Abstract
Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), known as Medfly, is a severe agricultural invasive pest in Argentinian fruit-producing regions. The native habitat disturbance and introduction and spread of exotic host plants strongly favored Medfly proliferation. This scenario is common throughout the northern subtropical citrus-growing region. Environmentally friendly strategies to suppress Medfly populations by the National Fruit Fly Control and Eradication Program have currently been taken. One of these actions involves augmentative biological control through releases of the exotic parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Consequently, the hypothesis that the effectiveness of D. longicaudata females, from two different population lines, in controlling Medfly larvae progressively increases as the density of released females increases was tested. One parasitoid line derives from larvae of a biparental Medfly strain. The other hails from irradiated larvae of the genetic sexing Temperature Sensitive Lethal Vienna-8 medfly strain reared at the “BioPlanta San Juan” biofactory. Parasitoids foraged for 24 h on peaches artificially inoculated with naked lab-reared biparental Medfly larvae. Peaches were placed near the roof or on the ground in field cages. Five treatments (20, 40, 80, 160, and 320 females released) and a control (no parasitoids) for each population line were carried out throughout summer and autumn 2016. Host density (200 larvae) remained constant. At 320 released parasitoid females, both D. longicaudata population lines highly increased the Medfly mortality in both testing seasons, and foraged skillfully on peaches at both fruit height levels. These data encourage the application of augmentative biological control against Medfly.
This is a preview of subscription content, log in via an institution to check access.
References
Aluja M, Ordano M, Guillen L, Rull J (2012) Understanding long-term fruit flies (Diptera: Tephritidae) population dynamics: implications for area wide management. J Econ Entomol 105:823–836. https://doi.org/10.1603/EC11353
Buonocore Biancheri MJ, Suárez LC, Bezdjian LP, Van Nieuwenhove GA, Rull J, Ovruski SM (2019) Response of two parasitoid species (Hymenoptera: Braconidae, Figitidae) to tephritid host and host food substrate cues. J Appl Entomol 143:344–356. https://doi.org/10.1111/jen.12595
Carta Gadea SL, Suárez L, Buonocore Biancheri MJ, Murúa F, Molina D, Laria O, Ovruski SM (2020) Effects of exposure time and ratio of irradiated larvae from three medfly strains on progeny yield in Diachasmimorpha longicaudata (Hymenoptera: Braconidae) mass rearing. Biocontrol Sci Techn 30:592–602. https://doi.org/10.1080/09583157.2020.1749834
Conover WJ, Iman RL (1981) Rank transformation as a bridge between parametric and nonparametric statistics. J Am Stat Assoc 35:124–129. https://doi.org/10.1080/00031305.1981.10479327
de Pedro L, Tormos J, Harbi A, Ferrara F, Sabater-Muñoz B, Asís JD, Beitia F (2019) Combined use of the larvo-pupal parasitoids Diachasmimorpha longicaudata and Aganaspis daci for biological control of the medfly. Ann Appl Biol 174:40–50. https://doi.org/10.1111/aab.12468
Duan JJ, Messing RH (2000) Host specificity tests of Diachasmimorpha kraussii (Hymenoptera: Braconidae), a newly introduced opiine fruit fly parasitoid with four nontarget tephritids in Hawaii. Biol Control 19:28–34. https://doi.org/10.1006/bcon.2000.0842
Duyck PF, David P, Junod G, Brunel C, Dupont R, Quilici S (2006) Importance of competition mechanism in successive invasions by poliphagous Tephritidae in La Reunion. Ecology 87:1770–1780
Eben A, Benrey B, Sivinski J, Aluja M (2000) Host species and host plant effects on preference and performance of Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environ Entomol 29:87–94. https://doi.org/10.1603/0046-225x-29.1.87
Funes CF, Escobar LI, Meneguzzi NG, Ovruski SM, Kirschbaum DS (2017) Occurrence of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in organically grown Rubus spp. (Rosales: Rosaceae), in two very contrasting environments of northwestern Argentina. Fla Entomol 100:672–674. https://doi.org/10.1653/024.100.0330
