Source: UNIV OF HAWAII submitted to
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
Funding Source
Reporting Frequency
Accession No.
Grant No.
Project No.
Proposal No.
Multistate No.
Program Code
Project Start Date
Aug 15, 2005
Project End Date
Aug 14, 2008
Grant Year
Project Director
Messing, R. H.
Recipient Organization
Performing Department
Non Technical Summary
Four invasive tephritid fruit fly species (Bactrocera cucurbitae, B. dorsalis, B. latifrons and Ceratitis capitata) are serious pests of many horticultural crops in Hawaii and other tropical regions. Successful introduction and establishment of several parasitoids in the past has resulted in significant suppression of C. capitata and B. dorsalis. However, the other two fly pests, particularly B. cucurbitae, continue to cause severe economic damage, in large part due to a lack of effective natural enemies. Current control methods mainly rely on chemical insecticides or the application of toxic baits that may disrupt or destroy the local biodiversity that sustains and regulates agro-ecosystems. This project aims to enhance fruit fly biological control through the introduction and evaluation of safe and effective new parasitoid species. We will determine their target host range, evaluate their effectiveness against four pest fruit fly species, address their potential impact on non-target flies, and determine their competitiveness against extant parasitoids in quarantine. Our goal is to discover and introduce effective parasitoids for sustainable suppression, particularly against B. cucurbitae, which will ultimately increase economic benefits to growers through expanded opportunities in diversified agriculture in Hawaii.
Animal Health Component
Research Effort Categories

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
Goals / Objectives
(1) To search for and import fruit fly parasitoids new to Hawaii, especially (but not exclusively) from West Africa and Pacific islands (such as D. hageni from the Northern Mariannas), and from cooperators in California (Bracon celer, Fopius dacicida, Psyttalia lounsburyi, and Utetes africanus). (2) To determine the bionomics and the host range of newly imported parasitoids in Hawaii, with reference to both target and non-target species. (3) To determine which new species are safe to release in Hawaiian ecosystems, and conduct all work necessary to have these species placed on the appropriate Hawaii Dept. of Agriculture lists and to obtain State and Federal permits required for field release. (4) To make field pre-releases of already approved parasitoids (e.g. F. ceratitivorus that is currently under review in quarantine), and to continue evaluating the field efficacy of D. kraussii in suppression of medfly and B. latifrons.
Project Methods
(1) We will travel to West Africa to conduct field exploration, rearing, colony establishment, and establish shipping procedures for parasitoid material to Hawaii. Laboratories at the International Institute of Tropical Agriculture in Benin will serve as a base of operations. We will also travel to Saipan and Guam to explore for and collect Diachasmimorpha hageni, particularly targeting the melon fly. In addition, we will obtain the new parasitoid species currently in rearing at the quarantine facilities of University of California at Berkeley. (2) We will conduct behavioral bioassays on parasitization and foraging effectiveness of newly imported parasitoids, test their competitive interactions with extant parasitoids, and evaluate their non-target impact in the Hawaii Department of Agriculture Quarantine Facility in Honolulu. Promising new parasitoid species that have minimal risk of non-target impacts will then be highlighted to obtain release permits for further field cage pre-release tests. (3) Once release permits are granted for two previously imported parasitoids from east Africa (Fopius ceratitivorus and F. caudatus) (currently in review), we will conduct pre-release evaluation of these two parasitoids. Meanwhile, we will continue field release trials of Diachasmimorpha kraussii against medfly and B. latiforns in Maui.

Progress 08/15/05 to 08/14/08

OUTPUTS: A series of experiments conducted in quarantine indicated that Fopius ceratitivorus from Eastern Africa is an environmentally safe and potentially effective biological control agent of the Mediterranean fruit fly, Ceratitis capitata. The parasitoid did not have any negative impacts on non-target flies (including gall formers and flowerhead feeders) and did not even parasitize the other three (fruit infesting) pest species that occur in the islands. A general principle that may be responsible in some situations for mediating non-target impacts of introduced parasitoids was elucidated: competitor-free-space (or enemy-free-space) was shown to influence the adaption of new hosts by an introduced species Results of this research indicating environmental safety were collated into a formal Environmental Assessment and submitted to the state Office of Environmental Quality Control. Additional dossiers were submitted to the Hawaii Dept. of Agriculture requesting field release permits. PARTICIPANTS: Drs. Xingeng Wang and Aime Bokonon-Ganta contributed extensively to the quarantine rearing and experimental testing of the new parasitoids. Dr. Stefan Kroder gained new knowledge in the environmental adaptations of the new parasitoids and how this may influence geographic distribution and competitive interactions among species. All three of these post-docs gained advanced research training. TARGET AUDIENCES: Since the medfly attacks hundreds of different species of horticultural commodities, almost all farmers who grow fruits and vegetables in Hawaii can benefit by improved biological control of this invasive pest. PROJECT MODIFICATIONS: Not relevant to this project.

We have learned that certain ecological situations (intra-guild competition) can lead to non-target impacts- this may help to guide our risk analysis for biocontrol in the future. We have further refined our techniques for rearing and non-target testing in quarantine - knowledge that can be used with other imported fruit fly parasitoids.


