Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T04:18:41.307Z Has data issue: false hasContentIssue false
  • English
  • Français

Exposure to essential oils and ethanol vapors affect fecundity and survival of two frugivorous fruit fly (Diptera: Tephritidae) pest species

Published online by Cambridge University Press:  02 April 2020

A. Oviedo ,
G. Van Nieuwenhove ,
C. Van Nieuwenhove  and
J. Rull Open the ORCID record for J. Rull [Opens in a new window]
A. Oviedo
Affiliation:
Facultad de Ciencias Naturales e I.M.L, UNT-Cátedra de Biología Celular y de los Microorganismos, Miguel Lillo 205, 4000, San Miguel de Tucumán, Tucumán, Argentina
G. Van Nieuwenhove
Affiliation:
Facultad de Ciencias Naturales e I.M.L, UNT-Cátedra de Biología Celular y de los Microorganismos, Miguel Lillo 205, 4000, San Miguel de Tucumán, Tucumán, Argentina Departamento Zoología, Fundación Miguel Lillo, Instituto de Entomología, Miguel Lillo 251, 4000, San Miguel de Tucumán, Tucumán, Argentina
C. Van Nieuwenhove*
Affiliation:
Facultad de Ciencias Naturales e I.M.L, UNT-Cátedra de Biología Celular y de los Microorganismos, Miguel Lillo 205, 4000, San Miguel de Tucumán, Tucumán, Argentina CERELA-CONICET, Chacabuco 145, 4000, San Miguel de Tucumán, Tucumán, Argentina
J. Rull*
Affiliation:
PROIMI Biotecnología-CONICET, LIEMEN-División Control Biológico de Plagas, Av. Belgrano y Pje. Caseros, T4001MVB San Miguel de Tucumán, Tucumán, Argentina
*
Author for correspondence: C. Van Nieuwenhove, Email: carina@cerela.org.ar; J. Rull, Email: pomonella@gmail.com
Author for correspondence: C. Van Nieuwenhove, Email: carina@cerela.org.ar; J. Rull, Email: pomonella@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Plant-derived compounds can be an environmentally friendly alternative to synthetic pesticide use for pest management. Essential oils (EOs) in several plant families have been found to be toxic to various pest species of insects through topical application, ingestion, and as fumigants. Previous studies revealed that, among various environmentally friendly insecticides, the EOs of Baccharis dracunculifolia and Pinus elliottii and an ethanol extract of Solanum granulosoleprosum plus Ricinus communis, were toxic to Ceratitis capitata and Anastrepha fraterculus (Diptera: Tephritidae) when applied topically to pupae or when ingested by adults. Here, we aimed to examine the potentially toxic effects of these plant-derived compounds when these two pestiferous fruit fly species were exposed to their vapors. We also examined their fumigant effect on female fecundity and fertility and compared it with water and ethanol controls. Exposure of C. capitata and A. fraterculus sexually mature adults to volatiles and vapors of both B. dracunculifolia and P. elliottii EOs resulted in lower longevity (half-life), survivorship, and female fecundity than the water vapor control. Toxicity of C. capitata was greater for P. elliottii than for B. dracunculifolia while the reverse was true for A. fraterculus. Exposure to vapors of S. granulosoleprosum + R. communis (S + R) had no effect on longevity but reduced survivorship of adults of both species. Interestingly, exposure to vapors of S + R, 50% (v/v) and pure ethanol resulted in greater fecundity of females of both frugivorous fly species than the water control. By contrast, fertility (% egg hatch) was in all cases high (>85%) and not different than the water control. Exposure to ethanol vapors appears to have similar effects on frugivorous tephritids as those reported on saprophagous and frugivorous species of Drosophila, a novel finding that may have important practical implications.

Keywords

Adult survivalAnastrepha fraterculusbiopesticidesCeratitis capitatarational pest managementreproductive parameters
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 4 , August 2020 , pp. 558 - 565
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press.