Garcia FRM, Ovruski SM, Suárez L, Cancino J, Liburd OE (2020) Biological control of tephritid fruit flies in the Americas and Hawaii: a review of the use of parasitoids and predators. Insects 11:662. https://doi.org/10.3390/insects11100662
García-Medel D, Sivinski J, Díaz-Fleischer F, Ramirez-Romero R, Aluja M (2007) Foraging behavior by six fruit fly parasitoids (Hymenoptera: Braconidae) released as single- or multiple-species cohorts in field cages: influence of fruit location and host density. Biol Control 43:12–22. https://doi.org/10.1016/j.biocontrol.2007.06.008
Gonzalez P, Montoya P, Perez-Lachaud G, Cancino J, Liedo P (2010) Host discrimination and superparasitism in wild and mass-reared Diachasmimorpha longicaudata (Hym.: Braconidae) females. Biocontrol Sci Techn 20:137–148. https://doi.org/10.1080/09583150903437266
Harbi A, Beitia F, Ferrara F, Chermiti B, Sabater-Muñoz B (2018) Functional response of Diachasmimorpha longicaudata (Ashmead) over Ceratitis capitata (Wiedemann): influence of temperature, fruit location and host density. Crop Prot 109:115–122. https://doi.org/10.1016/j.cropro.2018.03.010
Hendrichs J, Kenmore P, Robinson AS, Vreysen MJB (2007) Area-wide integrated management (AW-IPM): principles, practice and prospects. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide Control of Insects Pests: From Research to Field Implementation. Springer, Dordrecht, The Netherlands, pp 3–33
Meirelles RN, Redaelli LR, Ourique CB (2013) Comparative biology of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) reared on Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae). Fla Entomol 96:412–418. https://doi.org/10.1653/024.096.0204
Meirelles RN, Redaelli LR, Ourique CB (2015) Thermal requirements and annual number of generations of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) reared in the South American Fruit Fly and the Mediterranean Fruit Fly (Diptera: Tephritidae). Fla Entomol 98:1223–1226. https://doi.org/10.1653/024.098.0432
Messing RH, Jang EB (1992) Response of the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to host-fruit stimuli. Environ Entomol 21:1189–1195. https://doi.org/10.1603/0046-225X-34.3.576
Messing RH, Klungness LM, Purcell MF, Wong TT (1993) Quality control parameters of reared Opiinae parasitoids used in augmentative biological control of tephritid fruit flies in Hawaii. Biol Control 3:140–147
Miranda M, Sivinski J, Rull J, Cicero L, Aluja M (2015) Niche breadth and interspecific competition between Doryctobracon crawfordi and Diachasmimorpha longicaudata (Hymenoptera: Braconidae), native and introduced parasitoids of Anastrepha spp. fruit flies (Diptera: Tephritidae). Biol Control 82:86–95. https://doi.org/10.1016/j.biocontrol.2014.12.008
Montoya P, Liedo P, Benrey B, Barrera JF, Cancino J, Aluja M (2000a) Functional response and superparasitism by Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Ann Entomol Soc Am 93:47–54. https://doi.org/10.1603/0013-8746(2000)093[0047:FRASBD]2.0.CO;2
Montoya P, Liedo P, Benrey B, Barrera JF, Cancino J, Sivinski J, Aluja M (2000b) Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biol Control 18:212–224. https://doi.org/10.1006/bcon.2000.0819
Montoya P, Cancino J, Zenil M, Santiago G, Gutierrez JM (2007) The augmentative biological control component in the Mexican national campaign against Anastrepha spp. fruit flies. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide Control of Insects Pests: From Research to Field Implementation. The Netherlands, Springer, Dordrecht, pp 661–670
Montoya P, Pérez-Lachaud G, Liedo L (2012a) Superparasitism in the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) and the implications for mass rearing and augmentative release. Insects 3:900–911. https://doi.org/10.3390/insects3040900
Montoya P, Cancino J, Ruiz L (2012b) Packing of fruit fly parasitoids for augmentative releases. Insects 3:889–899. https://doi.org/10.3390/insects3030889
Montoya P, Ruiz L, Pérez-Lachaud G, Cancino J, Liedo P (2013) Field superparasitism by Diachasmimorpha longicaudata attacking Anastrepha spp. larvae on mango fruits. Biol Control 64:160–165. https://doi.org/10.1016/j.biocontrol.2012.10.015
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 62:681–1593. https://doi.org/10.1007/s10526-017-9826-8
