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Effects of toxic baits and food-based attractants for fruit flies on the parasitoid Fopius arisanus (Sonan) (Hymenoptera: Braconidae)

Published online by Cambridge University Press:  04 September 2019

Simón Farah ,
Matheus Rakes ,
Diego Portalanza Open the ORCID record for Diego Portalanza [Opens in a new window] ,
Dori E. Nava ,
Angelica Durigon ,
Anderson D. Grützmacher ,
Nivia Dias-Pini  and
Mariuxi Goméz-Torres
Simón Farah*
Affiliation:
Ministry of Agriculture, Livestock, Aquaculture and Fisheries – MAGAP, ZIP Code 170517, Quito, Ecuador Federal University of Pelotas, Postal Code 96010-610, Pelotas, RS, Brazil
Matheus Rakes
Affiliation:
Federal University of Pelotas, Postal Code 96010-610, Pelotas, RS, Brazil
Diego Portalanza
Affiliation:
Federal University of Santa Maria, Postal Code 97105-900, Santa Maria (RS), Brazil
Dori E. Nava
Affiliation:
Embrapa Clima Temperado, Postal Code 96010-971, Pelotas, RS, Brazil
Angelica Durigon
Affiliation:
Federal University of Santa Maria, Postal Code 97105-900, Santa Maria (RS), Brazil
Anderson D. Grützmacher
Affiliation:
Federal University of Pelotas, Postal Code 96010-610, Pelotas, RS, Brazil
Nivia Dias-Pini
Affiliation:
Embrapa Agroindústria Tropical, ZIP Code 60511-110, Fortaleza, CE, Brazil
Mariuxi Goméz-Torres
Affiliation:
Ministry of Agriculture, Livestock, Aquaculture and Fisheries – MAGAP, ZIP Code 170517, Quito, Ecuador
*
Author for correspondence: Simón Farah, Email: simonfarah2006@hotmail.com
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Abstract

This study aimed to evaluate the effects of toxic baits and attractants for fruit flies on the biology of its parasitoid Fopius arisanus. We tested two food-based attractants; hydrolysed corn protein (Biofruit® 3%) and sugarcane molasses (7%), their mixtures with spinosad and malathion-based insecticides, and a ready-to-use commercial bait (Success 0.02 CB®). Malathion-based lures were used as references for mortality (i.e., positive control), while negative control was honey. The formulations Biofruit® + malathion (T1), molasses + malathion (T2), and spinosad + molasses (T3) were toxic to F. arisanus, being classified as harmful (class 4). In addition, toxic baits composed of Biofruit + spinosad (T4) reduced parasitism by 97.99%, being rated as moderately harmful (class 3). Yet, Success 0.02 CB® (T7) was considered slightly toxic (class 2), causing a 64.55% reduction in parasitism. Regarding the biological parameters of F. arisanus, offspring number and parasitoid longevity were significantly reduced by using hydrolysed protein attractants when compared to the control (honey). However, sugarcane molasses improved parasitoid reproduction and longevity, as did the honey. Lastly, ingestion tests showed the major role of attractants in toxic-bait formulations against F. arisanus.

Keywords

Biological controlformulationsintegrated managementselectivityTephritidae
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 2 , April 2020 , pp. 278 - 284
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Copyright
Copyright © Cambridge University Press 2019

