Abstract
The potential negative impacts of biological pest control on non-target species have become the focus of a contentious debate. In this article, we use examples from both classical and augmentative biological control of fruit fly pests in Hawaii to address several important factors in assessing non-target risks of fruit fly parasitoids. Several fruit fly parasitoids have been introduced to Hawaii and contribute substantially to the reduction of pest populations in the state's farms and forests. However, an historical lack of host-specificity testing of these parasitoids with non-target species has raised concerns about their impact on non-pest fruit flies, including some flies deliberately introduced for biological control of weeds and others that are endemic Hawaiian species. When developing protocols to assess risks of introduced fruit fly parasitoids, we need first to define an appropriate range of species against which host specificity should be tested. For assessing susceptibility of a non-target species to parasitoids, behavioral tests are as important as suitability tests. Experimental factors, such as host-exposure substrate, absence or presence of preferred hosts, and laboratory vs. natural conditions, are shown to affect the results of host-specificity tests and risk analysis. Still, assessing long-term, indirect ecological impacts of parasitoids and weighing potential risks and benefits in multiple dimensions (besides dollar values) remains a challenge to environmentalists, conservationists, applied ecologists, and biocontrol practitioners.
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References
Asquith, A. (1995), “Alien species and the extinction crisis of Hawaii's invertebrates,” Endangered Species Update 12: 6–7.
Barratt, B. (1996), “Biological control: Is it environmentally safe?,” Forests and Birds 282: 36–41.
Baranowski, R., H. Glenn, and J. Sivinski (1993), “Biological control of the Caribbean fruit fly (Diptera: Tephritidae),” Florida Entomologists 76: 245–251.
Bautista R. C., and E. J. Harris (1996), “Effect of fruit substrates on parasitization of tephritid fruit flies (Diptera) by the parasitoid Biosteres arisanus (Hymenoptera: Braconidae),” Environmental Entomology 25: 470–475.
Bess, H. A. (1950), “Notes on parasites of tephritid flies,” Pro-ceedings of the Hawaii Entomological Society 14: 26.
Bess, H. A., and F. H. Haramoto (1958), “Biological control of pamakani, Eupatorium adenophorum, in Hawaii by a tephritid gall fly, Procecidochares utilis, 1: The life history of the fly and its effectiveness in the control of the weed,” Proceedings of the 10th International Congress of Entomology 4: 543–548.
Bess, H. A., and F. H. Haramoto (1959), “Biological control of pamakani, Eupatorium adenophorum, in Hawaii by a tephritid gall fly, Procecidochares utilis, 2: Population studies of the weed, fly, and the parasites of the fly,” Ecology 40: 244–249.
Bess, H. A., and F. H. Haramoto (1972), “Biological control of pamakani, Eupatorium adenophorum, in Hawaii by a tephritid gall fly, Procecidochares utilis, 3: Status of the weed, fly and parasites of the fly in 1966- 1971 versus 1950- 1957,” Proceedings of the Hawaii Entomological Society 21: 165–178.
Bess, H. A., R. van den Bosch, and F. H. Haramoto (1961), “Fruit fly parasites and their activities in Hawaii,” Proceedings of the Hawaii Entomological Society 17: 367–578.
Burns, R. E., J. D. Diaz, and T. C. Holler (1996), Inundative release of the parasitoid Diachasmimorpha longicau-data for the control of the Caribbean fruit fly, Anastrepha suspensa,” in G. J. Steck and B. A. McPheron (eds.), Fruit fly pests: A world assessment of their biology and management (pp. 377–381). Del Ray Beach, FL: St. Lucie Press.
Clancy, D. W. (1950), “Notes on parasites of tephritid flies,” Proceedings of the Hawaii Entomological Society 14: 25–26.
Clancy, D. W. (1952), “Notes on parasites of tephritid flies,” Proceedings of the Hawaii Entomological Society 14: 374–375.
Clausen, C. P. (1956), “Biological control of fruit flies,” Journal of Economic Entomology 49: 176–178.
Clausen, C. P. (1978), “Introduced parasites and predators of arthropod pests and weeds: A world reviews,” US Department of Agricultural Handbook 480: 320–335.