Núñez-Campero SR, Suárez L, Buonocore Biancheri MJ, Cancino J, Murúa F, Molina D, Laría O, Aluja M, Ovruski SM (2020) Host suitability and fitness-related parameters in Coptera haywardi (Hymenoptera: Diapriidae) reared on irradiated Ceratitis capitata (Diptera: Tephritidae) pupae stemming from the tsl Vienna-8 genetic sexing strain. J Econ Entomol 113:1666–1674. https://doi.org/10.1093/jee/toaa109
Oroño LE, Ovruski SM (2007) Presence of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) in a guild of parasitoids attacking Anastrepha fraterculus (Diptera: Tephritidae) in northwestern Argentina. Fla Entomol 90:410–412. https://doi.org/10.1653/0015-4040(2007)90[410:PODLHB]2.0.CO;2
Ovruski SM, Schliserman P (2012) Biological control of tephritid fruit flies in Argentina: historical review, current status, and future trends for developing a parasitoid mass-release program. Insects 3:870–888. https://doi.org/10.3390/insects3030870
Ovruski SM, Aluja M, Sivinski J, Wharton RA (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 Manag Rev 5:81–107. https://doi.org/10.1023/A:1009652431251
Ovruski SM, Schliserman P, Aluja M (2003) Native and introduced host plants of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in Northwestern Argentina. J Econ Entomol 96:1108–1118. https://doi.org/10.1093/jee/96.4.1108
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. https://doi.org/10.1016/S1049-9644(03)00127-0
Ovruski SM, van Nieuwenhove G, Bezdjian L, Schliserman P (2012) Evaluation of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) as a mortality factor of Ceratitis capitata (Diptera: Tephritidae) infesting Citrus species under laboratory and field-cage conditions. Biocontrol Sci Techn 22:187–202. https://doi.org/10.1080/09583157.2011.648167
Purcell MF (1998) Contribution of biological control to integrated pest management of tephritid fruit flies in the tropics and subtropics. Integrated Pest Manag Rev 3:63–83. https://doi.org/10.1023/A:1009647429498
Purcell MF, Jackson CG, Long JP, Batchlor MA (1994) Influence of guava ripening on parasitism levels of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), by Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) and other parasitoids. Biol Control 4:396–403. https://doi.org/10.1006/bcon.1994.1050
Rosenheim JA, Hoy MA (1989) Confidence intervals for the Abbott’s formula correction of bioassay data for control response. J Econ Entomol 82:331–335. https://doi.org/10.1093/jee/82.2.331
Sánchez G, Murúa F, Suárez L, Van Nieuwenhove G, Taret G, Pantano V, Ovruski SM (2016) Augmentative releases of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) for Ceratitis capitata (Diptera: Tephritidae) control in a fruit-growing region of Argentina. Biol Control 103:101–107. https://doi.org/10.1016/j.biocontrol.2016.08.002
Schliserman P, Ovruski SM, DeColl OR (2003) The recovery and permanent establishment of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) in Misiones, northeastern Argentina. Fla Entomol 86:491–492. https://doi.org/10.1653/0015-4040(2003)086[0491:TEODLH]2.0.CO;2
Schliserman P, Aluja M, Rull J, 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. Biol Invasions 16:2599–2613. https://doi.org/10.1007/s10530-014-0690-5
Schliserman P, Aluja M, Rull J, Ovruski SM (2016) Temporal diversity and abundance patterns of parasitoids of fruit-infesting Tephritidae (Diptera) in the Argentinean Yungas: implications for biological control. Environ Entomol 45:1184–1198. https://doi.org/10.1093/ee/nvw077
Segura DF, Viscarret MM, Ovruski SM, Cladera JL (2012) Response of the fruit fly parasitoid Diachasmimorpha longicaudata to host and host-habitat volatile cues. Entomol Exp Appl 143:164–176. https://doi.org/10.1111/j.1570-7458.2012.01246.x
SENASA (2017) Moscas de los Frutos. http://www.senasa.gob.ar/cadena-vegetal/frutales/produccion-primaria/programas-fitosanitarios/mosca-de-los-frutos-0 (Access on July 28, 2021)
Silva RAD, Nascimento DBD, Deus EDGD, Souza GDD, Oliveira LPSD (2007) Host and parasitoids of Anastrepha spp. (Diptera: Tephritidae) in Itaubal do Piririm, Amapá State. Brazil Ciência Rural 37:557–560. https://doi.org/10.1590/S0103-84782007000200041
StatSoft, Inc. 2011. STATISTICA (data analysis software system), version 10.0. www.statsoft.com.
