Abstract
Biological control by the generalist egg parasitoid Fopius arisanus (Sonan) (Hymenoptera: Braconidae) has been proposed against Bactrocera carambolae (Drew & Hancock) (Diptera: Tephritidae) in northern Brazil. This study assessed possible effects of F. arisanus on native parasitoids by focusing on competition with the native wasp Doryctobracon areolatus (Szépligeti) (Hymenoptera: Braconidae) on two hosts, Anastrepha fraterculus (Wiedemann), a native tephritid, and Ceratitis capitata (Wiedemann), an introduced pest tephritid. Laboratory and greenhouse cage studies showed that F. arisanus parasitized < 3% of the native host in competition or alone compared to 41–65% for C. capitata, while D. areolatus parasitized 12–42% of the native host and < 4% on C. capitata. The host origin of F. arisanus did not affect subsequent parasitism rates on native or exotic hosts. However, when reared on C. capitata, F. arisanus had higher parasitism on C. capitata than on A. fraterculus. Lab and greenhouse competition studies showed that F. arisanus had no measurable detrimental effect on the native parasitoid in either the native or introduced host, suggesting that F. arisanus interfered minimally with the native parasitoid. Based on these results and other relevant studies showing non-preference of F. arisanus for the native fruit fly species, as well as the non-preference of native parasitoids for exotic fruit flies, we infer that the release of F. arisanus against exotic tephritids such as C. capitata and B. carambolae in Brazil would not cause major disruption of the native populations of A. fraterculus parasitoids.
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References
Adaime R, Sousa MSM, Jesus-Barros CRD, Deus GE, Pereira JF, Strikis PC, Souza-Filho MF (2017) Frugivorous flies (Diptera: Tephritidae, Lonchaeidae), their host plants, and associated parasitoids in the extreme north of Amapá state, Brazil. Fla Entomol 100:316–324
Adaime R, Lima AL, Sousa MSM (2018) Conservative biological control of fruit flies in the Brazilian Amazon. Innovations Agronomiques 64:47–59
Aluja M, Ovruski SM, Sivinski J, Córdova-García G, Schliserman P, Núñez-Campero SR, Ordano M (2013) Inter-specific competition and competition-free space in the tephritid parasitoids Utetes anastrephae and Doryctobracon areolatus (Hymenoptera: Braconidae: Opiinae). Ecol Entomol 38:485–496
Bess HA, van Den Bosch R, Haramoto FH (1961) Fruit fly parasites and their activities in Hawaii. Proc Hawaii Entomol Soc 17:367–378
Bittencourt MAL, Santos OO, Brito EA, Araújo EL, Marinho CF (2012) Parasitoids (Braconidae) associated with Anastrepha (Tephritidae) in host fruits on the Southern coast of Bahia. Brazil Rev Ciên Agron 43(4):811–815
Bokonon-Ganta AH, Ramadan MM, Messing RH (2007) Reproductive biology of Fopius ceratitivorus (Hymenoptera: Braconidae), an egg-larval parasitod of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Biol Control 41:361–367
Brasil. Ministério da agricultura, pecuária e abastecimento. Instrução normativa n◦ 38, de 1 de outubro de 2018. Diário Oficial [da] República Federativa do Brasil, Brasília, DF, 2 out. 2018. Seção 1. https://www.in.gov.br/materia/-/asset_publisher/Kujrw0TZC2Mb/content/id/43461167/do1-2018-10-02-instrucao-normativa-n-38-de-1-de-outubro-de-2018-43461024. Accessed 15 December 2019.