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References

Appiah, EF, Ekesi, S, Salifu, D, Afreh-Nuamah, K, Obeng-Ofori, D, Khamis, F and Mohamed, SA (2013) Effect of temperature on immature development and longevity of two introduced opiine parasitoids on Bactrocera invadens. Journal Applied Entomology 137, 571–579. https://doi.org/10.1111/jen.12036.CrossRefGoogle Scholar
Beloti, VH, Alves, GR, Araújo, DFD, Picoli, MM, Moral, RA, Demétrio, CGB and Yamamoto, PT (2015) Lethal and sublethal effects of insecticides used on citrus, on the ectoparasitoid Tamarixia radiata. PloS One 10, 1–14. https://doi.org/10.1371/journal.pone.0132128.CrossRefGoogle ScholarPubMed
Benelli, G, Giunti, G, Tena, A, Desneux, N, Caselli, A and Canale, A (2017) The impact of adult diet on parasitoid reproductive performance. Journal of Pest Science 90, 1–17. https://doi.org/10.1007/s10340-017-0835-2.CrossRefGoogle Scholar
Bhargavi, M (2016) Sensitivity of Trichogramma japonicum (Ashmead) to different insecticides. Asian Journal of Science and Technology 7, 2585–2587.Google Scholar
Bittencourt, MAL, Santos, OOD, Brito, EDA, Araújo, EL and Marinho, CF (2012) Parasitoids associated with Anastrepha (tephritidae) in host fruits on the Southern coast of Bahia, Brazil. Revista Ciência Agronômica 43, 811–815. https://doi.org/10.1590/S1806-66902012000400024.CrossRefGoogle Scholar
Blibech, I, Ksantini, M, Jardak, T and Bouaziz, M (2015) Effect of insecticides on Trichogramma parasitoids used in biological control against sprays oleae insect pest. Advances in Chemical Engineering and Science 5, 362–372. https://doi.org/10.4236/aces.2015.53038.CrossRefGoogle Scholar
Boller, E, Vogt, H, Ternes, P and Malavolta, C (2006) Working document on selectivity of pesticides (2005): Internal Newsletter issued by the publication commission for the IOBC/WPRS council and executive committee, Issue Nr 40.Google Scholar
Botton, M, Arioli, CJ, Machota, MZ Jr, Nunes, MZ and Rosa, JM (2016) Moscas das-frutas na fruticultura de clima temperado: situação atual e perspectivas de controle através do emprego de novas formulações de iscas tóxicas e da captura massal. Agropecuária Catarinense 29, 103–108.Google Scholar
Castilhos, RV, Grützmacher, AD, Nava, DE, Zotti, MJ, Siqueira, PRB and Spagnol, D (2013) Selectivity of pesticides used in peach orchards on the larval stage of the predator Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae). Semina: Ciências Agrarias 34, 3585–3596. https://doi.org/10.5433/1679-0359.Google Scholar
Costa, MA, Moscardini, VF, Gontijo, PC, Carvalho, GA, Oliveira, RL and Oliveira, HN (2014) Sublethal and transgenerational effects of insecticides in developing Trichogramma galloi (Hymenoptera: Trichogrammatidae). Ecotoxicology 23, 1399–1408. https://doi.org/10.1007/s10646-014-1282-y.CrossRefGoogle Scholar
Dias, VS, Silva, JG, Lima, KM, Petitinga, CS, Hernández-Ortiz, V, Laumann, RA and Joachim-Bravo, IS (2016) An integrative multidisciplinary approach to understanding cryptic divergence in Brazilian species of the Anastrepha fraterculus complex. Biological Journal of the Linnean Society 117, 725–746. https://doi.org/10.1111/bij.12712.CrossRefGoogle Scholar
Gonçalves, RS, Nava, DE, Pereira, HC, Lisbôa, H, Grützmacher, AD and Valgas, RA (2013) Biology and fertility life table of Aganaspis pelleranoi (Hymenoptera: Figitidae) in larvae of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae). Annals of the Entomological Society of America 106, 791–798. https://doi.org/10.1603/AN13044.CrossRefGoogle Scholar
Groth, MZ, Loeck, AE, Nörnberg, SD, Bernardi, D and Nava, DE (2016) Biology of Fopius arisanus (Hymenoptera: Braconidae) in two species of fruit flies. Journal of Insect Science 16, 1–7. https://doi.org/10.1093/jisesa/iew087.CrossRefGoogle ScholarPubMed
Harris, EJ, Bautista, RC, Vargas, RI and Jang, EB (2007) Rearing Fopius arisanus (Sonan) (Hymenoptera: Braconidae) in Mediterranean fruit fly (Diptera: Tephritidae). Proceedings of the Hawaiin Entomological Society 39, 121–126. http://hdl.handle.net/10125/1298.Google Scholar
Härter, W, Grützmacher, AD, Nava, DE, Gonçalves, RS and Botton, M (2011) Isca tóxica e disrupção sexual no controle da mosca-da-fruta sul-americana e da mariposa-oriental em pessegueiro. Pesquisa Agropecuária Brasileira 45, 229–235. https://doi.org/10.1590/S0100-204X2010000300001.CrossRefGoogle Scholar
