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Can Anastrepha fraterculus larval feeding influence chemotaxis and parasitism of Diachasmimorpha longicaudata and Aganaspis pelleranoi?

Published online by Cambridge University Press:  05 April 2021

Patricia Daniela da Silva Pires Open the ORCID record for Patricia Daniela da Silva Pires [Opens in a new window] ,
Josué Sant’ Ana Open the ORCID record for Josué Sant’ Ana [Opens in a new window]  and
Luiza Rodrigues Redaelli Open the ORCID record for Luiza Rodrigues Redaelli [Opens in a new window]
Patricia Daniela da Silva Pires*
Affiliation:
Department of Crop Protection, PPG-Fitotecnia, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Rio Grande do Sul, Brazil
Josué Sant’ Ana
Affiliation:
Department of Crop Protection, PPG-Fitotecnia, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Rio Grande do Sul, Brazil
Luiza Rodrigues Redaelli
Affiliation:
Department of Crop Protection, PPG-Fitotecnia, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Rio Grande do Sul, Brazil
*
Author for correspondence: Patricia Daniela da Silva Pires, Email: [email protected]
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Abstract

Anastrepha fraterculus (Diptera: Tephritidae) is a major barrier to fruit production and exportation. In Brazil, the native parasitoid Aganaspis pelleranoi (Hymenoptera: Figitidae) and the exotic parasitoid Diachasmimorpha longicaudata (Hymenoptera, Braconidae) stand out as biological control agents. Knowledge of the factors that affect interactions among parasitoids, A. fraterculus, and host fruits may enhance the use of these agents in biological control programmes. This study evaluated the chemotaxis and parasitism of A. pelleranoi and D. longicaudata females reared on A. fraterculus larvae and kept on an artificial diet, red guava (Psidium guajava) or apple (Malus domestica). Females of both parasitoid species that emerged from larvae raised on artificial diet, guava or apple, were tested to Y olfactometer choice tests. In the parasitism tests, both parasitoid species were made to choose between A. fraterculus larvae brushed with water, apple pulp or guava pulp. D. longicaudata females from artificial diet (control) did not distinguish between fruit odours; however, females of D. longicaudata from larvae kept in apple or guava directed to the odours of their original fruit. The greatest parasitism for D. longicaudata occurred in the units that contained the pulp in which the larvae grew. A. pelleranoi from artificial diet preferred guava odours, including the females kept in apple. Similar results were observed in the parasitism bioassays. Our results found that A. fraterculus larval feeding influenced search behaviour and parasitism of D. longicaudata, whereas A. pelleranoi rearing experience did not affect its host choices.

Keywords

BraconidaeFigitidaefruit flyHymenopteralearningparasitoids
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 5 , October 2021 , pp. 560 - 567
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Altafini, DL, Redaelli, LR and Jahnke, SM (2013) Superparasitism of Ceratitis capitata and Anastrepha fraterculus (Diptera: Tephritidae) by Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Florida Entomologist 96, 391–395.CrossRefGoogle Scholar
Alvarenga, CD, Brito, ES, Lopes, EN, Silva, MA, Alves, DA, Matrangolo, CAR and Zucchi, RA (2005) Introdução e recuperação do parasitoide exótico Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) em pomares comerciais de goiaba no norte de Minas Gerais. Neotropical Entomology 34, 133–136.CrossRefGoogle Scholar