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allwood, AJ, Vueti, ET, Leblanc, L and Bull, R (2002) Eradication of introduced Batrocera (Diptera: Tephritidae) in Nauru using male annihilation and protein bait application techniques. In: Veitch, D and Clout, M (eds) Turning the Tide: The Eradication of Invasive Species, pp 19–25. IUCN SSC Invasive Species Specialist Group. IUCN, Gland, Switzerland/Cambridge, UK, viii + 414 ppGoogle Scholar
Allwood, AJ, Vueti, ET, Leblanc, L and Bull, R (2002) Eradication of introduced Batrocera (Diptera: Tephritidae) in Nauru using male annihilation and protein bait application techniques. In: Veitch, D and Clout, M (eds) Turning the Tide: The Eradication of Invasive Species, pp 19–25.Google Scholar
Bachmann, GE, Segura, DF, Devescovi, F, Juárez, ML, Ruiz, MJ, Vera, MT and Fernández, PC (2015) Male sexual behavior and pheromone emission is enhanced by exposure to guava fruit volatiles in Anastrepha fraterculus. PLoS ONE 10, e0124250.CrossRefGoogle ScholarPubMed
Bakkali, F, Averbeck, S, Averbeck, D and Idaomar, M (2008) Biological effects of essential oils – a review. Food and Chemical Toxicology 46, 446–475.CrossRefGoogle ScholarPubMed
Barud, FJ, López, S, Tapia, A, Feresin, GE and López, ML (2014) Attractant, sexual competitiveness enhancing and toxic activities of the essential oils from Baccharis spartioides and Schinus polygama on Ceratitis capitata Wiedemann. Industrial Crops and Products 62, 299–304.CrossRefGoogle Scholar
Bazzoni, E, Sanna Passino, G, Moretti, MDL and Prota, R (1997) Toxicity of anethole and its effects on egg production of Ceratitis capitata Wied. (Diptera: Tephritidae). Annals of Applied Biology 131, 369–374.CrossRefGoogle Scholar
Benelli, G, Flamini, G, Canale, A, Cioni, PL and Conti, B (2012) Toxicity of some essential oil formulations against the Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera Tephritidae). Crop Protection 42, 223–229.CrossRefGoogle Scholar
Buttery, RG (1981) Vegetable and fruit flavors. In Teranishi, R, Flath, RA and Sugisawa, H (eds), Flavor Research, Recent Advances. New York: Marcel Dekker, Inc., pp. 175–216.Google Scholar
Canale, A, Benelli, G, Conti, B, Lenzi, G, Flamini, G, Francini, A and Cioni, PL (2013) Ingestion toxicity of three Lamiaceae essential oils incorporated in protein baits against the olive fruit fly, Bactrocera oleae (Rossi) (Diptera Tephritidae). Natural Product Research 27, 2091–2099.CrossRefGoogle Scholar
Cha, DH, Adams, T, Werle, CT, Sampson, BJ, Adamczyk, JJ Jr, Rogg, H and Landolt, PJ (2014) A four-component synthetic attractant for Drosophila suzukii (Diptera: Drosophilidae) isolated from fermented bait headspace. Pest Management Science 70, 324–331.CrossRefGoogle ScholarPubMed
Chaaban, A, Martins, CEN, Bretanha, LC, Micke, GA, Carrer, AR, Rosa, NF and Molento, MB (2018) Insecticide activity of Baccharis dracunculifolia essential oil against Cochliomyia macellaria (Diptera: Calliphoridae). Natural Product Research 32, 2954–2958.CrossRefGoogle Scholar
Chang, CL, Il Kyu Cho, IK and Li, QL (2009) Insecticidal activity of basil oil, trans-anethole, estragole, and linalool to adult fruit flies of Ceratitis capitata, Bactrocera dorsalis, and Bactrocera cucurbitae. Journal of Economic Entomology 102, 203–209.CrossRefGoogle ScholarPubMed
Cook, SM, Khan, ZR and Pickett, JA (2007) The use of push-pull strategies in integrated pest management. Annual Review of Entomology 52, 374–400.CrossRefGoogle ScholarPubMed
Dayan, FE, Cantrell, CL and Duke, SO (2009) Natural products in crop protection. Bioorganic & Medicinal Chemistry 17, 4022–4034.CrossRefGoogle ScholarPubMed
Dinesh, DS, Kumari, S, Kumar, V and Das, P (2014) The potentiality of botanicals and their products as an alternative to chemical insecticides to sandflies (Diptera: Psychodidae): a review. Journal of Vector Borne Diseases 51, 1–7.Google ScholarPubMed
Dudley, R (2004) Ethanol, fruit ripening, and the historical origins of human alcoholism in primate frugivory. Integrative and Comparative Biology 44, 315–323.CrossRefGoogle ScholarPubMed
Enan, E (2001) Insecticidal activity of essential oils: octopaminergic sites of action. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 130, 325–337.Google ScholarPubMed