Härter, WR, Botton, M, Nava, DE, Grützmacher, AD, Gonçalves, RS, Machota, R Jr, Bernardi, D and Zanardi, OZ (2015) Toxicities and residual effects of toxic baits containing Spinosad or Malathion to control the adult Anastrepha fraterculus (Diptera: Tephritidae). Florida Entomologist 98, 202–208. https://doi.org/10.1653/024.098.0135.CrossRefGoogle Scholar
Harvey, JA, Cloutier, J, Visser, B, Ellers, J, Wäckers, FL and Gols, R (2012) The effect of different dietary sugars and honey on longevity and fecundity in two hyperparasitoid waps. Journal of Insect Physiology 58, 816–823. https://doi.org/10.1016/j.jinsphys.2012.03.002.CrossRefGoogle Scholar
Hogervorst, PA, Wäckers, FL and Romeis, J (2007) Effects of honeydew sugar composition on the longevity of Aphidius ervi. Entomologia Experimentalis et Applicata 122, 223–232. https://doi.org/10.1111/j.1570-7458.2006.00505.x.CrossRefGoogle Scholar
Kovaleski, A, Sugayama, RL and Malavasi, A (1999) Movement of Anastrepha fraterculus from native breeding sites into apple orchards in Southern Brazil. Entomologia Experimentalis et Applicata 91, 459–465. https://doi.org/10.1046/j.1570-7458.1999.00514.x.CrossRefGoogle Scholar
Malavasi, A and Zucchi, RA (2000) Moscas-das-frutas de importância econômica no Brasil: conhecimento básico e aplicado. Ribeirão Preto: Holos editora, 327p.Google Scholar
Manoukis, NC, Geib, SM and Vargas, RI (2014) Effect of host Bactrocera dorsalis sex on yield and quality of the parasitoid Fopius arisanus. BioControl 59, 395–402. https://doi.org/10.1007/s10526-014-9575-x.CrossRefGoogle Scholar
Mendiburu, F (2016) Agricolae: Statistical Procedures for Agricultural Research. R package version 1. pp. 2–4.Google Scholar
Narváez, A, Cancino, J, Canal, DN and Wyckhuys, KAG (2012) Effect of different dietary resources on longevity, carbohydrate metabolism, and ovarian dynamics in two fruit fly parasitoids. Arthropod-Plant Interactions 6, 361–374. https://doi.org/10.1007/s11829-012-9188-1.CrossRefGoogle Scholar
Nicácio, JN, Uchôa, MA, Faccenda, O, Guimarães, JA and Marinho, CF (2011) Native larval parasitoids (Hymenoptera) of frugivorous Tephritoidea (Diptera) in south pantanal region, Brazil. Florida Entomologist 94, 407–419. https://doi.org/10.1653/024.094.0305.CrossRefGoogle Scholar
Nunes, AM, Müller, F, Gonçalves, RS, Garcia, MS, Costa, V and Nava, DE (2013) Moscas frugívoras e seus parasitoides nos municípios de Pelotas e Capão do Leão, Rio Grande do Sul, Brasil. Ciência Rural 42, 6–12. http://dx.doi.org/10.1590/S0103-84782012000100002.CrossRefGoogle Scholar
Pelz, KS, Isaacs, R, Wise, JC and Gut, LJ (2005) Protection of fruit against infestation by apple maggot and blueberry maggot (Diptera: Tephritidae) using compounds containing spinosad. Journal of Economic Entomology 98, 432–437. https://doi.org/10.1603/0022-0493-98.2.432.CrossRefGoogle ScholarPubMed
Perre, P, Faria, FA, Jorge, LR, Rocha, A, Torres, RS, Souza-Filho, MF and Zucchi, RA (2016) Toward an automated identification of Anastrepha fruit flies in the fraterculus group (Diptera, Tephritidae). Neotropical Entomology 45, 554–558. https://doi.org/10.1007/s13744-016-0403-0.CrossRefGoogle Scholar
Poncio, S, Nunes, MA, Gonçalves, RS, Lisboa, H, Manica-Berto, R, Garcia, SM and Nava, DE (2016) Biology of Doryctobracon brasiliensis at different temperatures: development of life table and determining thermal requirements. Journal of Applied Entomology 140, 775–785. https://doi.org/10.1111/jen.12308.CrossRefGoogle Scholar
Prokopy, RJ, Papaj, DR, Hendrichs, J and Wong, TTY (1992) Behavioral responses of Ceratitis capitata flies to bait spray droplets and natural food. Entomologia Experimentalis et Applicata 64, 247–257. https://doi.org/10.1111/j.1570-7458.1992.tb01615.x.CrossRefGoogle Scholar
Purcell, MF, Groth, JD and Messing, RH (1994) Insecticide effect on three tephritid fruit flies and associated braconid parasitoids in Hawaii. Journal of Economic Entomology 87, 1455–1462. https://doi.org/10.1093/jee/87.6.1455.CrossRefGoogle Scholar
R development core team (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rousse, P, Harris, EJ and Quilici, S (2005) Fopis arisanus, an egg-pupal parasitoid of Tephritidae. Overview. Biocontrol News and Information 26, 59–69.Google Scholar