Badii, KB, Billah, MK, Afreh-Nuamah, K, Obeng-Ofori, D and Nyarko, G (2015) Review of the pest status, economic impact and management of fruit-infesting flies (Diptera: Tephritidae) in Africa. African Journal of Agricultural Research 10, 1488–1498.CrossRefGoogle Scholar
Belda, C and Riudavets, J (2010) Attraction on the parasitoid Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae) to odors from grain and store product pest in a Y-tube olfactometer. Biological Control 54, 29–34.CrossRefGoogle Scholar
Benelli, G, Revadi, S, Carpita, A, Giunti, G and Raspi, A (2013) Behavioral and electrophysiological responses of the parasitic wasp Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae) to Ceratitis capitata-induced fruit volatiles. Biological Control 64, 116–124.CrossRefGoogle Scholar
Bernays, EA (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annual Review of Entomology 46, 703–727.CrossRefGoogle ScholarPubMed
Canale, A, Geri, S and Benelli, G (2014) Associative learning for host-induced fruit volatiles in Psyttalia concolor (Hymenoptera: Braconidae), a koinobiont parasitoid of tephritid flies. Bulletin of Entomological Research 104, 774–780.CrossRefGoogle Scholar
Cancino, J, Liedo, P, Ruiz, L, López, G, Montoya, P and Barrera, JF (2012) Discrimination by Coptera haywardi (Hymenoptera: Diapriidae) of hosts previously attacked by conspecifics or by the larval parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Biocontrol Science Technology 22, 899–914.CrossRefGoogle Scholar
Carrasco, M, Montoya, P, Cruz-Lopes, L and Rojas, JC (2005) Responses of the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to mango fruit volatiles. Environmental Entomology 34, 576–583.CrossRefGoogle Scholar
Corbet, SA (1985) Insect chemosensory responses: a chemical legacy hypothesis. Ecological Entomology 10, 143–153.CrossRefGoogle Scholar
Costa, RIF, Silva, CG, Marchiori, CH, Amaral, BB, Poletti, MM and Torres, LC (2007) Parasitismo em Anastrepha sp. (Diptera: Tephritidae) por Aganaspis pellaranoi (Brèthes, 1924) e Direratapis sp. (Hymenoptera: Figitidae: Eucoilinae). Ciência Agrotecnologia 31, 720–723.CrossRefGoogle Scholar
Del-Claro, K (2012) Origens e importância das relações plantas-animais para ecologia e conservação. In Del-Claro, K and Torezan-Silingardi HM, (eds), Ecologia das Plantas-Animais, uma Abordagem Ecológica. Rio de Janeiro, RJ, Brazil: Technical Books Editora, pp. 37–50.Google Scholar
Dicke, M (2009) Behavioural and community ecology of plants that cry for help. Plant, Cell and Environment 32, 654–665.CrossRefGoogle ScholarPubMed
Dicke, M and Baldwin, IT (2010) The evolutionary context for herbivory-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science 15, 167–175.CrossRefGoogle Scholar
Dukas, R and Duan, JJ (2000) Potential fitness consequences of associative learning in a parasitoid wasp. Behavioral Ecology 11, 536–543.CrossRefGoogle Scholar
Eben, A, Benrey, B, Sivinski, J and Aluja, M (2000) Host species and host plant effects on performance of Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environmental Entomology 29, 87–94.CrossRefGoogle Scholar
Ekesi, S, De Meyer, M, Mohamed, SA, Virgilio, M and Borgemeister, C (2016) Taxonomy, ecology and management of native and exotic fruit fly species in Africa. Annual Review of Entomology 61, 219–238.CrossRefGoogle ScholarPubMed
Fligner, MA and Killeen, TJ (1976) Distribution-free two-sample tests for scale. Journal of the American Statistical Association 71, 210–213.CrossRefGoogle Scholar
