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BIOLOGICAL CONTROL OF FRUIT FLIES
The fruit flies of the family Tephritidae constitute a group of agricultural pests of worldwide importance, as they attack a wide range of fruits and vegetables. The most important are the several species of Dacus and Ceratitis, which occur in many countries of warm temperate and subtropical climates; Anastrepha, an American genus occurring from Mexico and the West Indies through South America; and Rhagoletis, with a more restricted host range, occurring in the north temperate region. The Mediterranean fruit fly, although eradicated periodically from the state of Florida where it had "peninsular" distribution, is presently firmly established in southern Mexico where it is temporarily contained by a massive sterile-male and parasite release effort by the U. S. Department of Agriculture. Eventually this species may move north and pose a continuous threat along the Mexico-United States border. Another chronic threat has been the permanently established population in the Hawaiian Islands, from which periodic accidental invasions of California are thought to occur. Recently, Carey & Dowell (1989), Greathead & Waage (1983), Gilstrap et al (1987), Wharton (1989) and Wong & Ramadan (1990) have noted that further biological control efforts are definitely justified against fruit flies.
Principal Fruit Flies in California
The Mediterranean fruit fly in particular has received a lot of attention in recent times. It is a major pest throughout the Mediterranean region, portions of Africa, the Middle East, Central and South America, Mexico, and Hawaii, and has become established in Australia. In France, it is able to persist from year to year only in areas bordering the Mediterranean, yet survival is reported in Austria, where severe winters, with continuous frosts, can cause up to 90% mortality of the pupae (Clausen 1978). Several studies have investigated the potential economic of C. capitata in California and elsewhere. Details on this and various abatement tactics may be found in UC/AID (1977) Galt & Albertson (1981), Carey (1982, 1984), Gilmore (1983), Dowell (1983), Schreibner (1983), Spitler & Couey (1983), Williamson (1983), Krainaker et al. (1987) and Carter (1990). Although parasitic insects have been imported against it, all except one species were obtained from areas outside the fly\'s native range in central Africa. However, some reductions in infestations are attributable to natural enemy activity in the invaded areas, especially when parasitic insects are mass released as biotic insecticides (Wong & Ramadan 1990, Wong et al. 1990).
Some investigators believe that the Medfly is already permanently established in California and that unless the current eradication effort is greatly increased, it is just a matter of time before it will spread throughout the state (Barinaga 1990). The Malathion and other baits currently in use against Medflies may not be potent enough for fast eradication, as it is recognized that Medflies will not eat the bait unless that is the only substance placed in their cages (Citrograph 1990). Under outdoor conditions they may prefer to seek out clean ripening fruit.
As it becomes increasingly apparent that fruit flies pose continuous threats to California\'s agriculture through periodic invasions of our borders, there is an urgent need to consider the application of alternative methods to chemicals in eradication and control programs. The implementation of effective biological controls at the sources of an invasion as well as within the state boundaries where breeding may occur, offers an environmentally sound, non-polluting alternative. There is a need to (1) develop and improve techniques for the search, procurement and evaluation of natural enemies of fruit flies in their natural ranges (parasites, predators and pathogens); (2) introduce and study foreign natural enemies and evaluate their respective effectiveness under field conditions in Hawaii, southern Mexico, and California; (3) develop a mass production scheme for periodic releases of introduced natural enemies in infested areas of California, and to observe their effectiveness under natural conditions; and (4) build a culture bank of natural enemies for use in conjunction with other eradication and control methods (e.g., sterile-male releases) during periodic invasions of this pest and in anticipation of its possible permanent establishment in the State of California.