  • Wang, X. G., A. H. Bokonon-Ganta & R. H. Messing. 2008. Intrinsic inter-specific competition in a guild of tephritid fruit fly parasitoids: effect of co-evolutionary history on competitive superiority. Biological Control 44: 312 to 320.
  • Wang, X. G & R. H. Messing. 2008. Role of egg-laying experience in avoidance of superparasitism by the fruit fly parasitoid Fopius arisanus. Annals of the Entomological Society of America 101: 656-663.
  • Bokonon-Ganta, A. H. & R. H. Messing. 2008. Response of the egg-larval parasitoid, Fopius ceratitivorus Wharton (Hymenoptera: Braconidae) to the Gall-Forming Tephritid Fly, Eutreta xanthochaeta (Diptera: Tephritidae). Proc. Haw. Entomol. Soc. 40.
  • Messing, R. H. & X. G. Wang. 2009. Competitor-free space mediates non-target impact of an introduced biological control agent. Ecological Entomology 34: 107 to 113.

Progress 08/15/06 to 08/14/07

OUTPUTS: Colonies of two newly introduced African parasitoids of tephritid fruit flies (Fopius caudatus and F. ceratitivorus) were strengthened in quarantine rearing cages for studies relating to their potential release into Hawaii's farms for biological control. Experiments were conducted on the host range and bionomic features of both species. Experiments were conducted to compare the temperature tolerances and parasitic efficiency of one previously established species (Fopius arisanus) and one newly introduced species (F. ceratitivorus) of parasitoids that attack and kill eggs of the Mediterranean fruit fly, Ceratitis capitata. Efficiency of parasitism, developmental rates, and sex ratios of the parasitoids were determined over a range of temperatures in the laboratory that correspond with the wide thermal ambient range experienced by medfly populations in the field in Hawaii. The results of a series of experiments regarding the environmental safety of F. ceratitivorus were disseminated to the appropriate State and Federal regulatory authorities in an attempt to get approval for releasing these natural enemies in the field. State authorities further disseminated the dossier to individuals on the Entomology sub-committee and the Plants and Animals Advisory Committee for environmental risk analysis review. PARTICIPANTS: Dr. Aime Bokonon-Ganta, former post-doc at the University of Hawaii at Manoa, conducted experiments on the host range and bionomics of F. ceratitivorus. Dr. Stefan Kroder, current post-doc at the University of Hawaii at Manoa, conducted experiments on the comparative temperature tolerances of several parasitoid species, and the competitive interactions among these species. TARGET AUDIENCES: Target audiences include all farmers that raise crops impacted by the medfly. Since this pest is known to attack over 300 species of plants, the targets include a wide range of farmers of almost all fruit and vegetable species. PROJECT MODIFICATIONS: Our progress has been delayed by complicated bureaucratic obstacles that interfere with the timely issuance of release permits for newly imported biocontrol agents, as well as by the crowded conditions in the State Quarantine Facility that restrict us to working with no more that two new species at any one time.

Through a long series of analyses, we have learned that the newly introduced egg-parasitoid Fopius ceratitivorus from Kenya is extremely unlikely to have any negative environmental impacts if released into the field in Hawaii. It also has a high likelihood of establishing in areas that are only marginally suitable for the competing parasitoid F. arisanus. This knowledge is being presented to regulatory officials to secure release permits. A second African parasitoid, Fopius caudatus, appears to have a narrow host range and may also contribute to the overall guild of biocontrol agents.


  • Bokonon-Ganta, A. H., M. Ramadan & R. H. Messing. 2007. Reproductive biology of Fopius ceratitivorus (Hymenoptera: Braconidae), an egg-larval parasitoid of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Biological Control 41: 361-367.

Progress 08/15/05 to 08/14/06

We have imported and established in quarantine a colony of the opiine braconid parasitoid Fopius caudatus from Kenya. This is the first colony of this species ever to be established anywhere in the world (previous attempts in Israel, Guatemala, and here in Hawaii have failed). In preliminary studies we determined that the parasitoid attacks the eggs of Mediterranean fruit fly (Ceratitis capitata) and successfully develops, emerging from the pre-pupal stage. Host range testing with other pest fruit flies as well as non-target species is in progress. We also continued to gather data on the biology and host range of another opiine braconid egg-attacking parasitoid of C. capitata. Fopius ceratitvorus was found to be host-specific to medfly, it cannot succesfully develop on Bactrocera cucurbitae, B. dorsalis, or B. latifrons. Furthermore, the parasitoid completely ignores non-target hosts that do not occur in fruit tissues, including the gall forming tephritids Eutreta xanthochaeta and Procecidochares alani, as well as the flower head feeder Trupanea dubautiae. We have submitted a dossier and all necessary documentation regarding F. ceratitivorus to the Hawaii Dept. of Agriculture in application for a release permit to take the wasp out of quarantine and conduct field evaluations. We have already received necessary Federal permits to do so.

By importing additional species of parasitoids we can increase natural mortality of fruit flies in Hawaii with minimal non-target risk. This has the potential to reduce pesticide inputs on farms and increase agricultural profitability and sustainability.


  • Bokonon-Ganta, A. H., Ramadan, M. M., Wang, X. G. & Messing, R. H. 2005. Biological performance and potential of Fopius ceratitivorus (Hymenoptera: Braconidae), an egg-pupal parasitoid of tephritid fruit flies, newly imported to Hawaii. Biological Control 33: 238-247.
  • Bokonon-Ganta, A. H. & R. H. Messing. 2006. Biological control of tephritid fruit flies in Hawaii with reference to the newly discovered egg-larval parasitoid, Fopius ceratitivorus (Wharton). Proceedings of the Hawaiian Entomological Society, in press.