Medfly Population Suppression through Augmentative Release of an Introduced Parasitoid in an Irrigated Multi-Fruit Orchard of Central–Western Argentina

Simple Summary Ceratitis capitata, commonly known as the Mediterranean fruit fly or medfly, is one of the most damaging invasive insect pests for fruit production and trade worldwide. Augmentative biological control (ABC) using parasitoids, insects whose larvae develop as parasites that eventually kill their hosts, is an eco-friendly strategy for medfly suppression and is used in several countries. This strategy relies on periodic releases of large numbers of mass reared parasitoids in an area where naturally occurring parasitoids are too few to control the target pest. ABC has been incorporated for 10 years into medfly suppression strategies in the irrigated fruit production valleys of San Juan province, northwestern Argentina, by the San Juan Fruit Fly Control and Eradication Program. In this study, we report the results of mass releases of the Southeast Asia-native parasitoid Diachasmimorpha longicaudata in a fruit farm from early summer (December) to mid-autumn (May) over two successive years. The effect of the released parasitoids on the suppression of the medfly population was evaluated based on captures of adult flies in food-baited traps, and the resultant levels of parasitism of fly larvae were assessed based on adult flies in sentinel fruit traps. Our results showed a substantial decrease in the medfly population on the parasitoid release farm. Therefore, ABC can be an effective tool for medfly control in San Juan. Abstract Biological control through the augmentative release of parasitoids is an important complementary tool that may be incorporated into other strategies for the eradication/eco-friendly control of pest fruit flies. However, not much information is available on the effectiveness of fruit fly parasitoids as biocontrol agents in semi-arid and temperate fruit-growing regions. Therefore, this study evaluated the effect of augmentative releases of the larval parasitoid Diachasmimorpha longicaudata (Ashmead) on Ceratitis capitata (Wiedemann) (medfly) populations over two fruit seasons (2013 and 2014) on a 10 ha irrigated fruit farm in San Juan province, central–western Argentina. The parasitoids were mass reared on irradiated medfly larvae of the Vienna-8 temperature-sensitive lethal genetic sexing strain. About 1692 (±108) parasitoids/ha were released per each of the 13 periods throughout each fruit season. Another similar farm was chosen as a control of non-parasitoid release. The numbers of captured adult flies in food-baited traps and of recovered fly puparia from sentinel fruits were considered the main variables to analyze the effect of parasitoid release on fly population suppression using a generalized least squares model. The results showed a significant decrease (p < 0.05) in the medfly population on the parasitoid release farm when compared to the Control farm, demonstrating the effectiveness of augmentative biological control using this exotic parasitoid. Thus, D. longicaudata could be used in combination with other medfly suppression strategies in the fruit production valleys of San Juan.

[1]  S. Steinmöller,et al.  Origin and potential for overwintering of Ceratitis capitata (Wiedemann) captured in an official survey in Germany , 2022, Journal of Plant Diseases and Protection.

[2]  A. R. Abot,et al.  Sequential sampling plan for Ceratitis capitata (Diptera: Tephritidae) in guava orchards. , 2022, Anais da Academia Brasileira de Ciencias.

[3]  A. R. Abot,et al.  Spatial distribution of Ceratitis capitata in guava orchards and influences from orchard management. , 2022, Brazilian journal of biology = Revista brasleira de biologia.

[4]  J. Rull,et al.  Dynamic seasonal response of Ceratitis capitata (Diptera: Tephritidae) to fruit juice-based lures in fig orchards , 2021 .

[5]  J. Cancino,et al.  Biological Control of Tephritid Fruit Flies in the Americas and Hawaii: A Review of the Use of Parasitoids and Predators , 2020, Insects.

[6]  P. Liedo,et al.  Suppression of Ceratitis capitata (Wied.) (Diptera: Tephritidae) populations in coffee in the Mexico–Guatemala border region through the augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) , 2019, Biocontrol Science and Technology.

[7]  J. Cancino,et al.  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 , 2019, Biological Control.

[8]  B. Sabater-Muñoz,et al.  Combined use of the larvo‐pupal parasitoids Diachasmimorpha longicaudata and Aganaspis daci for biological control of the medfly , 2018, Annals of Applied Biology.

[9]  A. Urbaneja,et al.  Biological control using invertebrates and microorganisms: plenty of new opportunities , 2018, BioControl.

[10]  D. Kirschbaum,et al.  Occurrence of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in Organically Grown Rubus (Rosales: Rosaceae), in Two Contrasting Environments of Northwestern Argentina , 2017, Florida Entomologist.

[11]  P. Liedo,et al.  Effect of Diachasmimorpha longicaudata releases on the native parasitoid guild attacking Anastrepha spp. larvae in disturbed zones of Chiapas, Mexico , 2017, BioControl.

[12]  L. Suárez,et al.  Augmentative releases of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) for Ceratitis capitata (Diptera: Tephritidae) control in a fruit-growing region of Argentina , 2016 .

[13]  P. Liedo,et al.  Area Freedom in Mexico from Mediterranean Fruit Fly (Diptera: Tephritidae): A Review of Over 30 Years of a Successful Containment Program Using an Integrated Area-Wide SIT Approach , 2015 .