The need for investigation into the biological control of fruit flies in Hawaii, Mexico and California is ever more important as it becomes recognized that insecticides, although offering expedient and predictable results under certain conditions, are often inadequate and at least perceived as dangerous, if not physically dangerous to wildlife and humans alike. As problems involving insecticidal residues and insect resistance to chemicals continue to increase, many programs directed at the control of fruit flies must ultimately be modified with increased dosages and costs to such an extent that they invariably arouse the concern and ire of naturalist and conservationist organizations. A case in point is the fire ant eradication program. By 1959 extensive damages to wildlife and domestic animals had positively been attributed to the effects of several insecticides used in the program (Clawson 1959). Fire ant control was finally declared unsuccessful in 1960, and in some states, fire ant numbers were actually reported to have increased since the eradication program began (Byrd 1960, Cottam 1959). Presently, a new effort to control fire ants is being attempted with natural enemies imported from Brazil and Argentina.
Biological Control Efforts Against Fruit Flies
The biological control efforts against fruit flies of the genus Tephritidae have been extensive over the past half century, a thorough review being given in Clausen (1987). However, as it becomes increasingly apparent that the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), and Mexican fruit fly, Anastrepha ludens (Loew) pose a continued threat to California\'s agriculture through periodic invasions of our borders, there is an urgent need to consider the application of alternative methods to chemicals in eradication and control programs. The implementation of effective biological controls at the sources of an invasion as well as within the state boundaries where breeding may occur, offers an environmentally sound, non-polluting alternative. There is an urgent need to (1) search for, procure and initially evaluate natural enemies of Mediterranean and Mexican fruit flies in their natural ranges in central Africa and southern Mexico (parasites, predators and pathogens); (2) introduce and study foreign natural enemies in the adult stage, and evaluate their respective effectiveness under field conditions in Hawaii, southern Mexico, and if applicable, California; (3) attempt development of a mass production scheme of resident California fruit flies (e.g., walnut husk fly) to serve as acceptable hosts for Medfly natural enemies for use in laboratory study and periodic colonization efforts in infested areas of California, and (4) to test the feasibility of building a culture bank of Medfly and Mexican fruit fly natural enemies on resident California fruit flies for use in conjunction with other eradication and control methods (e.g., sterile-male releases, adult fly baiting) during periodic invasions of these pests and in anticipation of their possible permanent establishment in the State of California.
Medfly. Cerititis capitata (Wiedemann)-- The Mediterranean fruit fly was first described fin 1824 and was first noted as a pest in citrus in 1829 from shipments of oranges to England from the Azores. The fly spread throughout the world over the next 100 years and was continually noted as a destructive pest wherever it was found. The first program for the biological control of the medfly was undertaken by the government of Western Australia in 1902 with the engagement of George Compere to search for natural enemies and to determine the aboriginal home of the medfly. Unfortunately Compere was never able to ascertain the aboriginal home nor did he establish the parasites he collected from India, Sri Lanka and Brazil in Western Australia.
The medfly invaded Hawaii in 1910 and soon thereafter the Board of Commissioners hired Filipi Silvestri to again search for natural enemies of this fly. It was determined by experts of the day that collections should concentrate in Western Africa. Therefore, Silvestri traveled for eight months through West and East Africa and South Africa. He found only six specimens of the medfly on the entire journey, but reared many parasitic insects from other fruit-infesting tephritids collected along the way. He managed to establish four species in Hawaii: Opius concolor Szepligeti, Biosteres tryoni (Cameron), Coptera silvestrii Kieffer and Dirhinus anthracina Walker. Two more missions over the next 30 years were sent out in hopes of obtaining parasitic insects, but only Tetrastichus giffardianus Silvestri and Biosteres fullawayi (Silvestri) were established.
Other biological control programs were undertaken in several countries where the medfly was firmly established, but these programs have not been well documented, and the extent of control of any of the parasitic species is virtually unknown, the notable exception being Hawaii. Even in Hawaii control was never noteworthy and the medfly problem was finally overshadowed by the introduction of Dacus dorsalis Hendel. For North America the answer to the medfly invasions starting in 1929 was complete eradication by means of fruit stripping and poisoned bait sprays.