Etges, WJ and Klassen, CS (1989) Influences of atmospheric ethanol on adult Drosophila mojavensis: altered metabolic rates and increases in fitness among populations. Physiological Zoology 62, 170–193. doi: 10.1086/physzool.62.1.30160004CrossRefGoogle Scholar
Geer, BW, Langevin, ML and McKechnie, SW (1985) Dietary ethanol and lipid synthesis in Drosophila melanogaster. Biochemical Genetics 23, 7–8.CrossRefGoogle ScholarPubMed
Ghabbari, M, Guarino, S, Caleca, V, Saiano, F, Sinacori, M, Baser, N and Verde, GL (2018) Behavior-modifying and insecticidal effects of plant extracts on adults of Ceratitis capitata (Wiedemann) (Diptera Tephritidae). Journal of Pest Science 91, 907–917.CrossRefGoogle Scholar
Gregg, PC, Del Socorro, AP and Landolt, PJ (2018) Advances in attract-and-kill for agricultural pests: beyond pheromones. Annual Review of Entomology 63, 453–470.CrossRefGoogle ScholarPubMed
Ibrahim, MA, Kainulainen, P, Aflatuni, A, Tiilikkala, K and Holopainen, JK (2001) Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: with special reference to limonene and its suitability for control of insect pests. Agriculture and Food Science in Finland 10, 243–259.CrossRefGoogle Scholar
Ioannou, CS, Papadopoulos, NT, Kouloussis, NA, Tananaki, CI and Katsoyannos, BI (2012) Essential oils of citrus fruit stimulate oviposition in the Mediterranean fruit fly Ceratitis capitata (Diptera: Tephritidae). Physiological Entomology 37, 330–339.CrossRefGoogle Scholar
Isman, MB (2000) Plant essential oils for pest and disease management. Crop Protection 19, 603–608.CrossRefGoogle Scholar
Isman, MB, Miresmailli, S and Machial, C (2011) Commercial opportunities for pesticides based on plant essential oils in agriculture, industry and consumer products. Phytochemistry Reviews 10, 197–204.CrossRefGoogle Scholar
Jang, EB and Light, DM (1996) Olfactory semiochemicals of tephritids. In McPheron, BA and Steck, GJ (eds), Fruit by Pests: A World Assessment of Their Biology and Management. Delray Beach, FL, 608: St. Lucie Press, pp. 73–90.Google Scholar
Jankowska, M, Rogalska, J, Wyszkowska, J and Stankiewicz, M (2017) Molecular targets for components of essential oils in the insect nervous system – a review. Molecules 23, 34.CrossRefGoogle ScholarPubMed
Kostyukovsky, M, Rafaeli, A, Gileadi, C, Demchenko, N and Shaay, E (2002) Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: possible mode of action against insect pests. Pest Management Science 58, 1101–1106.CrossRefGoogle ScholarPubMed
Koul, O, Walia, S and Dhaliwal, GS (2008) Essential oils as green pesticides: potential and constraints. Biopesticide International 4, 63–84.Google Scholar
Martínez, L, Plata-Rueda, A, Colares, H, Campos, J, Dos Santos, M, Fernandes, F, Serrão, JE and Zanuncio, J (2018) Toxic effects of two essential oils and their constituents on the mealworm beetle, Tenebrio molitor. Bulletin of Entomological Research 108, 716–725.CrossRefGoogle ScholarPubMed
Nerio, LS, Olivero-Verbel, J and Stashenko, E (2010) Repellent activity of essential oils: a review. Bioresource Technology 101, 372–378.CrossRefGoogle ScholarPubMed
Niogret, J and Epsky, ND (2018) Attraction of Ceratitis capitata (Diptera: Tephritidae) sterile males to essential oils: the importance of linalool. Environmental Entomology 47, 1287–1292.CrossRefGoogle ScholarPubMed
Oviedo, A, Van Nieuwenhove, G, Van Nieuwenhove, C and Rull, J (2017) Biopesticide effects on pupae and adult mortality of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae). Austral Entomology 57, 457–464.CrossRefGoogle Scholar
Ovruski, S, Schliserman, P and Aluja, M (2003) Native and introduced host plants of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in Northwestern Argentina. Journal of Economic Entomology 96, 1108–1118.CrossRefGoogle Scholar
Papachristos, DP, Kimbaris, AC, Papadopoulos, NT and Polissiou, MG (2009) Toxicity of citrus essential oils against Ceratitis capitata (Diptera: Tephritidae) larvae. Annals of Applied Biology 155, 381–389.CrossRefGoogle Scholar
Pavlidou, V, Karpouhtsis, I, Franzios, G, Zambetaki, A, Scouras, Z and Mavragani-Tsipidou, P (2004) Insecticidal and genotoxic effects of essential oils of Greek sage, Salvia fruticosa, and mint, Mentha pulegium, on Drosophila melanogaster and Bactrocera oleae (Diptera: Tephritidae). Journal of Agricultural and Urban Entomology 21, 39–49.Google Scholar
