, Volume 60, Issue 3, pp 317–330 | Cite as

Classic biological control of olive fruit fly in California, USA: release and recovery of introduced parasitoids

  • Kent M. DaaneEmail author
  • Xingeng Wang
  • Diego J. Nieto
  • Charles H. Pickett
  • Kim A. Hoelmer
  • Arnaud Blanchet
  • Marshall W. Johnson


The establishment of olive fruit fly Bactrocera oleae (Rossi) in California, USA instigated a classical biological program. This study reports the release and recovery of two solitary larval endoparasitoids, Psyttalia humilis Silvestri and Psyttalia lounsburyi (Silvestri) imported from sub-Saharan Africa, and released in five coastal and three inland counties in California, USA. Both parasitoid species were recovered post-release within the same fruit season and dispersed up to 1,500 m from a release location. P. lounsburyi was recovered post-release the following fruit seasons at numerous sites, and up to 945 days after the last release at one site. It is now established in California coastal regions, but not at the inland release sites. We discuss ecological factors and aspects of parasitoid biology that could improve or impede the permanent establishment of olive fruit fly parasitoids in California.


Bactrocera oleae Psyttalia Pteromalus Biological control Climatic adaptability Host specificity 



We thank Monica Cooper, John Hutchins, Karmit Levy, Emily Kuhn, Mathew Middleton, Karen Sime, and Kevin Welzel (University of California, Berkeley, USA), Martha Gerik (University of California, Riverside, USA) for assistance; David Headrick, Pete Peterson, and Therese Kapaun (California Polytechnic State University, San Luis Obispo, USA) for facilitating field study and help; Scott Ritterbuck, Walt French, Anne May and David Righetti for using their olive trees; Walker Jones (USDA-ARS European Biological Control Laboratory, Montferrier, France), and Pedro Rendon (USDA-APHIS-PPQ Parasitoid Rearing Facility, Guatemala) for providing parasitoids; and Victoria Yokoyama (USDA-ARS, Parlier, California, USA) for useful discussions on field release. Funds were provided by the California Specialty Crop Block Grant, California Olive Committee, USDA APHIS, CDFA Biological Control Program, USDA-CSREES Special Grants Program: Pest Management Alternatives, and the Cañada College Trustees Fund.