Castilho AP, Pasinato J, Santos JEV, Costa AS, Nava DE, Jesus CR, Adaime R (2019) Biology of Bactrocera carambolae (Diptera: Tephritidae) on four hosts. Rev Bras Entomol 63:302–307
Daane KM, Wang X, Nieto DJ, Pickett CH, Hoelmer KA, Blanchet A, Johnson MW (2015) Classic biological control of olive fruit fly in California, USA: release and recovery of introduced parasitoids. BioControl 60:317–330
Duyck PF, David P, Quilici S (2007) Can more k-selected species be better invaders? a case study of fruit flies in La Réunion. Diversity Distrib 13:535–543
George J, Lapointe SL (2019) Host-plant resistance associated with Poncirus trifoliata influence oviposition, development and adult emergence of Diaphorina citri (Hemiptera: Liviidae). Pest Manag Sci 75:279–285
Gnanvossou D, Hanna R, Bokonon-Ganta AH, Ekesi S, Mohamed SA (2016) Release, establishment and spread of the natural enemy Fopius arisanus (Hymenoptera: Braconidae) for control of the invasive oriental fruit fly Bactrocera dorsalis (Diptera: Tephritidae) in Benin, West Africa. In: Ekesi S, Mohamed S, De Meyer M (eds) Fruit fly research and development in Africa—Towards a sustainable management strategy to improve horticulture. Springer, Cham, Switzerland, pp 575–600
Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton, NJ
Gonçalves RS, Nunes AM, Poncio S, Manica-Berto R, Nornberg SD, Grutzmacher AD, Nava DE (2018) Bionomics, thermal requirements and life table of the fruit fly parasitoid Doryctobracon areolatus (Hymenoptera: Braconidae) under various thermal regimes. Biol Control 127:101–108
Groth MZ, Loeck AE, Nornberg SD, Bernardi D, Nava DE (2016) Biology of Fopius arisanus (Hymenoptera: Braconidae) in two species of fruit flies. J Insect Sci 16(1):96
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
King BH (1987) Offspring sex ratios in parasitoid wasps. Q Rev Biol 62:367–396
Liquido NJ, McQuate GT, Birnbaum AL, Halin M, Nakamichi K, Inskeep J, Ching A, Marnell S, Kurashima R (2017) A review of recorded host plants of oriental fruit fly, Bactrocera (Bactrocera) dorsalis (Hendel) (Diptera: Tephritidae). USDA CPHST. https://coffhi.cphst.org/. Accessed 23 November 2019
Manoukis N, Geib S, Seo D, Mckenney M, Vargas R, Jang E (2011) An optimized protocol for rearing Fopius arisanus, a parasitoid of tephritid fruit flies. J Vis Exp 53:e2901
Ministério da agricultura, pecuária e abastecimento. Instrução normativa n° 39, de 1 de outubro de (2018) Lista de pragas quarentenárias ausentes (PQA) para o Brasil. Diário Oficial da União, Brasília 190(1):11–14
Marchioro CA (2016) Global potential distribution of Bactrocera carambolae and the risks for fruit production in Brazil. PLoS ONE 11(11):e0166142
Marsaro Júnior AL, Deus EG, Ronchi-Teles B, Adaime R, Silva Júnior RJ (2013) Species of Anastrepha (Diptera: Tephritidae) captured in a guava orchard (Psidium guajava L., Myrtaceae) in Boa Vista, Roraima. Brazil Braz J Biol 73:879–886
Montoya P, Cancino J, Pérez-Lachaud G, Liedo P (2011) Host size, superparasitism and sex ratio in mass-reared Diachasmimorpha longicaudata, a fruit fly parasitoid. BioControl 56:11–17
Montoya P, López P, Cruz J, López F, Cadena C, Cancino J, Liedo P (2017) Effect of Diachasmimorpha longicaudata releases on the native parasitoid guild attacking Anastrepha spp. larvae in disturbed zones of Chiapas. Mexico BioControl 62:581–593
Montoya P, Suárez A, Cancino J (2009) Fopius arisanus oviposition in four Anastrepha fruit fly species of economic importance in Mexico. BioControl 54:437–444
Murillo FD, Cabrera-Mireles H, Barrera JF, Liedo P, Montoya P (2015) Doryctobracon areolatus (Hymenoptera, Braconidae) a parasitoid of early developmental stages of Anastrepha obliqua (Diptera, Tephritidae). J Hymenopt Res 46:91–105