Duan, J. J., and R. H. Messing (1996), “Response of 2 opiine fruit fly parasitoids (Hymenoptera: Braconidae) to the lantana gall fly (Diptera: Tephritidae),” Environmental Entomology 25: 1428–1437
Duan, J. J., and R. H. Messing (1997), “Effects of two opiine parasitoids (Hymenoptera: Braconidae) introduced for fruit fly control on a non-target native Hawaiian tephritid, Trupanea dubautiae (Diptera: Tephritidae),” BiologicalControl 8: 177–184.
Duan, J. J., M. F. Purcell, and R. H. Messing (1996), “Para-sitoids of non-target tephritid flies in Hawaii: Implications for biological control of fruit fly pests,” Entomophaga 41:245–256.
Duan, J. J., A. Mukhta, J. Kailash, and R. H. Messing (1997a), “Evaluation of the impact of the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Bracon-idae) on a non-target tephritid, Eutreta xanthochaeta (Diptera: Tephritidae),” Biological Control 8: 58–64.
Duan, J. J., M. F. Purcell, and R. H. Messing (1997b), “Ovipositional responses of 3 opiine fruit fly parasitoids (Hymenoptera: Braconidae) to gall-forming tephritids (Diptera: Tephritidae),” Biological Control 9: 81–88.
Fisher, M. (1971), Index of world Opiinae. Paris: LeFranc¸ois.
Fisher, M. (1973), “Hymenoptera Braconidae (Opiinae I),” Das Tierreich 91: 1–620.
Fisher, M. (1977), “Hymenoptera Braconidae (Opiinae II),” Das Tierreich 96: 1–1001.
Field, R. P., and S. M. Darby (1991), “Host specificity of the parasitoid, Sphecophaga vesparum (Curtis) (Hymenoptera: Ichneumonidae), a potential biological control agent of the social wasps, Vespula germanica (Fabricius) and V.vulgaris (Linnaeus (Hymenoptera: Vespidae) in Australia,” New Zealand Journal of Zoology 18: 193–197.
Funasaki, G. Y., P. Y. Lai, L. M. Nakahara, J. W. Beardsley, and A. K. Ota (1988), “A review of biological control introductions in Hawaii: 1890 to 1985,” Proceedings of the Hawaii Entomological Society 28: 105–160.
Glas P. C. G., and L. E. M. Vet (1983), “Host-habitat location and host location by Diachasma alloeum Muesebeck (Hym.:Braconidae), a parasitoid of Rhagolettis pomonella Walsh (Dipt.: Tephritidae),” Netherlands Journal of Zoology 33: 41–54.
Greany, P. D., T. R. Ashley, R. M. Baranowski, and D. L. Cham-bers (1976), “Rearing and life history studies on Biosteres longicaudatus,” Entomophaga 21: 207–215.
Greany, P. D., J. H. Tumlinson, D. L. Chambers, and G. M. Boush (1977), “Chemically mediated host finding by Biosteres (Opius) longicaudatus, a parasitoid of tephritid fruit fly larvae,” Journal of Chemical Ecology 3: 189–195.
Hardy, D. E., and M. D. Delfinado (1980), Insects of Hawaii, Vol. 13: Diptera: Cyclorrhapha III. Honolulu: The University Press of Hawaii.
Headrick, D. H., and R. D. Goeden (1994), “Relationships of biological control to the medfly eradication program in southern California,” in J. G. Morse, R. I. Metcalf, J. R. Carey and R. V. Dowell (eds.), The Mediterranean fruit fly in California: Defining critical research (pp. 59–70). River-side: University of California Press.
Howarth, F. G. (1983), “Classical biocontrol: Panacea or Pandora's box,” Proceedings of the Hawaii EntomologicalSociety 24: 239–244.
Howarth, F. G. (1985), “Impacts of alien land arthropods and mollusks on native plants and animals in Hawaii,” in C. P. Stone and J. M. Scott (eds.), Hawaii's terrestrial ecosystems: Preservation and management (pp. 149–179). Honolulu: University of Hawaii Press.
Howarth, F. G. (1991), “Environmental impacts of classical biological control,” Annual Review of Entomology 36: 485–509.
