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The ripeness stage but not the cultivar influences the attraction of Anastrepha obliqua to guava

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Abstract

The West Indian fruit fly, Anastrepha obliqua (Macquart), infests a wide diversity of tropical fruit. Previous studies suggest that A. obliqua adults are attracted to volatile compounds common in different hosts. However, to date, most studies have used ripe fruit for the identification of attractive compounds. In this study, we investigated the attraction of sexually mature A. obliqua females and males to two cultivars and three ripening stages of guava. We also identified the attractive compounds to A. obliqua by combined gas chromatography-electroantennographic detector (GC-EAD) and gas chromatography-mass spectrometry (GC–MS) and evaluated the biological activity of the identified compounds in field-cage tests. We found that individuals of both sexes of A. obliqua showed no preference to the volatiles of either of the two cultivars of guava evaluated. In contrast, flies were more attracted to ripe and half-ripe fruit than to unripe ones. GC-EAD analyses of extracts of ripe “Creole” or “Thai” cultivars identified six compounds that elicited antennal responses by A. obliqua females and males. The compounds were identified by GC–MS as ethyl butyrate, cis-3-hexen-1-ol, ethyl hexanoate, cis-3-hexenyl acetate, ethyl benzoate, and ethyl octanoate. Half-ripe guava emit ethyl butyrate, cis-3-hexen-1-ol, ethyl hexanoate, and cis-3-hexenyl acetate, while only traces of cis-3-hexenyl-acetate were found in unripe guava. Field-cage tests with synthetic standards confirmed that the compounds identified are responsible for the attraction of A. obliqua flies to ripe guava.

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References

  • Alagarmalai J, Nestel D, Dragushich D, Nemny-Lavy E, Anshelevich L, Zada A, Soroker V (2009) Identification of host attractants for the Ethiopian fruit fly, Dacusciliatus Loew. J Chem Ecol 35:542–551

    Article  CAS  PubMed  Google Scholar 

  • Aluja M, Arredondo J, Díaz-Fleischer F, Birke A, Rull J, Niogret J, Epsky N (2014) Susceptibility of 15 mango (Sapindales: Anacardiaceae) cultivars to the attack by Anastrepha ludens and Anastrepha obliqua (Diptera: Tephritidae) and the role of underdeveloped fruit as pest reservoirs: Management implications. J Econ Entomol 107:375–388

    Article  CAS  PubMed  Google Scholar 

  • Artiaga-López T, Hérnandez E, Dominguez-Gordillo J, Moreno DS, Orozco-Dávila D (2004)Mass-production of Anastrepha obliqua at the moscafrut fruit fly facility, Mexico.In BN Barnes (eds.) Proceedings of the 6th International Symposium on Fruit Flies of Economic Importance. Isteg Scientific Publications, Irene, South Africa, pp. 389–392

  • Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman and Hall, New York, p 312

    Book  Google Scholar 

  • Birke A, Aluja M (2011) Anastrepha ludens and A. serpentina (Diptera: Tephritidae) do not infest Psidium guajava (Myrtaceae), but A. obliqua occasionally share this resource with A. striata in nature. J Econ Entomol 104:1204–1211

    Article  PubMed  Google Scholar 

  • Birke A, Guillén L, Midgarden D, Aluja M (2013) Fruit flies Anastrepha ludens (Loew), A. obliqua (Macquart) and A.grandis (Macquart) (Diptera : Tephritidae): three pestiferous tropical fruit flies that could potentially expand their range to temperate areas. In: Peña J (ed.) Potential invasive pests of agricultural crops. CAB International, Wallingford, Oxfordshire, pp 192–213

    Chapter  Google Scholar 

  • Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    Article  CAS  PubMed  Google Scholar 

  • Cha DH, Powell THQ, FederLinn JLCE Jr (2011) Identification of host fruit volatiles from three mayhaw species (Crataegus Series Aestivales) attractive to mayhaw-origin Rhagoletis pomonella flies in the Southern United States. J Chem Ecol 37:961–973

    Article  CAS  PubMed  Google Scholar 

  • Conchou L, Anderson P, Birgersson G (2017) Host plant species differentiation in a polyphagous moth: olfaction is enough. J Chem Ecol 43:794–805

    Article  CAS  PubMed  Google Scholar 

  • Conchou L, Lucas P, Camille M, Magali P, Michael S, Renou M (2019) Insect odorscapes: from plant volatiles to natural olfactory scenes. Front Physiol 10:972

    Article  PubMed  PubMed Central  Google Scholar 

  • Cornelius ML, Duan JJ, Messing RH (2000) Volatile host fruit odors as attractants for the oriental fruit fly (Diptera: Tephritidae). J Econ Entomol 93:93–100

    Article  CAS  PubMed  Google Scholar 

  • Cruz-López L, Malo EA, Toledo J, Virgen A, Mazo ADEL, Rojas JC (2006) A new potential attractant for Anastrepha obliqua from Spondias mombin fruits. J Chem Ecol 32:351–365