Murillo FD, Montoya P, Cabrera-Mireles H, Barrera JF, Liedo P (2019) Intrinsic competition between Diachasmimorpha longicaudata and three native species of parasitoids (Hymenoptera: Braconidae: Opiinae) of Anastrepha (Diptera: Tephritidae) fruit flies under laboratory conditions. Biocontrol Sci Technol 29:230–240
Nunes AM, Costa KZ, Faggioni KM, Costa MLZ, Gonçalves RS, Walder JMM, Garcia MS, Nava DE (2013) Artificial diets for the rearing of adult and larvae of South American fruit fly. Pesq Agropec Bras 48:1309–1314
Nunes AM, Nava DE, Muller FA, Gonçalves RS, Garcia MS (2011) Biology of Doryctobracon areolatus and parasitism on Anastrepha fraterculus larvae, in the laboratory. Pesq Agropec Bras 46:679–671
Ovruski SM, Schliserman P, Aluja M (2004) Indigenous parasitoids (Hymenoptera) attacking Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in native and exotic host plants in Northwestern Argentina. Biol Control 29:43–57
Ovruski SM, Wharton RA, Schliserman P, Aluja M (2005) Abundance of Anastrepha fraterculus (Diptera: Tephritidae) and its associated native parasitoids (Hymenoptera) in “feral” guavas growing in the endangered northernmost Yungas forests of Argentina with an update on the taxonomic status of opiine parasitoids previously reported in this country. Environ Entomol 34(4):807–818
Paranhos BJ, Sivinski J, Stuhl C, Holler T, Aluja M (2013) Intrinsic competition and competitor-free-space influence the coexistence of parasitoids (Hymenoptera: Braconidae: Opiinae) of Neotropical Tephritidae (Diptera). Environ Entomol 42:717–723
Paranhos BJ, Nava DE, Malavasi A (2019) Biological control of fruit flies in Brazil. Pesq Agropec Bras 54:e26037
Purcell MF (1998) Contribution of biological control to integrated pest management of tephritid fruit flies in the tropic and subtropics. Int Pest Manage Rev 3:63–83
Purcell MF, Herr JC, Messing RH, Wong TT (1998) Interaction between augmentatively released Diachasmimorpha longicaudata (Hymenoptera: Braconidae) and a complex of opiine parasitoids in a commercial guava orchard. Biocontrol Sci Technol 8:139–151
Poncio S, Montoya P, Cancino J, Nava DE (2015) Is Anastrepha obliqua (Diptera: Tephritidae) a natural host of the Neotropical parasitoids Doryctobracon crawfordi and Opius hirtus? Austral Entomol 55:18–24
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/
Ramadan MM, Wong TTY, Beardsley JW (1992) Reproductive behavior of Biosteres arisanus (Sonan) (Hymenoptera: Braconidae), an egg-larval parasitoid of the oriental fruit fly (Diptera: Tephritidae). Biol Control 2:28–34
Ricalde MP, Nava DE, Loeck AE, Donatti MG (2012) Temperature-dependent development and survival of Brazilian populations of the Mediterranean fruit fly, Ceratitis capitata, from tropical, subtropical and temperate regions. J Insect Sci 12:33
Rocha KL, Mangine T, Harris EJ, Lawrence PO (2004) Immature stages of Fopius arisanus (Hymenoptera: Braconidae) in Bactrocera dorsalis (Diptera: Tephritidae). Fla Entomol 87:164–168
Rousse P, Harris EJ, Quilice S (2005) Fopius arisanus, an egg-pupal parasitoid of Tephritidae. Overview Biocontrol News and Information 26:59–69
Silva JG, Dutra VS, Santos MS, Silva NMO, Vidal DB, Nink RA, Guimarães JA, Araujo EL (2010) Diversity of Anastrepha spp. (Diptera: Tephritidae) and associated braconid parasitoids from native and exotic hosts in Southeastern Bahia, Brazil. Environ Entomol 39(5):1457–1465
Sime KR, Daane KM, Wang XG, Johnson MW, Messing RH (2008) Evaluation of Fopius arisanus as a biological control agent for the olive fruit fly in California. Agric Forest Entomol 10:423–431