Piesik, D, Łyszczarz, A, Tabaka, P, Lamparski, R, Bocianowski, J and Delaney, KJ (2010) Volatile induction of three cereals: influence of mechanical injury and insect herbivory on injured plants and neighboring uninjured plants. Annals of Applied Biology 157, 425–434.CrossRefGoogle Scholar
Porto, KR, Motti, PR, Yano, M, Roel, AR, Cardoso, CA and Matias, R (2017) Screening of plant extracts and fractions on Aedes aegypti larvae found in the state of Mato Grosso do Sul (linnaeus, 1762)(culicidae). Anais da Academia Brasileira de Ciências 89, 895–906.CrossRefGoogle Scholar
Rajendran, S and Sriranjini, V (2008) Plant products as fumigants for stored-product insect control. Review. Journal of Stored Products Research 44, 126–135.CrossRefGoogle Scholar
Regnault-Roger, C, Vincent, C and Arnason, JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annual Review of Entomology 57, 405–424.CrossRefGoogle Scholar
Ruiz, MJ, Juárez, ML, Alzogaray, RA, Arrighi, F, Arroyo, L, Gastaminza, G and Vera, T (2014) Toxic effect of citrus peel constituents on Anastrepha fraterculus Wiedemann and Ceratitis capitata Wiedemann immature stages. Journal of Agricultural and Food Chemistry 62, 10084–10091.CrossRefGoogle ScholarPubMed
Robacker, DC (2009) Attractiveness to Anastrepha ludens (Diptera: Tephritidae) of plant essential oils and a synthetic food-odour lure. Journal of Applied Entomology 131, 202–208.CrossRefGoogle Scholar
Royer, JE, Khan, M and Mayer, DG (2018) Methyl-isoeugenol, a highly attractive male lure for the cucurbit flower pest Zeugodacus diversus (Coquillett) (syn. Bactrocera diversa) (Diptera: Tephritidae: Dacinae). Journal of Economic Entomology 111, 1197–1201.CrossRefGoogle Scholar
Salvatore, A, Borkosky, S, Willink, E and Bardon, A (2004) Toxic effects of lemon peel constituents on Ceratitis capitata. Journal of Chemical Ecology 30, 323–333.CrossRefGoogle ScholarPubMed
Schliserman, P, Aluja, M, Rull, J and Ovruski, SM (2014) Habitat degradation and introduction of exotic plants favor persistence of invasive species and population growth of native polyphagous fruit fly pests in a Northwestern Argentinean mosaic. Biological Invasions 16, 2599–2613.CrossRefGoogle Scholar
Segura, DF, Belliard, SA, Vera, MT, Bachmann, GE, Ruiz, MJ, Jofreinse-Barud, F and Shelly, TE (2018) Plant chemicals and the sexual behavior of male tephritid fruit flies. Annals of the Entomological Society of America 111, 239–264.CrossRefGoogle Scholar
Shelly, TE (2001) Exposure to α-copaene and α-copaene-containing oils enhances mating success of male Mediterranean fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 94, 497–502.CrossRefGoogle Scholar
Straten, SV and Maarse, H (1983) Volatile Compounds in Food, 5th Edn., Zeist, The Netherlands: Central Institute for Nutrition and Food Research TNO.Google Scholar
Suckling, DM, Kean, JM, Stringer, LD, Cáceres-Barrios, C, Hendrichs, J, Reyes-Flores, J and Dominiak, BC (2016) Eradication of tephritid fruit fly pest populations: outcomes and prospects. Pest Management Science 72, 456–465.CrossRefGoogle ScholarPubMed
Tan, KH, Nishida, R, Jang, EB and Shelly, TE (2014) Pheromones, male lures, and trapping of tephritid fruit flies. In Trapping and the Detection, Control, and Regulation of Tephritid Fruit Flies. Dordrecht: Springer, pp. 15–74.Google Scholar
Tripathi, AK, Upadhyay, S, Bhuiyan, M and Bhattacharya, PR (2009) A review on prospects of essential oils as biopesticide in insect-pest management. Journal of Pharmacognosy and Phytotherapy 1, 52–63.Google Scholar
Upadhyay, N, Dwivedy, AK, Kumar, M, Prakash, B and Dubey, NK (2018) Essential oils as eco-friendly alternatives to synthetic pesticides for the control of Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Journal of Essential Oil-Bearing Plants 21, 282–297.CrossRefGoogle Scholar
Uramoto, K, Martins, DS and Zucchi, RA (2008) Fruit flies (Diptera, Tephritidae) and their associations with native host plants in a remnant area of the highly endangered Atlantic Rain Forest in the State of Espírito Santo, Brazil. Bulletin of Entomological Research 98, 457–466.CrossRefGoogle Scholar
Vera, MT, Ruiz, MJ, Oviedo, A, Abraham, S, Mendoza, M, Segura, DF and Willink, E (2013) Fruit compounds affect male sexual success in the South American fruit fly, Anastrepha fraterculus (Diptera: Tephritidae). Journal of Applied Entomology 137, 2–10.CrossRefGoogle Scholar