Keiser, I. (1968), “Residual effectiveness of foliar sprays against the Oriental fruit fly, melon fly and Mediterranean fruit fly,” Journal of Economic Entomology 61: 438–443.
Leyva, J. L., H. W. Browning, and F. E. Gilstrap (1991), “Effect of host fruit species, size, and color on parasitization of Anastrepha ludens (Diptera: Tephritidae) by Diachasmimor-pha longicaudata (Hymenoptera: Braconidae),” Environmental Entomolology 20: 1469–1474.
Lockwood, J. A. (1987), “The moral standing of insects and the ethics of extinction,” Florida Entomologist 70: 70–89.
Lockwood, J. A. (1993), “Environmental issues involved in biological control of rangeland grasshoppers (Orthoptera: Acrididae) with exotic agents,” Environmental Entomology 22: 503–518.
Lockwood, J. A. (1996), “The ethics of biological control: Understanding the moral implications of our most powerful ecological technology,” Agriculture and Human Values 13(1): 2–19.
Loope, L. L., and A. C. Medeiros (1992), “Potential effects of alien fruit fly eradication on natural areas of Hawaii: An exploratory investigation in Haleakala National Park,” Journal of the Hawaii Audubon Society 52: 71–75.
Messing, R. H. (1996), “Status and needs of biological control research for Tephritid flies,” in G. J. Steck and B. A. McPheron (eds.), Fruit fly pests: A world assessment of their biology and management (pp. 365–367). Del Ray Beach, FL: St. Lucie Press.
Messing, R. H., and E. B. Jang (1992), “Response of the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to host fruit stimuli,” Environmental Entomology 21: 1189–1195.
Messing, R. H., L. M. Klungness, E. B. Jang, and K. A. Nishiji-ma(1997), “Response of the melon fly parasitoid Psyttalia fletcheri (Hym.: Braconidae) to host-habitat stimuli,” Journal of Insect Behavior 9: 933–945.
Newell, I. M., and F. H. Haramoto (1968), “Biotic factors influencing populations of Dacus dorsalis in Hawaii,” Proceedings of the Hawaii Entomological Society 20: 81–139.
Nishida, T. (1955), “Natural enemies of the melon fly, Dacus cucurbitae Coquillett in Hawaii,” Annals of the Entomological Society of America 48: 171–178.
Nishida, T. (1956), “An experimental study of the ovipositional behavior of Opius fletcheri,” Proceedings of the Hawaii Entomological Society 16: 126–134.
Ramadan M. M., T. T. Y. Wong, and J. W. Beardsley, Jr. (1989), “Insectary production of Biosteres tryoni (Cameron) (Hymenoptera: Braconidae), a larval parasitoid of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae),” Proceedings of the Hawaii Entomological Society 29: 41–48.
Ramadan, M. M., T. T. Y. Wong, and J. C. Herr (1994), “Is the oriental fruit fly (Diptera: Tephritidae) a natural host for the opiine parasitoid Diachasmimorpha tryoni (Hymenoptera: Braconidae)?,” Environmental Entomology 23: 761–769.
Sands, D. P. A. (1993), “Effects of confinement on para-sitoid/ host interactions: Interpretation and assessment for biological control of arthropod pests,” in S. A. Corey, D. J. Dall and W. M. Milne (eds.), Pest control in sustainable agriculture (pp. 196–199). Canberra, Australia: CSIRO.
Secord, D., and P. Kareiva (1996), “Perils and pitfalls in the host specificity paradigm,” BioScience 46: 436–447.
Silvestri, F. (1914), “Report of an expedition to Africa in search of the natural enemies of fruit flies (Trypetidae) with descriptions, observations, and biological notes.” Territory of Hawaii Board of Agriculture and Forestry, Division of Entomology Bulletin 3.
Simberloff, D. (1992), “Conservation of pristine habitats and unintended effects of biological control,” in W. C. Kauffman and J. E. Nechols (eds.), Selection criteria and ecological consequences of importing natural enemies (pp. 103–117). Lanham, MD: Thomas Say Publications in Entomology: Proceedings of the Entomological Society of America.
Simberloff, D., and P. Stiling (1996), “How risky is biological control?,” Ecology 77: 1965–1974.