Gandolfi, M, Mattiacci, L and Dorn, S (2003) Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proceedings of the Royal Society B 270, 2623–2629.CrossRefGoogle Scholar
Garcia, FRM and Corseuil, E (2004) Native hymenopteran parasitoids associated with fruit flies (Diptera: Tephritidae) in Santa Catarina state, Brazil. Florida Entomologist 87, 517–521.CrossRefGoogle Scholar
Gonçalves, RS, Nava, DE, Pereira, HC, Lisbôa, H, Grutzmacher, AD and Valgas, RA (2013) Biology and fertility life table of Aganaspis pellaranoi (Hymenoptera: Figitidae) in larvae of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae). Annals of the Entomological Society of America 106, 791–798.CrossRefGoogle Scholar
Guimarães, JA and Zucchi, RA (2004) Parasitism behavior of three species of Eucoilinae (Hymenoptera: Cynipoidea: Figitidae) fruit fly parasitoids (Diptera) in Brazil. Neotropical Entomology 33, 217–224.CrossRefGoogle Scholar
Guimarães, JA, Zucchi, RA, Diaz, NB, Souza Filho, MF and Uchôa, FMA (1999) Espécies de Eucoilinae (Hymenoptera: Cynipoidea: Figitidae) parasitoides de larvas de frugívoras (Diptera: Tephritidae e Lonchaiedae) no Brasil. Anais da Sociedade Entomológica do Brasil 28, 63–273.CrossRefGoogle Scholar
Guimarães, JA, Gallardo, FE, Diaz, NB and Zucchi, RA (2003) Eucoilinae species (Hymenoptera: Cynipoidea: Figitidae) parasitoids of fruit-infesting dipterous in Brazil. Identity, geographical distribution and host associations. Zootaxa 278, 1–23.CrossRefGoogle Scholar
Harbi, A, Beitia, F, Ferrara, F, Chermiti, B and Sabater-Muñoz, B (2018) Functional response of Diachasmimorpha longicaudata (Ashmead) over Ceratitis capitata (Wiedemann): Influence of temperature, fruit location and hostdensity. Crop Protection 109, 115–122.CrossRefGoogle Scholar
Harbi, A, Pedro, L, Ferrara, FAA, Tormos, J, Chermiti, B, Beitia, F and Sabater-Munoz, B (2019) Diachasmimorpha longicaudata parasitism response to medly host fruit and fruit infestation age. Insects 10, 211.CrossRefGoogle Scholar
Juniper, BE, Watkins, R and Harris, SA (1999) The origin of the apple. Proceedings of the Eucarpia Symposium on the Fruit Breeding and Genetics 484, 27–33.Google Scholar
Karban, R and Chen, Y (2007) Induced resistance in rice against insects. Bulletin of Entomological Research 97, 327–335.CrossRefGoogle ScholarPubMed
Khan, ZR, James, DG, Midega, CAO and Pickett, JA (2008) Chemical ecology and conservation biological control. Biological Control 45, 210–224.CrossRefGoogle Scholar
Lambert, D (1992) Zero-inflated Poisson regression, with an application to defects in manufacturing. Technometrics 34, 1–14.CrossRefGoogle Scholar
Lewis, WJ and Martin, WR (1990) Semiochemicals for use with parasitoids: status and future. Journal of Chemical Ecology 16, 3067–3089.CrossRefGoogle Scholar
Leyva, JL, Browning, HW and Gilstrap, FE (1991) Effect of host fruit species, size, and color on parasitization of Anastrepha ludens (Diptera: Tephritidae) by Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environmental Entomology 20, 1469–1474.CrossRefGoogle Scholar
Malavasi, A (2000) Áreas-livres ou de baixa prevalência. In Malavasi, A and Zucchi, RA (eds), Moscas-das-frutas de Importância Econômica no Brasil: Conhecimento Básico e Aplicado. Ribeirão Preto, SP, Brazil: Holos, pp. 175–181.Google Scholar
Masry, A, Clarke, AR and Cunningham, JP (2018) Learning influences host versus nonhost discrimination and postalighting searching behavior in the Tephritid fruit fly parasitoid Diachasmimorpha kraussii (Hymenoptera: Braconidae). Journal of Economic Entomology 111, 787–794.CrossRefGoogle Scholar