Stuhl C, Sivinski J, Teal P, Paranhos B, Aluja M (2011) A compound produced by fruigivorous Tephritidae (Diptera) larvae promotes oviposition behavior by the biological control agent Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environ Entomol 40:727–736. https://doi.org/10.1603/EN10198
Suárez L, Murúa F, Lara N, Escobar J, Taret G, Rubio J, van Nieuwenhove G, Bezdjian L, Schliserman P, Ovruski SM (2014) Biological control of Ceratitis capitata (Diptera: Tephritidae) in Argentina: releases of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) in fruit-producing semi-arid areas of San Juan. Nat Sci 6:664–675. https://doi.org/10.4236/ns.2014.69066
Suárez L, Buonocore Biancheri MJ, Murúa F, Bilbao M, García M, Cancino J, Martín O, Molina D, Laría O, Ovruski SM (2019a) Effects of host age and radiation dose in Diachasmimorpha longicaudata (Hymenoptera: Braconidae) mass-reared on Medfly larvae of the tsl Vienna 8 genetic sexing strain. Biol Control 130:51–59. https://doi.org/10.1016/j.biocontrol.2018.12.013
Suárez L, Buonocore Biancheri MJ, Sánchez G, Murúa F, Funes CF, Kirschbaum DS, Molina D, Laría O, Ovruski SM (2019b) Effects of releasing two Diachasmimorpha longicaudata population lines for the control of Ceratitis capitata infesting three key host fruit species. Biol Control 133:58–65. https://doi.org/10.1016/j.biocontrol.2019.03.011
Suárez L, Buonocore Biancheri MJ, 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 113:1134–1144. https://doi.org/10.1093/jee/toaa062
Acknowledgements
We thank to Patricia Colombres and Guillermo Borchia (PROIMI-CONICET) for the technical assistance. Special thanks are for the biological material provided by the “BioPlanta San Juan” mass-rearing facility belonging to the San Juan Biotechnology Center of the Dirección de Sanidad Vegetal, Animal y Alimentos, San Juan, Argentina. The Consejo Nacional de Investigaciones Científicas y Técnicas de la República Argentina (CONICET-Argentina) is also thanked for awarding a Ph. D. research scholarship to María Josefina Buonocore Biancheri.
Funding
Financial support was provided by Fondo Nacional de Ciencia y Tecnología-Agencia Nacional de Promoción Científica y Tecnológica (FONCyT-ANPCyT, Argentina) through grant PICT-2013–0604.
Author information
Authors and Affiliations
Contributions
MJBB, LCS, DSK, and SMO conceived the research and wrote the manuscript. MJBB and SMO conducted experiments. MJBB, LCS, and SMO analyzed data and conducted statistical analyses. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Edited by German Vargas
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Buonocore Biancheri, M.J., Suárez, L.d.C., Kirschbaum, D.S. et al. Augmentative Releases of Two Diachasmimorpha longicaudata (Hymenoptera: Braconidae) Population Lines Under Field-Cage Conditions to Control Ceratitis capitata (Diptera: Tephritidae). Neotrop Entomol 52, 212–226 (2023). https://doi.org/10.1007/s13744-022-00981-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-022-00981-8