Sivinski, J. M. (1996), “The past and potential of biological control of fruit flies,” in G. J. Steck and B. A. McPheron (eds.), Fruit fly pests: A world assessment of their biology and management (pp. 369–375). Del Ray Beach, FL: St. Lucie Press.
Steiner, L. F. (1952), “Fruit fly control in Hawaii with poison-bait sprays containing protein hydrolysates,” Journal of Economic Entomology 336–843.
US Fish and Wildlife Service (1996), “Endangered and threatened wildlife and plants: Reviews of plant and animal taxa that are candidates for listing as endangered or threatened species,” Federal Register 61(40): 7596–7602.
Van Driesche, R. G., and M. Hoddle (1997), “Should arthropod parasitoids and predators be subject to host range testing when used as biological control agents?,” Agriculture and Human Values 14(3): 211–226 (this issue).
Vargas, R. I., L. Whitehand, W. A. Walsh, J. Spencer, and C. L. Hsu (1995), “Aerial releases of sterile Mediterranean fruit fly (Diptera: Tephritidae) by helicopter: Dispersal, recovery, and population suppression,” Journal of Economic Entomology 88: 1279–1287.
Wagner, W. L., D. R. Herbst, and S. H. Sohmer (1990), Manual of the flowering plants of Hawaii, Vol. I. Honolulu: University of Hawaii and Bishop Museum Press.
Wharton, R. A., and P. M. Marsh (1978), “New world opiinae (Hymenoptera: Braconidae) parasitic on Tephritidae (Dip-tera),” Journal of the Washington Academy Society 68: 147–167.
Wharton, R. A., and F. E. Gilstrap (1983), “Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus s.l. (Diptera: Tephriti-dae),” Annals of the Entomological Society of America 76: 721–742.
Wharton, R. A. (1989), “Classical biological control of fruit infesting Tephritidae,” in A. S. Robinson and G. Hooper (eds.), World crop pests: Fruit flies, their biology, natural enemies, and control, Vol. 3b (pp. 303–313). Amsterdam: Elsevier Science.
Wapshere, A. J. (1974), “A strategy for evaluating the safety of organisms for biological weed control,” Annals of Applied Biology 77: 201–211.
Wong, T. T. Y., and M. M. Ramadan (1987), “Parasitization of the Mediterranean and oriental fruit flies (Diptera: Tephriti-dae) in the Kula area of Maui, Hawaii,” Journal of Economic Entomology 80: 77–80.
Wong, T. T. Y., and M. M. Ramadan (1992), “Mass-rearing biology of larval parasitoids (Hymenoptera: Braconidae: Opiinae) of tephritid flies (Diptera: Tephritidae) in Hawaii,” in T. E. Anderson and N. C. Leppla (eds.), Advances in insect rearing for research and pest management (pp. 405–426). Boulder, CO: Westview Press.
Wong, T. T. Y., N. Mochizuki, and J. I. Nishimoto (1984), “Seasonal abundance of parasitoids of the Mediterranean and oriental fruit flies (Diptera: Tephritidae) in the Kula area of Maui, Hawaii,” Journal of Economic Entomology 13: 140–145.
Wong, T. T. Y., M. M. Ramadan, D. O. McInnis, N. Mochizuki, J.A. Nishimoto, and J. C. Herr (1991), “Augmentative releases of Diachasmimorpha tryoni (Hymenoptera: Braconidae) to suppress a Mediterranean fruit fly population in Kula, Maui, Hawaii,” Biological Control 1: 2–7.
Wong, T. T. Y., M. M. Ramadan, J. C. Herr, and D. O. McInnis (1992), “Suppression of a Mediterranean fruit fly population with concurrent parasitoid and sterile fly releases in Kula, Maui, Hawaii,” Journal of Economic Entomology 85: 1671–1681.
Zw¨ olfer, H., and P. Harris (1971), “Host specificity determi-nation of insects for biological control of weeds,” Annual Review of Entomology 16: 159–178.
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Duan, J.J., Messing, R.H. Biological control of fruit flies in Hawaii: Factors affecting non-target risk analysis. Agriculture and Human Values 14, 227–236 (1997). https://doi.org/10.1023/A:1007456727655
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DOI: https://doi.org/10.1023/A:1007456727655