[14]  J. Rubio,et al.  Biological Control of Ceratitis capitata (Diptera: Tephritidae) in Argentina: Releases of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) in Fruit-Producing Semi-Arid Areas of San Juan , 2014 .

[15]  M. Aluja,et al.  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 , 2014, Biological Invasions.

[16]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[17]  Tomasz Burzykowski,et al.  Linear Mixed-Effects Models Using R: A Step-by-Step Approach , 2013 .

[18]  Andrzej T. Galecki,et al.  Linear mixed-effects models using R , 2013 .

[19]  J. Sivinski.  Augmentative biological control: research and methods to help make it work , 2013 .

[20]  F. Garcia,et al.  Augmentative Biological Control Using Parasitoids for Fruit Fly Management in Brazil , 2012, Insects.

[21]  P. Liedo,et al.  Superparasitism in the Fruit Fly Parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) and the Implications for Mass Rearing and Augmentative Release , 2012, Insects.

[22]  R. Vargas,et al.  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 , 2012, Insects.

[23]  J. V. Lenteren,et al.  The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake , 2012, BioControl.

[24]  Chris Nakas,et al.  Population-specific demography and invasion potential in medfly , 2011, Ecology and evolution.

[25]  J. Terblanche,et al.  Thermal variability alters climatic stress resistance and plastic responses in a globally invasive pest, the Mediterranean fruit fly (Ceratitis capitata) , 2010 .

[26]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

[27]  J. Terblanche,et al.  Thermal tolerance in adult Mediterranean and Natal fruit flies (Ceratitis capitata and Ceratitis rosa): Effects of age, gender and feeding status , 2009 .

[28]  A. Zuur,et al.  Mixed Effects Models and Extensions in Ecology with R , 2009 .

[29]  D. Guillén,et al.  Expansion of the National Fruit Fly Control Programme in Argentina , 2007 .

[30]  J. Cancino,et al.  The Augmentative Biological Control Component in the Mexican National Campaign Against Anastrepha spp. Fruit Flies , 2007 .

[31]  Jorge Hendrichs,et al.  Area-Wide Control of Insect Pests , 2007 .

[32]  J. Sivinski,et al.  The effects of sterile males and two braconid parasitoids, Fopius arisanus (Sonan) and Diachasmimorpha krausii (Fullaway) (Hymenoptera), on caged populations of Mediterranean fruit flies, Ceratitis capitata (Wied.) (Diptera: Tephritidae) at various sites in Guatemala. , 2006 .

[33]  J. Cancino,et al.  PARASITOID RELEASES IN THE CONTROL OF CERATITIS CAPITATA (DIPTERA: TEPHRITIDAE) OUTBREAKS, IN COFFEE GROWING ZONES OF CHIAPAS, MEXICO , 2005 .

[34]  R. Messing,et al.  Potential Interactions Between Pupal and Egg- or Larval-Pupal Parasitoids of Tephritid Fruit Flies , 2004 .

[35]  C. Cáceres.  Mass Rearing of Temperature Sensitive Genetic Sexing Strains in the Mediterranean Fruit Fly (Ceratitis Capitata) , 2002, Genetica.

[36]  M. Aluja,et al.  Native and Introduced Host Plants of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in Northwestern Argentina , 2003 .

[37]  R. Copeland,et al.  Indigenous Hosts of Ceratitis capitata (Diptera:Tephritidae) in Kenya , 2002 .

[38]  V. Carey,et al.  Mixed-Effects Models in S and S-Plus , 2001 .

[39]  S. Peck,et al.  Potential for Areawide Integrated Management of Mediterranean Fruit Fly (Diptera: Tephritidae) with a Braconid Parasitoid and a Novel Bait Spray , 2001, Journal of economic entomology.

[40]  J. Sivinski,et al.  Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). , 2000 .

[41]  J. Sivinski,et al.  Development of Aerial Releases of Diachasmimorpha tryoni (Cameron) (Hymenoptera: Braconidae), a Parasitoid that Attacks the Mediterranean Fruit Fly, Ceratitis capitata (Weidemann) (Diptera: Tephritidae), in the Guatemalan Highlands , 2000 .

[42]  J. Sivinski,et al.  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 , 2000 .

[43]  Douglas M. Bates,et al.  LINEAR AND NONLINEAR MIXED-EFFECTS MODELS , 1998 .

[44]  R. E. Burns,et al.  Inundative Release of the Parasitoid Diachasmimorpha longicaudata for the Control of the Caribbean Fruit Fly, Anastrepha suspensa , 1996 .

[45]  J. Sivinski,et al.  Suppression of a Caribbean Fruit Fly (Anastrepha suspensa(Loew) Diptera: Tephritidae) Population through Augmented Releases of the ParasitoidDiachasmimorpha longicaudata(Ashmead) (Hymenoptera: Braconidae) , 1996 .

[46]  R. Causse,et al.  Mediterranean fruit fly Ceratitis capitata Wiedemann (Dipt., Trypetidae) back in Southern France , 1993 .

[47]  J. Herr,et al.  Augmentative releases of Diachasmimorpha tryoni (Hymenoptera: Braconidae) to suppress a mediterranean fruit fly (Diptera: Tephritidae) population in Kula, Maui, Hawaii , 1991 .