    Article  PubMed  CAS  Google Scholar 

  • Cunningham JP, Carlsson MA, Villa TF, Dekker T, Clarke AR (2016) Do fruit ripening volatiles enable resource specialism in polyphagous fruit flies? J Chem Ecol 42:931–940

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Santiz E, Rojas JC, Cruz-Lopez L, Hernandez E, Malo EA (2016) Olfactory response of Anastrepha striata (Diptera:Tephritidae) to guava and sweet orange volatiles. Insect Sci 23:720–727

    Article  CAS  PubMed  Google Scholar 

  • Doutt RL (1959) The biology of parasitic Hymenoptera. Annu Rev Entomol 4:161–182

    Article  Google Scholar 

  • Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Espinoza Roblero A (2017) Identificación de los compuestos volátiles involucrados en la preferencia olfativa de Anastrepha obliqua por dos cultivares de Averrhoa carambola. Unpublished M Sc thesis, El Colegio de la Frontera Sur, Mexico

  • Finch S, Collier RH (2000) Host-plant selection by insects—a theory based on ‘appropriate/inappropriate landings’ by pest insects of cruciferous plants. Entomol Exp App 96:91–103

    Article  Google Scholar 

  • Fu L, Li Z, Huang G, Wu X, Ni W, Qu W-W (2014) The current and future potential geographic range of West Indian fruit fly, Anastrepha obliqua (Diptera : Tephritidae). Insect Sci 21:234–244

    Article  PubMed  Google Scholar 

  • Gámez AM, León SP (2020) Preimaginal conditioning affects oviposition choices in the silkworm moth (Bombyx mori). Behav Proc 175:104121

    Article  Google Scholar 

  • García-Ramirez M, Cibrián-Tovar J, Arzufí-Barrera R, López-Collado J, Soto-Hernández M (2004) Preferencia de Anastrepha ludens (Loew) (Diptera:Tephritidae) por volátiles de frutos verdes o amarillos de mango y naranja. Agrociencia 38:423–430

    Google Scholar 

  • Ghaninia M, Amooghli Tabari M (2016) Olfactory cues explain differential attraction of the striped rice stem borer to different varieties of rice plant. J Appl Entomol 140:376–385

    Article  Google Scholar 

  • Guillén L, Adaime R, Birke A, Velázquez O, Angeles G, Ortega F, Ruíz E, Aluja M (2017) Effect of resin ducts and sap content on infestation and development of immature stages of Anastrepha obliqua and Anastrepha ludens (Diptera: Tephritidae) in four mango (Sapindales: Anacardiaceae) cultivars. J Econ Entomol 110:719–730

    PubMed  Google Scholar 

  • Hassel MP, Southwood TRE (1978) Foraging strategies of insects. Annu Rev Ecol Syst 9:75–98

    Article  Google Scholar 

  • Jang EB, Light DM (1991) Behavioral responses of female Oriental fruit flies to the odor of papayas at three ripeness stages in a laboratory flight tunnel (Diptera: Tephritidae). J Insect Behav 4:751–762

    Article  Google Scholar 

  • Joel DM (1978) The secretory ducts of mango fruits: a defense system effective against the Mediterranean fruit fly. Isr J Bot 27:44–45

    Google Scholar 

  • López-Ley JU, Toledo J, Malo EA, Gomez J, Santiesteban A, Rojas JC (2016) Carambola cultivar, fruit ripeness, and damage by conspecific larvae influence the host-related behaviors of Anastrepha obliqua (Diptera: Tephritidae). J Econ Entomol 109:154–160

    Article  PubMed  CAS  Google Scholar 

  • Malavasi A, Zuchi RA (eds) (2000) Moscas-das Frutas de Importânce Econômica no Brasil. Conocimiento Básico e Aplicado. Holos Editora Ltda-ME, Ribeirao Preto

    Google Scholar 

  • Malo EA, Cruz-López L, Toledo J, Del Mazo A, Virgen A, Rojas JC (2005) Behavioral and electrophysiological responses of the Mexican fruit fly (Diptera: Tephritidae) to guava volatiles. Florida Entomol 88:364–371

    Article  Google Scholar 

  • Malo EA, Gallegos-Torres I, Toledo J, Valle-Mora J, Rojas JC (2012) Attraction of the West Indian fruit fly to mango fruit volatiles. Entomol Exp Appl 142:45–52

    Article  CAS  Google Scholar 

  • Najar-Rodriguez AJ, Galizia CG, Stierle J, Dorn S (2010) Behavioral and neurophysiological responses of an insect to changing ratios of constituents in host plant-derived volatile mixtures. J Exp Biol 213:3388–3397

    Article  CAS  PubMed  Google Scholar 

  • Ning SY, Yang HY, Fan DS, Feng JN (2018) Influence of larval experience on preference of a subterranean insect Delia antiqua on Allium hosts. J Appl Entomol 142:263–271