Matthews, RW and Matthews, JR (2010) Insect Behavior. New York, USA: John Wiley & Sons.CrossRefGoogle Scholar
Meirelles, RN, Redaelli, LR, Jahnke, SM, Ourique, CB and Ozorio, DVB (2016) Parasitism of fruit flies (Tephritidae) in field, after the releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) in Rio Grande do Sul. Revista Brasileira de Fruticultura 38, 1–10.CrossRefGoogle Scholar
Morton, JF (1987) Guava. In Dowling, CF Jr (ed.), Fruits of Warm Climates. Winterville, NC, USA: Creative Resources Systems, pp. 356–363.Google Scholar
Nava, DE and Botton, M (2010) Bioecologia e Controle de Anastrepha Fraterculus e Ceratitis capitata em Pessegueiro. Pelotas, Brazil: Embrapa (Documento 315).Google Scholar
Nunes, MZ, Boff, MIC, Santos, RSS, Franco, CR, Wille, PE, Rosa, JM and Amarante, CVT (2015) Damage and development of Anastrepha fraterculus (Diptera: Tephritidae) in fruits of two pear cultivars. Agrociencia Uruguay 19, 42–48.Google Scholar
Ourique, CB, Redaelli, LR, Efrom, CFS and Pedrini, D (2018) Effects of kaolin and limestone on infestation of south American fruit fly in citrus orchards. Biological Agriculture & Horticulture 35, 61–71.CrossRefGoogle Scholar
Ovruski, SM, Aluja, M, Sivinski, J and Wharton, R (2000) Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: diversity, distribution, taxonomic status and their use in fruit fly biological control. Integrated Pest Management Reviews 5, 81–107.CrossRefGoogle Scholar
Ovruski, SM, Schliserman, P and Aluja, M (2004) Indigenous parasitoids (Hymenoptera) attacking Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in native and exotic host plants in northwestern Argentina. Biological Control 29, 43–57.CrossRefGoogle Scholar
Ovruski, SM, Wharton, RA, Rull, J and Guillén, L (2007) The effect of four fruit species on the parasitization rate of Anastrepha fraterculus (Diptera: Tephritidae, Trypetinae) by Diachasmimorpha longicaudata (Hymenoptera: Braconidae, Opiinae) under laboratory conditions. Biocontrol Science and Technology 17, 1079–1085.CrossRefGoogle Scholar
Piepho, HP (2004) An algorithm for a letter-based representation of all-pairwise comparisons. Journal of Computational and Graphical Statistics 13, 456–466.CrossRefGoogle Scholar
R Development Core Team, (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Santos, JP, Redaelli, LR, Sant'Ana, J and Hickel, ER (2015) Suscetibilidade de genótipos de macieira a Anastrepha fraterculus (Díptera: Tephritidae) em diferentes níveis de infestação. Revista Brasileira de Fruticultura 37, 90–95.CrossRefGoogle Scholar
Segura, DF, Viscarret, MM, Ovruski, SM and Cladera, JL (2012) Response of the fruit fly parasitoid Diachasmimorpha longicaudata to host and host-habitat volatile cues. Entomologia Experimentalis et Applicata 143, 164–176.CrossRefGoogle Scholar
Segura, DF, Nussenbaum, AL, Viscarret, MM, Devescovi, F, Bachmann, GE, Corley, JC, Ovruski, SM and Cladera, JL (2016) Innate host habitat preference in the parasitoid Diachasmimorpha longicaudata: functional significance and modifications through learning. PLoS One 11, 1–18.CrossRefGoogle ScholarPubMed
Shapiro, SS and Wilk, MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52, 591–611.CrossRefGoogle Scholar
Silva, JWP, Bento, JMS and Zucchi, RA (2007) Olfactory response of three parasitoid species (Hymenoptera: Braconidae) to volatiles of guavas infested or not with fruit fly larvae (Diptera: Tephritidae). Biological Control 41, 304–311.CrossRefGoogle Scholar