Ruiz, L, Flores, S, Cancino, J, Arredondo, J, Valle, J, Díaz-Fleischer, F and Williams, T (2008) Lethal and sublethal effects of spinosad-based GF-120 bait on the tephritid parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Biological Control 44, 296–304. https://doi.org/10.1016/j.biocontrol.2007.10.022.CrossRefGoogle Scholar
Salles, LAB (1992) Metodologia de criação de Anastrepha fraterculus (Wiedemann, 1830) (Diptera: Tephritidae) em dieta artificial em laboratório. Anais da Sociedade Entomológica do Brasil 21, 479–486.Google Scholar
Santos, WGN, Fernandes, EC, Araujo, EL, Ferreira, ADCL and Lacerda Filho, MLB (2013) Moscas-das-frutas em um pomar comercial de mangueira, no Litoral do Rio Grande do Norte. Agropecuária Científica no Semiárido 9, 01–06.Google Scholar
Souza, AR, Lopes-Mielezrski, GN, Lopes, EN, Querino, RB, Corsato, CDA, Giustolin, TA and Zucchi, RA (2012) Hymenopteran parasitoids associated with frugivorous larvae in a Brazilian Caatinga-Cerrado ecotone. Environmental Entomology 41, 233–237. http://dx.doi.org/10.1603/EN11121.CrossRefGoogle Scholar
Souza, CR, Sarmento, RA, Venzon, M, Santos, GRD, Silveira, MCAC and Tschoeke, PH (2015) Lethal and sublethal effects of neem on Aphis gossypii and Cycloneda sanguinea in watermelon. Acta Scientiarum. Agronomy 37, 233–239. http://dx.doi.org/10.4025/actasciagron.v37i2.19517.CrossRefGoogle Scholar
Tompkins, JM, Wratten, SD and Wäckers, FL (2010) Nectar to improve parasitoid fitness in biological control: does the sucrose: hexose ratio matter? Basic and Applied Ecology 11, 264–271. https://doi.org/10.1016/j.baae.2009.12.010.CrossRefGoogle Scholar
Vargas, RI, Peck, SL, Mc Quate, GT, Jackson, CG, Stark, JD and Armstrong, JW (2001) Potential for areawide integrated management of Mediterranean fruit fly (Diptera: Tephritidae) with a braconid parasitoid and a novel bait spray. Journal Economic Entomology 94, 817–825. https://doi.org/10.1603/0022-0493-94.4.817.CrossRefGoogle Scholar
Vargas, RI, Miller, NW and Prokopy, RJ (2002) Attraction and feeding responses of Mediterranean fruit fly and a natural enemy to protein baits laced with two novel toxins, phloxine B and spinosad. Entomologia Experimentalis et Applicata 102, 273–282. https://doi.org/10.1046/j.1570-7458.2002.00948.x.CrossRefGoogle Scholar
Vargas, RI, Leblanc, L, Putoa, R and Eitam, A (2007) Impact of introduction of Bactrocera dorsalis (Diptera: Tephritidae) and classical biological control releases of Fopius arisanus (Hymenoptera: Braconidae) on economically important fruit flies in French Polynesia. Journal of Economic Entomology 100, 670–679. https://doi.org/10.1603/0022-0493.CrossRefGoogle ScholarPubMed
Vargas, RI, Stark, JD, Banks, J, Leblanc, L, Manoukis, NC and Peck, S (2013) Spatial dynamics of two oriental fruit fly (Diptera: Tephritidae) parasitoids, Fopius arisanus and Diachasmimorpha longicaudata (Hymenoptera: Braconidae), in a guava orchard in Hawaii. Environmental Entomology 42, 888–901. https://doi.org/10.1603/EN12274.CrossRefGoogle Scholar
Wakefield, ME, Bell, HA and Gatehouse, AM (2010) Longevity and fecundity of Eulophus pennicornis, an ectoparasitoid of the tomato moth Lacanobia oleracea, is affected by nutritional state and diet quality. Agricultural and Forest Entomology 12, 19–27. https://doi.org/10.1111/j.1461-9563.2009.00441.x.CrossRefGoogle Scholar
Wang, XG and Messing, RH (2008) Role of egg-laying experience in avoidance of superparasitism by fruit fly parasitoid Fopius arisanus (Hymenoptera: Braconidae). Annals of the Entomological Society of America 101, 656–663. https://doi.org/10.1603/0013-8746(2008)101[656:ROEEIA]2.0.CO;2.CrossRefGoogle Scholar
Wang, XG, Jarjees, EA, McGraw, BK, Bokonon-Ganta, AH, Messing, RH and Johnson, MW (2005) Effects of spinosad-based fruit fly bait GF-120 on tephritid fruit fly and aphid parasitoids. Biological Control 35, 155–162. https://doi.org/10.1016/j.biocontrol.2005.07.003.CrossRefGoogle Scholar
Zenil, M, Liedo, P, Williams, T, Valle, J, Cancino, J and Montoya, P (2004) Reproductive biology of Fopius arisanus (Hymenoptera: Braconidae) on Ceratitis capitata and Anastrepha spp. (Dip.: Tephritidae). Biological Control 29, 169–178. https://doi.org/10.1016/S1049-9644(03)00140-3.CrossRefGoogle Scholar