  1. Burrack HJ, Connell JH, Zalom FG (2008) Comparison of olive fruit fly (Bactrocera oleae (Gmelin)) (Diptera: Tephritidae) captures in several commercial traps in California. Int J Pest Manag 54:227–234CrossRefGoogle Scholar
  2. Copeland RS, White IM, Okumu M, Machera P, Wharton RA (2004) Insects associated with fruits of the Oleaceae (Asteridae, Lamiales) in Kenya, with special reference to the Tephritidae (Diptera). Bish Mus Bull Entomol 12:135–164Google Scholar
  3. Daane KM, Johnson MW (2010) Olive fruit fly: managing an ancient pest in modern times. Annu Rev Entomol 55:155–169CrossRefGoogle Scholar
  4. Daane KM, Sime KR, Wang XG, Nadel H, Johnson MW, Walton VM (2008) Psyttalia lounsburyi (Hymenoptera: Braconidae), potential biological control agent for the olive fruit fly in California. Biol Control 44:78–89CrossRefGoogle Scholar
  5. Daane KM, Johnson MW, Pickett CH, Sime KR, Wang XG, Nadel H, Andrews JW, Hoelmer KA (2011) Biological controls investigated to aid management of the olive fruit fly in California. Calif Agric 65:21–28CrossRefGoogle Scholar
  6. Daane KM, Wang XG, Johnson MW, Cooper ML (2012) Low temperature storage effects on two olive fruit fly parasitoids. BioControl 58:175–185CrossRefGoogle Scholar
  7. DeBach P, Rosen D (1991) Biological control by natural enemies. Cambridge University Press, Cambridge, UKGoogle Scholar
  8. El-Heneidy AH, Omar AH, El-Sherif H, El-Khawas MA (2001) Survey and seasonal abundance of the parasitoids of the olive fruit fly, Bactrocera (Dacus) oleae Gmel. (Diptera: Trypetidae) in Egypt. Arab J Plant Prot 19:80–85Google Scholar
  9. Hoelmer KA, Kirk AA, Pickett CH, Daane KM, Johnson MW (2011) Prospects for improving biological control of olive fruit fly, Bactrocera oleae (Diptera: Tephritidae), with introduced parasitoids (Hymenoptera). Biocontrol Sci Technol 21:1005–1025CrossRefGoogle Scholar
  10. Hoffmann MP, Ode PR, Walker DL, Gardner J, van Nouhuys S, Shelton AM (2001) Performance of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) reared on factitious host, including the target host Ostrinia nubilalis. Biol Control 21:1–10CrossRefGoogle Scholar
  11. Johnson MW, Wang XG, Nadel H, Opp SB, Patterson KL, Stewart-Leslie J, Daane KM (2011) High temperature affects olive fruit fly populations in California’s Central Valley. Calif Agric 65:29–33CrossRefGoogle Scholar
  12. Kakani EG, Zygouridis NE, Tsoumani KT, Seraphides N, Zalom FG, Mathiopoulos KD (2010) Spinosad resistance development in wild olive fruit fly Bactrocera oleae (Diptera: Tephritidae) populations in California. Pest Manag Sci 66:447–453PubMedGoogle Scholar
  13. Kapaun T, Nadel H, Headrick D, Vredevoe L (2010) Biology and parasitism rates of Pteromalus nr. myopitae (Hymenoptera: Pteromalidae), a newly discovered parasitoid of olive fruit fly Bactrocera oleae (Diptera: Tephritidae) in coastal California. Biol Control 53:76–85CrossRefGoogle Scholar
  14. Loni A (1997) Developmental rate of Opius concolor (Hym.: Braconidae) at various constant temperatures. Entomophaga 42:359–366CrossRefGoogle Scholar
  15. Miranda MA, Miquel M, Terrassa J, Melis N, Monerris M (2008) Parasitism of Bactrocera oleae (Diptera, Tephritidae) by Psyttalia concolor (Hymenoptera, Braconidae) in the Balearic Islands (Spain). J Appl Entomol 132:798–805CrossRefGoogle Scholar
  16. Nadel H, Daane KM, Hoelmer KA, Pickett CH, Johnson MW (2009) Non-target host risk assessment of the idiobiont parasitoid, Bracon celer (Hymenoptera: Braconidae), for biological control of olive fruit fly in California. Biocontrol Sci Technol 19:701–715CrossRefGoogle Scholar
  17. Nardi F, Carapelli A, Boore JL, Roderick GK, Dallai R, Frati F (2010) Domestication of olive fly through a multi-regional host shift to cultivated olives: comparative dating using complete mitochondrial genomes. Mol Phylogenet Evol 57:678–686CrossRefPubMedGoogle Scholar
  18. Neuenschwander P (1982) Searching for parasitoids of Dacus oleae (Gmel) (Dipt., Tephritidae) in South Africa. J Appl Entomol 94:509–522Google Scholar
  19. Neuenschwander P, Bigler F, Delucchi V, Michelakis S (1983) Natural enemies of preimaginal stages of Dacus oleae Gmel. (Dipt., Tephritidae) in Western Crete. I. Bionomics and phonologies. Boll Lab Entomol Agrar “Filippo Silvestri” 40:3–32Google Scholar
  20. Orsini MA, Daane KM, Sime KR, Nelson EH (2007) Mortality of olive fruit fly pupae in California. Biocontrol Sci Technol 17:797–807CrossRefGoogle Scholar
  21. Raspi A, Loni A (1994) Alcune note sull’allevamento massale di Opius concolor Szépligeti (Hym.: Braconidae) e su recenti tentative d’introduzione della specie in Toscana e Liguria. Frustula Entomol 30:135–145Google Scholar
  22. Rehman JU, Wang XG, Johnson MW, Daane KM, Jilan G, Khan MA, Zalom FG (2009) Effects of Peganum harmala (Zygophyllaceae) seed extracts on the olive fruit fly (Diptera: Tephritidae) and its larval parasitoid, Psyttalia concolor (Hymenoptera: Braconidae). J Econ Entomol 102:2233–2240CrossRefPubMedGoogle Scholar
  23. Rugman-Jones PF, Wharton R, van Noort T, Stouthamer R (2009) Molecular differentiation of the Psyttalia concolor (Szepligeti) species complex (Hymenoptera: Braconidae) associated with olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), in Africa. Biol Control 49:17–26CrossRefGoogle Scholar