The success of these early and subsequent biological control programs against the medfly has been variable (Gilstrap & Hart 1987, Wharton & Gilstrap 1983). In Hawaii, a cooperative biological control program initiated in 1948 involved the release of 32 entomophagous species to combat both medfly and the oriental fruit fly. Three parasitic species, Biosteres longicaudatus (Ashmead), B. vandenboschi (Fullaway), and B. oophilus (Fullaway) became widespread and abundant (Bess et al. 1961). During 1966-1968, parasitization of the medfly and the oriental fruit fly was high (ca. 70%); it was mainly due to the egg-pupal parasite, B. oophilus (Haramoto & Bess 1970). During 1978-1981, Biosteres oophilus was still the predominant parasite as it accounted for ca. 80% of the total parasitization. Occasionally the larval-pupal parasite, Biosteres longicaudatus and B. tryoni (Cameron) achieved a parasitization of 32 and 8%, respectively (Wong et al. 1984). Extensive fruit collections done between 1949-1985 showed that Jerusalem cherry, coffee and peach were among the most important hosts of the medfly. These fruits yielded more than 100 larvae/Kg of infested fruits (Liquido et al. 1990; Nishida et al. 1985). The fruits that yielded a high number of medfly larvae were elliptical or spherical and yellowish or reddish. They had a diameter of 1-7 cm and a weight of 1-30 grams. Most of these hosts belonged to five plant families: Myrtaceae, Rutaceae, Rosaceae, Sapotaceae and Solanaceae (Liquido et al. 1990).
In Costa Rica a classical biological control program was initiated in 1955. During 1979-1980 parasitic insects were collected from <10% of C. capitata populations. These were two introduced braconids, B. longicaudatus and B. oophilus, and two indigenous cynipids, Ganaspis carvalhoi (Dettmer) and Odontosema anastrephae (Borgmeier) (Wharton et al. 1981). An exploration for natural enemies of the medfly, conducted in West-Central Africa during 1980-1982, showed that C. capitata occurred in low frequency in coffee plantations in Cameroon. Parasitization of tephritids in coffee by braconids ranged from 10-56% (Steck et al. 1986). In Guatemala infestation of C. capitata was serious in coffee and tangerine. The rest of the fruits were mainly infested by Anastrepha spp. (Eskafi 1988, 1990). Parasitization rate of C. capitata and Anastrepha spp. was low, ranging from 0.04 to 7.95%. The most common parasitic species recovered from both flies were B. longicaudatus and Doryctobracon crawfordi (Viereck) (Eskafi 1990).
The behavior of the ectoparasite Muscidifurax raptor (Girault & Sanders) in searching for the potential host C. capitata pupae was analyzed under laboratory conditions. The searching efficiency of M. raptor females decreased with increasing density. The proportion of avoidance of superparasitism was 0.615. The response to a high parasite density was to increase the proportion of males in the progeny, as males searching for mates interfered and decreased the searching activity of the females (Podoler & Menzel 1977, 1979). The medfly was susceptible to the Mexican strain of the nematode Steinernema feltiae. Emerging adults and pupae were not susceptible to the nematode, but the third instars (prior to pupating in the soil) suffered high mortalities (50-90%) when exposed to high nematode concentrations (150,000 - 500,000 nematodes/cup) (Lindegren & Vail 1986). Field exposure of mature larvae to a dose of 500 nematodes/cm2 yielded high mortality of C. capitata (Lindegren et al. 1990). In addition to the hymenopterous parasites and insect pathogenic nematodes, arthropod predators such as ants could play an important role in reducing fruit fly populations. Under laboratory conditions, the Argentine ant, Iridomyrmex humilis (Mayr) caused 50% mortality of medfly pupae after a 10 min. attack. However, ant predation could be important only in localized areas; it is not adequate to regulate medfly populations (Wong et al. 1984).