    Article  CAS  Google Scholar 

  • Nojima S, Linn C, Morris B, Zhang A, Roelofs W (2003) Identification of host fruit volatiles from hawthorn (Crataegus spp.) attractive to hawthorn-origin Rhagoletis pomonella flies. J Chem Ecol 29:321–336

    Article  CAS  PubMed  Google Scholar 

  • Orozco-Dávila D, Quintero L, Hernández E, Solís E, Artiaga T, Hernández R, Montoya P (2017) Mass rearing and sterile insect releases for the control of Anastrepha spp. pests in Mexico–a review. Entomol Exp Appl 164:176–187

    Article  Google Scholar 

  • Petit C, Dupas S, Thiéry D, Capdevielle-Dulac C, Le Ru B, Harry M, Calatayud PA (2017) Do the mechanisms modulating host preference in holometabolous phytophagous insects depend on their host plant specialization? A quantitative literature analysis. J Pest Sci 90:797–805

    Article  Google Scholar 

  • R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Stastitiscal Computing, Austria, Vienna

  • Rao D, Aguilar-Argüello S, Montoya P, Díaz-Fleischer F (2014) The effect of irradiation and mass rearing on the anti-predator behaviour of the Mexican fruit fly, Anastrepha ludens (Diptera: Tephritidae). Bull Entomol Res 104:176–181

    Article  CAS  PubMed  Google Scholar 

  • Rattanapun W, Amornsak W, Clarke AR (2009) Bactrocera dorsalis preference for and performance on two mango varieties at three stages of ripeness. Entomol Exp Appl 131:243–253

    Article  Google Scholar 

  • Ruiz-Arce R, Barr NB, Owen CL, Thomas DB, McPheron BA (2012) Phylogeography of Anastrepha obliqua inferred with mtDNA sequencing. J Econ Entomol 105:2147–2160

    Article  PubMed  Google Scholar 

  • Rull J, Brunel O, Mendez ME (2005) Mass rearing history negatively affects mating success of male Anastrepha ludens (Diptera: Tephritidae) reared for sterile insect technique programs. J Econ Entomol 98:1510–1516

    Article  PubMed  Google Scholar 

  • Schoonhoven LM, Van Loon JJA, Dicke M (2006) Insect plant biology, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Seo ST, Tang C-S, Sanidad S, Takenaka TH (1983) Hawaiian fruit flies (Diptera: Tephritidae): variation of index of infestation with benzyl isothiocyanate concentration and color of maturing papaya. J Econ Entomol 76:535–538

    Article  CAS  Google Scholar 

  • Silva R, Clarke AR (2019) The “sequential cues hypothesis”: a conceptual model to explain host location and ranking by polyphagous herbivores. Insect Sci. https://doi.org/10.1111/1744-7917.12719

    Article  PubMed  Google Scholar 

  • Szentesi A, Greany PD, Chambers DL (1979) Oviposition behavior of laboratory-reared and wild Caribbean fruit flies (Anastrepha suspensa; Diptera: Tephritidae): I. Selected chemical influences. Entomol Exp Appl 26:227–238

    Article  CAS  Google Scholar 

  • Toledo J, Malo EA, Cruz-López L, Rojas JC (2009) Field evaluation of potential fruit-derived lures for Anastrepha obliqua (Diptera: Tephritidae). J Econ Entomol 102:2072–2077

    Article  CAS  PubMed  Google Scholar 

  • Vallat A, Dorn S (2005) Changes in volatile emissions from apple trees and associated response of adult female codling moths over the fruit-growing season. J Agric Food Chem 53:4083–4090

    Article  CAS  PubMed  Google Scholar 

  • Visser JH (1986) Host odor perception by phytophagous insects. Annu Rev Entomol 31:121–144

    Article  Google Scholar 

  • Webster B, Cardé RT (2016) Use of habitat odour by host-seeking insects. Biol Rev Camb Philos Soc 92:1241–1249

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Armando Virgen for technical support, and the Campaña Nacional Contra las Moscas de la Fruta of the Programa Moscafrut (Senasica-Sader-IICA) for providing the flies used in this study. We thank Eric B. Jang (USDA-ARS) for reviewing an early version of this manuscript. This work was supported by Consejo Nacional de Ciencia y Technología through a graduate scholarship to Fernando Cortés Martínez.

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  1. Grupo de Ecología de Artrópodos y Manejo de Plagas, Departamento de Agricultura, Sociedad y Ambiente, El Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto Km 2.5, 30700, Tapachula, CHIS, Mexico

    Fernando Cortés-Martínez, Leopoldo Cruz-López, Pablo Liedo & Julio C. Rojas

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  1. Fernando Cortés-Martínez
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  2. Leopoldo Cruz-López
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Correspondence to Julio C. Rojas.

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Communicated by Marko Rohlfs.

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Cortés-Martínez, F., Cruz-López, L., Liedo, P. et al. The ripeness stage but not the cultivar influences the attraction of Anastrepha obliqua to guava. Chemoecology 31, 115–123 (2021). https://doi.org/10.1007/s00049-020-00332-2

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