  24. Silvestri F (1914) Report on an expedition to Africa in search of natural enemies of fruit flies (Trupaneidae) with descriptions, observations and biological notes. Hawaii Board Agric For Div Entomol Bull 3:1–146Google Scholar
  25. Sime KR, Daane KM, Messing RH, Johnson MW (2006a) Comparison of two laboratory cultures of Psyttalia concolor (Hymenoptera: Braconidae), as a parasitoid of the olive fruit fly. Biol Control 39:248–255CrossRefGoogle Scholar
  26. Sime KR, Daane KM, Andrews JW, Hoelmer KA, Pickett CH, Nadel H, Johnson MW, Messing RH (2006b) The biology of Bracon celer as a parasitoid of the olive fruit fly. BioControl 51:553–567CrossRefGoogle Scholar
  27. Sime KR, Daane KM, Nadel H, Funk CS, Messing RH, Andrews JW, Johnson MW, Pickett CH (2006c) Diachasmimorpha longicaudata and D. kraussii (Hymenoptera: Braconidae), potential parasitoids of the olive fruit fly. Biocontrol Sci Technol 16:169–179CrossRefGoogle Scholar
  28. Sime KR, Daane KM, Kirk AA, Andrews JW, Johnson MW, Messing RH (2007) Psyttalia ponerophaga (Hymenoptera: Braconidae) as a potential biological control agent of olive fruit fly Bactrocera oleae (Diptera: Tephritidae) in California. Bull Entomol Res 97:233–242CrossRefPubMedGoogle Scholar
  29. 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 For Entomol 10:423–431CrossRefGoogle Scholar
  30. Wang XG, Keller MA (2002) A comparison of host-searching efficiency of the two larval parasitoids of Plutella xylostella. Ecol Entomol 27:105–114CrossRefGoogle Scholar
  31. Wang XG, Johnson MW, Daane KM, Nadel H (2009a) High summer temperatures affect survival and reproduction of olive fruit fly (Diptera: Tephritidae). Environ Entomol 38:1496–1504CrossRefPubMedGoogle Scholar
  32. Wang XG, Johnson MW, Daane KM, Opp SB (2009b) Combined effects of heat stress and food supply on flight performance of olive fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 102:727–734CrossRefGoogle Scholar
  33. Wang XG, Johnson MW, Daane KM, Yokoyama VY (2009c) Larger olive fruit size reduces the efficiency of Psyttalia concolor, as a parasitoid of the olive fruit fly. Biol Control 49:45–51CrossRefGoogle Scholar
  34. Wang XG, Nadel H, Johnson MW, Daane KM, Hoelmer K, Walton VM, Pickett CH, Sime KR (2009d) Crop domestication relaxes both top-down and bottom-up effects on a specialist herbivore. Basic Appl Ecol 10:216–227CrossRefGoogle Scholar
  35. Wang XG, Johnson MW, Yokoyama VY, Pickett CH, Daane KM (2011) Comparative evaluation of two olive fruit fly parasitoids under varying abiotic conditions. BioControl 56:283–293CrossRefGoogle Scholar
  36. Wang XG, Levy K, Son Y, Johnson MW, Daane KM (2012) Comparison of thermal performances between a population of olive fruit fly and its co-adapted parasitoids. Biol Control 60:247–254CrossRefGoogle Scholar
  37. Wang XG, Levy K, Nadel H, Johnson MW, Blanchet A, Argov Y, Pickett CH, Daane KM (2013) Overwintering survival of olive fruit fly and two introduced parasitoids in California. Environ Entomol 42:467–476CrossRefPubMedGoogle Scholar
  38. Wharton RA, Trostle MK, Messing RH, Copeland RS, Kimani-Njogu SW, Lux S, Overholt WA, Mohamed S, Sivinski J (2000) Parasitoids of medfly, Ceratitis capitata, and related tephritids in Kenyan coffee: a predominantly koinobiont assemblage. Bull Entomol Res 90:517–526CrossRefPubMedGoogle Scholar
  39. Yokoyama VY, Rendόn PA, Sivinski J (2008) Psyttalia cf. concolor (Hymenoptera: Braconidae) for biological control of olive fruit fly (Diptera: Tephritidae) in California. Environ Entomol 37:764–773CrossRefPubMedGoogle Scholar
  40. Yokoyama VY, Cáceres CE, Kuenen LPS, Wang XG, Rendόn PA, Johnson MW, Daane KM (2010) Field performance and fitness of an olive fruit fly parasitoid, Psyttalia humilis (Hymenoptera: Braconidae), mass reared on irradiated Medfly. Biol Control 54:90–99CrossRefGoogle Scholar
  41. Yokoyama VY, Rendón PA, Wang XG, Opp SB, Johnson MW, Daane KM (2011) Response of Psyttalia humilis (Hymenoptera: Braconidae) to olive fruit fly (Diptera: Tephritidae) and conditions in California olive orchards. Environ Entomol 40:315–323CrossRefGoogle Scholar
  42. Yokoyama VY, Wang XG, Aldana A, Cáceres CE, Rendón PA, Johnson MW, Daane KM (2012) Performance of Psyttalia humilis (Hymenoptera: Braconidae) reared from irradiated host on olive fruit fly (Diptera: Tephritidae) in California. Environ Entomol 41:497–507CrossRefPubMedGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2015

Authors and Affiliations

  • Kent M. Daane
    • 1
    Email author
  • Xingeng Wang
    • 1
  • Diego J. Nieto
    • 2
  • Charles H. Pickett
    • 3
  • Kim A. Hoelmer
    • 4
  • Arnaud Blanchet
    • 4
  • Marshall W. Johnson
    • 5
  1. 1.Department of Environmental Science, Policy and ManagementUniversity of CaliforniaBerkeleyUSA
  2. 2.Department of Biological SciencesCañada CollegeRedwood CityUSA
  3. 3.California Department of Food and AgricultureSacramentoUSA
  4. 4.European Biological Control LaboratoryUSDA-ARSMontferrierFrance
  5. 5.Department of EntomologyUniversity of CaliforniaRiversideUSA

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