Typically, the most effective natural enemies of an insect occur in regions where the pest originated. The natural range of the Mediterranean fruit fly is the sub-Saharan central African region, including the Island of Madagascar. Although no information is available from Madagascar, a number of promising natural enemies have been discovered in Central Africa (Table 1; Bianchi & Krauss 1936, 1937; Gilstrap & Hart 1987, Greathead 1976, Silvestri 1914, Steck et al. 1986, van Zwaluwenburg 1936, 1937, Wharton, 1989, Wharton & Gilstrap 1983). However, because of technological difficulties associated with transportation and culture, only two species attacking Ceratitis capitata have been successfully translocated out of central Africa. A concentrated effort to locate natural enemies there might yield the kind of species capable of regulating this pest at low densities, as it has been known to be rare in that general region since the early 1900\'s (Silvestri 1913). The parasitic Hymenoptera are believed to be the most effective natural enemies of fruit flies. At least six species of fruit flies in the genus Ceratitis are known from central Africa, and numerous parasitic Hymenoptera have been reported active on them at very low host densities (Table 1, Silvestri 1913, Clausen 1978, F. Gilstrap, pers. comm.). These have not been tested by entomologists in California because the Mediterranean fruit fly has been quarantined. Therefore, promising species of natural enemies for Medfly might be found among these related species. Also, there has been no concentrated effort to locate disease organisms, such as viruses, bacteria and fungi, which might prove invaluable in eradication campaigns.
Table 1. Known parasitic species attacking fruit flies of the genus Ceratitis in their natural
Central African range
( Parasite species & Host stage attacked)
Biosteres caudatus Szepligeti larva Hedylus sp. larva, Diachasma fullawayi Silvestri larva, Galesus silvestrii Kieffer pupa, Diachasmimorpha longicaudata (Ashmead) larva ,
Microbracon celer (Szepligeti) larva?, Diachasmimorpha tryoni (Cameron) larva, Opius humilis Silvestri larva, Dirhinus ehrhorni Silvestri pupa, Opius inconsuetus Silvestri larva
Dirhinus giffardii Silvestri pupa, Hedylus giffardii Silvestri larva?, Ganaspis sp. larva? Opius n. sp. larva, Halticoptera sp. larva? , Spalangia afra Silvestri pupa
Opius perproximus Silvestri larva, Tetrastichus dacicida Silvestri larva, Tetrastichus giffardii Silvestri larva, Tetrastichus oxyurus Silvestri larva, Tetrastichus n. sp. larva
Mexican fruit fly. Anastrepha ludens (Loew)--Some of the natural enemies of oriental and Mediterranean fruit flies have shown activity on Anastrepha spp. in southern Mexico, and may be influential in partial biological control of that species (Aluja et al. 1990). However, there have been no formal attempts to obtain natural enemies from other areas where different species of Anastrepha occur, such as South America.
Two species of parasitic insects are already proven and available as biotic insecticides (augmentive releases) against Medfly. These are Diachasmimorpha longicaudata and D. tryoni, which have been used with some success in Mexico and Hawaii (USDA 1988, Wong et al. 1990a,b). The use of these parasites in lieu of Malathion during the establishment phase of specific natural enemies from central Africa, would greatly aid their survival and while providing some economic control of Medfly.
Misc. fruit flies--Several species of Rhagoletis are very important pests of cultivated cherries in North America and Europe, with some species having been considered as subjects for biological control, despite the low economic threshold. Infestation rates of less than 0.2% are currently required for commercial marketing of cherries in the United States. Four species of parasitic insects associated with the Oriental fruit fly, Dacus dorsalis Hendel, were introduced against such fruit flies. These included Opius longicaudatus compensans (Silv.), Opius longicaudatus farmosanus (Full.), Opius oophilus Full., and Opius longicaudatus novacaledonicus Full. These parasites were introduced from Hawaii and released against Rhagoletis indifferens Cueran and Rhagoletis fausta Osten Sak in Oregon and Washington in the 1950\'s (Clausen 1956b). However, none became established probably because they all originated in tropical regions. A parasite of R. cerasi, the European cherry fruit fly, was imported against the eastern cherry fruit fly, R. cingulata Loew during 1959-64 in New Jersey, without successful establishment. Other species including Biosteres sublaevis Wharton, Coptera occidentalis and Phygadeuon wiesmanni are under investigation in California and Oregon (Croft & AliNiazee 1992).
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