  CAS  Google Scholar 

  • Lima DB, Oliveira HKV, Melo JWS, Gondim Júnior MGC, Guedes RNC, Pallini A, Oliveira JEM (2017) Acaricides impair prey location in a predatory phytoseiid mite. J Appl Entomol 141:141–149

  • Lins JC, Van Loon JJ, Bueno VH, 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. Bio Control 59:707–718

    Google Scholar 

  • Maia WJM, Carvalho CF, Souza B, Cruz I, Maia TJ (2004) Predatory capacity and biological aspects of Chrysoperla externa (Hagen, 1861) (Neuroptera: Chrysopidae) fed on Rhopalosiphum maidis (Fitch, 1856). Cienc Agrotec 28:1259–1268. https://doi.org/10.1590/S1413-70542004000600006

    Article  Google Scholar 

  • Michereff MF, Magalhães DM, Hassemer MJ, Laumann RA, Zhou JJ, Paulo EDA, Blassioli-Moraes MC (2019) Variability in herbivore-induced defence signalling across different maize genotypes impacts significantly on natural enemy foraging behaviour. J Pest Sci 92:723–736. https://doi.org/10.1007/s10340-018-1033-6

    Article  Google Scholar 

  • Monteiro NV, Saraiva WVA, Dias-Pini NS, Maciel GPS, Vasconcelos JF, Duarte PM, Rodrigues S (2021). Aspectos biológicos de Chrysoperla externa visando ao controle biológico da mosca-branca-do-cajueiro. Embrapa Agroindústria Tropical- Boletim de Pesquisa e Desenvolvimento (INFOTECA-E). http://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1130075. (accessed 28 December 2021)

  • Niederbacher B, Winkler JB, Schnitzler JP (2015) Volatile organic compounds as non-invasive markers for plant phenotyping. J Exp Bot 66:5403–5416

    Article  CAS  Google Scholar 

  • Nordlund DA, Morrison RK (1990) Handling time, prey preference, and functional response for Chrysoperla rufilabris in the laboratory. Entomol Exp Appl 57:237

    Article  Google Scholar 

  • Núñez E (2008) Plagas de paltos y citricos en Perú, in: Ripa RS, Larral P (Eds), Manejo de plagas en paltos cítricos. Instituto de Investigaciones Agropecuarias, Chile, pp. 324–364. http://repositorio.senasa.gob.pe/handle/SENASA/123

  • Ortiz-Carreon FR, Rojas JC, Cisneros J, Malo EA (2019) Herbivore-induced volatiles from maize plants attract chelonus insularis, an egg-larval parasitoid of the fall armyworm. J Chem Ecol 45:326–337

    Article  CAS  Google Scholar 

  • Ozawa R, Shiojiri K, Sabelis MW, Takabayashi J (2008) Maize plants sprayed with either jasmonic acid or its precursor, methyl linolenate, attract armyworm parasitoids, but the composition of attractants differs. Entomol Exp Appl 129:189–199. https://doi.org/10.1111/j.1570-7458.2008.00767.x

    Article  CAS  Google Scholar 

  • Palomares-Pérez M, Bravo-Núñez M, Arredondo-Bernal HC (2019) Functional Response of Chrysoperla externa (Hagen 1861) (Neuroptera: Chrysopidae) fed with Melanaphis sacchari (Zehntner 1897) (Hemiptera: Aphididae). Proc Entomol Soc Wash 121:256–264. https://doi.org/10.4289/0013-8797.121.2.256

    Article  Google Scholar 

  • Pinto-Zevallos DM, Martins CB, Pellegrino AC, Zarbin PH (2013) Compostos orgânicos voláteis na defesa induzida das plantas contra insetos herbívoros. Quim Nova 36:1395–1405. https://doi.org/10.1590/S0100-40422013000900021

    Article  CAS  Google Scholar 

  • 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. Bio Control 80:103–112

    Article  Google Scholar 

  • Saraiva WVA, Dias-Pini NDS, Innecco R, Zocolo GJ, Rodrigues THS, Rêgo AS, Maciel GPDS (2021) Toxic effects of an essential oils mixture on Aleurodicus cocois (Hemiptera: Aleyrodidae) and Chrysoperla externa (Neuroptera: Chrysopidae). Biocontrol Sci Technol 31:526–540. https://doi.org/10.1080/09583157.2020.1871468

    Article  Google Scholar 

  • Saraiva WVA, Dias-Pini NS, Alves Filho EG, Melo JW, Fancelli M, Coutinho CR, Macedo VHM, Goiana ES (2022) Attraction of whitefly Aleurodicus cocois mediated by cashew volatiles. Phytoparasitica 50(2):399–410

    Article  CAS  Google Scholar 

  • Silva DB, Bueno VH, Van Loon JJ, Peñaflor MFG, Bento JMS, Van Lenteren JC (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 44:29–39. https://doi.org/10.1007/s10886-017-0909-x

    Article  CAS  Google Scholar 

  • Sousa ALV, Silva DB, Silva GG, Bento JMS, Penãflor MFG, Souza B (2020) Behavioral response of the generalist predator Orius insidiosus to single and multiple herbivory by two cell content-feeding herbivores on rose plants. Arthropod Plant Interact 14:227–236

    Article  Google Scholar 

  • Strapasson P, Pinto-Zevallos DM, Paudel S, Rajotte EG, Felton GW, Zarbin PH (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 40:1090–1098

    Article  CAS  Google Scholar 

  • Teodoro AV, Oliveira NNFC, Galvão AS, de Sena Filho JG, Pinto-Zevallos DM (2020) Interference of plant fixed oils on predation and reproduction of Neoseiulus baraki (Acari: Phytoseiidae) feeding on Aceria guerreronis (Acari: Eriophyidae). Bio Control 143:104204

    Article  CAS  Google Scholar 

  • Yoneya K, Takabayashi J (2013) Interaction–information networks mediated by plant volatiles: a case study on willow trees. J Plant Interact 8:97–202

    Article  Google Scholar 

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Acknowledgements

We would like to thank the National Council for Scientific and Technological Development (CNPq) for a master’s research scholarship to first author.

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Saraiva, W.V.A., Monteiro, N.V., da Silva Dias-Pini, N. et al. Chrysoperla externa (Hagen) (Neuroptera, Chrysopidae) is a good candidate for predation of Aleurodicus cocois (Curtis) (Hemiptera: Aleyrodidae) in cashew crop. Arthropod-Plant Interactions 17, 99–110 (2023). https://doi.org/10.1007/s11829-022-09937-6

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