Sivinski, J and Aluja, M (2003) The evolution of ovipositor length in the parasitic hymenoptera and the search for predictability in biological control. Florida Entomologist 86, 143–150.CrossRefGoogle Scholar
Sivinski, J, Pinero, J and Aluja, M (2000) The distributions of parasitoids (Hymenoptera) of Anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracruz, Mexico. Biological Control 18, 258–269.CrossRefGoogle Scholar
Storeck, A, Poppy, GM, Van Emden, HF and Powell, W (2000) The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani. Entomologia Experimentalis et Applicata 97, 41–46.CrossRefGoogle Scholar
Stuhl, C, Sivinski, J, Teal, P, Paranhos, B and Aluja, M (2011) A compound produced by frugivorous Tephritidae (Diptera) larvae promotes oviposition behavior by the biological control agent Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environmental Entomology 40, 727–736.CrossRefGoogle Scholar
Stuhl, C, Sivinski, J, Teal, P and Aluja, M (2012) Responses of multiple species of tephritid (Diptera) fruit fly parasitoids (Hymenoptera: Braconidae: Opiinae) to sympatric and exotic fruit volatiles. Florida Entomologist 95, 1031–1039.CrossRefGoogle Scholar
Terán, HR (1977) Comportamiento alimentario y su correlación a la reproducción en hembras de Ceratitis capitata (Wied.) (Diptera: Tephritidae). Revista Agronómica del Noroeste Argentino 14, 17–34.Google Scholar
Turlings, TCJ and Wackers, FL (2004) Recruitment of predators and parasitoids by herbivore-injured plants. Advances in Insect Chemical Ecology 2, 21–75.CrossRefGoogle Scholar
Turlings, TCJ, Wackers, FL, Vet, LEM, Lewis, WJ and Tumlinson, JH (1993) Learning of host-finding cues by hymenopterous parasitoids. In Papaj, DR and Lewis, AC (eds), Insect Learning: Ecological and Evolutionary Perspectives. New York, NY, USA: Chapman & Hall, pp. 51–78.CrossRefGoogle Scholar
Vinson, SB (1976) Host selection by insect parasitoids. Annual Review of Entomology 21, 109–33.CrossRefGoogle Scholar
War, AR, Paulraj, MG, Ahmad, T, Buhroo, AA, Hussainm, B, Ignacimuthu, S and Sharma, HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signaling and Behavior 7, 1306–1320.CrossRefGoogle ScholarPubMed
Wäschke, N, Meiners, T and Rostás, M (2013) Foraging strategies of parasitoids in complex chemical environments. In Wajnberg, E and Colazza, S (eds), Chemical Ecology of Insect Parasitoids. West Sussex, UK: John Wiley & Sons, pp. 37–63.CrossRefGoogle Scholar
Yuan, JS, Kollner, TG, Wiggins, G, Grant, J, Degenhardt, J and Chen, F (2008) Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. The Plant Journal 55, 491–503.CrossRefGoogle ScholarPubMed
Zadra, WC, Sant'Ana, J, Redaelli, LR and Tognon, R (2018) Plasticidade da aprendizagem de Diachasmimorpha longicaudata (Hymenoptera: Braconidae) associada a voláteis de frutos e óleos essenciais. Iheringia, Série zoologia 108, 1–9.CrossRefGoogle Scholar
Zart, M, Fernandes, OA and Botton, M (2009) Bioecologia e controle da mosca-das-frutas sul-americana Anastrepha fraterculus (Diptera: Tephritidae) na cultura da videira. Bento Gonçalves, Brazil: Embrapa (Circular técnica 81).Google Scholar
Zhöu, JJ (2010) Odorant-binding proteins in insects. Vitamins and Hormones 83, 241–272.CrossRefGoogle ScholarPubMed
Zucchi, RA (2000) Taxonomia. In Malavasi, A and Zucchi, RA (eds), Moscas-das-frutas de importância econômica no Brasil: conhecimento básico e aplicado. Ribeirão Preto, SP, Brazil: Holos, pp. 13–24.Google Scholar