Sivinski J, Aluja M, Holler T, Eitam A (1998) Phenological comparison of two braconid parasitoids of the Caribbean fruit fly (Diptera: Tephritidae). Environ Entomol 27:360–365
Suárez L, Biancheri MJB, Sánchez G, Cancino J, Murúa F, Bilbao M, Molina D, Laria O, Ovruski SM (2020) Radiation on medfly larvae of tsl Vienna-8 genetic sexing strain displays reduced parasitoid encapsulation in mass-reared Diachasmimorpha longicaudata (Hymenoptera: Braconidae). J Econ Entomol 113(3):1134–1144
Van den Bosch R, Haramoto FH (1953) Competition among parasites of the oriental fruit fly. P Hawaii Entomol Soc 15:201–206
Vargas RI, Leblanc L, Harris EJ, Manoukis NC (2012) Regional suppression of Bactrocera fruit flies (Diptera: Tephritidae) in the Pacific through biological control and prospects for future introductions into other areas of the world. Insects 3:727–742
Vargas RI, Nishida T, Beardsley JW (1993) Opiine parasitoids (Hymenoptera: Braconidae) of oriental fruit fly (Diptera: Tephritidae) on Kauai island, Hawaii: island wide relative abundance and parasitism rates in wild and orchard guava habitats. Environ Entomol 22:246–253
Wang XG, Messing RH (2003) Intra- and interspecific competition by Fopius arisanus and Diachasmimorpha tryoni (Hymenoptera: Braconidae), parasitoids of tephritid fruit flies. Biol Control 27:251–259
Wang XG, Messing RH, Bautista RC (2003) Competitive superiority of early acting species: a case study of opiine fruit fly parasitoids. Biocontrol Sci Technol 13:391–402
Wharton RA (1989) Classical biological control of fruit Tephritidae. In: Robinson A, Harper G (eds) World crop pests. Fruit flies: their biology, natural enemies, and control, 3B edn. Elsevier Science, Amsterdam, pp 303–313
Yang JQ, Cai PM, Chen J, Zhang HH, Wang C, Xiang HJ, Wu J, Yang YC, Chen JH, Ji QE, Song DG (2018) Interspecific competition between Fopius arisanus and Psyttalia incisi (Hymenoptera: Braconidae), parasitoids of Bactrocera dorsalis (Diptera: Tephritidae). Biol Control 121:183–189
Zenil M, Liedo P, Williams T, Valle J, Cancino J, Montoya P (2004) Reproductive biology of Fopius arisanus (Hymenoptera: Braconidae) on Ceratitis capitata and Anastrepha spp. (Diptera: Tephritidae). Biol Control 29:169–178
Zucchi RA, Moraes RCB (2008) Fruit flies in Brazil–Anastrepha species their host plants and parasitoids. http:/www.lea.esalq.usp.br/anastrepha/, updated on November 28, 2019. Accessed on June 23, 2020
Acknowledgements
We thank Dr. Eric Jang (USDA-ARS, Hilo, Hawaii USA) for graciously sending us five shipments of Ceratitis capitata pupae parasitized by Fopius arisanus, between 29 August 2012 and 24 June 2013 under material transfer agreement LQC Nº 014/2012. We wish to thank David Andow for English reviewing, and suggestions in the manuscript, Maria de Lourdes Z. da Costa for providing laboratory cages for the first experiment, and Roberto A. A. Pereira and Martin Z. Groth who helped us with the lab and greenhouse experiments. We would like to thank the financial support of FACEPE, process APQ-0012-5.01/15. Opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the USDA. USDA is an equal opportunity employer.
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Paranhos, B.A.G., Poncio, S., Morelli, R. et al. Non-target effects of the exotic generalist parasitoid wasp Fopius arisanus (Sonan) estimated via competition assays against Doryctobracon areolatus (Szepligeti) on both native and exotic fruit fly hosts. BioControl 66, 83–96 (2021). https://doi.org/10.1007/s10526-020-10057-4
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DOI: https://doi.org/10.1007/s10526-020-10057-4