The genus Ceratitis is one of the best known because of the notoriety of one of its Exotic fruit pests and members-the Mediterranean fruit fly. Over 100 Ceratitis species have been de- California agriculture scribed, of which six are known pests. The genus is thought to have evolved in Africa, and most species are distributed in regions James R. Carey u Robert V. Dowell with Mediterranean climates. Anastrepha includes 150 to 200 species Because of their worldwide distri- balance of commodity trade would shift native to the Caribbean, Mexico, and Cen- bution and numbers, future intro- temporarily to other states. But a estab- tral and South America. Two species are lished in California is likely to spread rap- now present in the southern United States, ductions of fruit into California idly toother states with similar climates and through either natural spread or introduc- are inevitable. Infestations of eco- potential hosts. Because of the adverse ef- tion by humans-the Mexican fruit fly in nomically important pests, includ- fects such establishment would have on the southern Texas and the Caribbean fruit fly ing but not limited to the medfly, U.S. agricultural economy, eradication in Florida. Mexican fruit fly, and oriental fruit programs are mandated by the federal Of the approximately 500 Dacus species, government. 30 to 40 are known or potential pests, in- fly, are expensive to treat, and their This article reviews thestatus of pest fruit cluding the oriental fruit fly, the melon fly, elimination is seldom certain. Re- flies in California agriculture. It includes and the Malaysian fruit fly. With the excep- searchers are seeking to improve general information on fruit fly ecology and tion of the olive fruit fly found in Europe, detection and control methods. biology and the state of basic and applied most members of this genus are tropical or research. subtropical and native to Africa, Asia, Aus- tralia, and theSouth Pacific. Aclose relative The frequency of pest fruit fly introductions Worldwide distribution of the oriental fruit fly is currently estab- into the state is on the increase. From the Virtually all pest fruit flies are in the lished in the South American country of time when records were first kept in the dipteran family , whose mem- Surinam. middle of last century until the mid-l980s, bers are known as the “true“ fruit flies. They Around 50 species have been eight exotic, or non-native, species were differ from the more common Drosophila described. Most are widely distributed captured, including the Mediterranean fruit species in that adults are relatively large over the temperate and subtropical regions. fly (medfly), Mexican fruit fly, and oriental (typically larger than house flies), and fe- These species have only one to two genera- fruit fly. In 1987 alone, nine species of fruit males tend to lay eggs in mature rather than tions per year and tend to attack a narrow flies were captured, three of which had in decomposing fruit. About 100 tephritid range of fruit species. The walnut husk fly never before been recovered. One of species are native to California. Most of and the maggot are two of the better these-an Asian species related to the orien- these feed on flower heads or are gall-form- known pests in this genus. tal fruit fly-had never been described by ers but do not attack fruit. The walnut husk fruit fly taxonomists. That summer the fly and the apple maggot are the only fruit- Host relations California Department of Food and Agri- attacking tephritids established in the state, Fruit flies have evolved to exploit virtually culture (CDFA) initiated separate eradica- having been introduced in the early 1920s every type of fruit and vegetable found any tion programs on five species: the apple and 1980s, respectively. place in the world. Some species, such as maggot, melon fly, medfly, peach fruit fly, Most tephritids of economic importance the apple maggot and papaya fruit fly, are and oriental fruit fly. The medfly has been fall into four genera: Ceratitis, Aimstrepha, highly specialized and attack only one host recovered in the state seven times since Dacus, and Rhagoletis . species or a narrow range of closely related 1982, when it was eradicated in Santa Clara County. The 1980-82 eradication campaign against the medfly marked the beginning of a new era in fruit fly research and in the CDFA’s detection, quarantine, and eradication protocols. There was a public outcry against chemical sprays, and growers be- came concerned over the possible perma- nent establishment of exotic fruit fly pests. Although there were and are no certain so- lutions, there has been progress on under- standing fruit fly biology and ecology as well as advances in control and detection techniques, technologies, and strategies. Establishment of a major fruit fly pest such as the medfly in California would have widespread effects on agriculture, because this species and others attack a large variety of high-value crops that are exported. Quarantines imposed by the major import- ing countries would require disinfestation procedures. These would increase costs 10% to loo%, depending on the fly species Worldwide distribution of fruit fly pests. Species listed for California are examples of recent intro- and commodities affected. The competitive ductions that have subsequently been eradicated.

38 CALIFORNIA AGRICULTURE. MAY-JUNE 1989 ones. Other species attack a wide variety of were extrapolated to the natural environ- affect stone fruits by direct attack as well as hosts; these ”generalists” include the West ment. Many involved in the program ig- by quarantine measures. Many citrus varie- Indian fruit fly, the medfly, the Mexican nored the results of long-term studies of the ties would be affected more by quarantine. fruit fly, and the oriental fruit fly. Some medfly as an introduced pest in other re- Cotton would probably be only marginally species attack extremely large hosts; for gions of the world. The medfly occurs in affected by direct damage and not at all by example, the jack fruit fly, a specialist from regions with climates similar to three of the a quarantine. Third, host records represent Southeast Asia, attacks jack fruit weighing four major climatic zones in California: cli- realized and not potential hosts and are several hundred pounds. Others, such as mates in most parts of the Sacramento Val- incomplete for most flies. The reason is that the medfly, may choose small hosts like ley and the coastal regions are classified as human activity often results in new combi- coffee cherries that only contain enough Mediterranean, similar to those of Greece nations of flies and hosts. The mango, for food resources for one to three larvae to and Italy; parts of the San Joaquin Valley example, was not a host of the Mexican fruit mature. near Fresno have climates classified as fly until it was introduced into Mexico and No fruit fly species have ovipositors steppe, similar to many parts of North Af- the Americas in the last century from India. adapted to directly penetrate thick citrus rica such as Tunisia; the climate near Similar situations certainly exist for many rinds, such as those on citron, or fruit with Barstow and Imperial is classified as hot California fruit fly hosts, but in this case, the hard skins, such as pomegranates or avoca- desert like many parts of Middle Eastern new pest is brought to the host. dos. These hard- or thick-skinned hosts are countries such as Egypt and Israel. The We estimate that roughly 80 species of not immune to attack, however, because medfly abounds in all of those countries. fruit flies found throughout the world are fruit fly females are usually able to find A number of countries with other serious realized or potential threats to California cracks or soft spots in the host for laying fruit fly pests have climates similar to those agriculture. They fall into three categories: eggs. As a result, even marginal hosts are in California. For example, three major (1) introduced species that are currently subject to the same quarantine regulations pests-the peach fruit fly, the melon fly, and established in thestate (walnut husk fly and as more favorable ones. the Ethiopian fruit fly-occur in Pakistan, apple maggot); (2) introduced species that many parts of which are hot and dry like were subsequently eradicated or died out Movement California’s Central Valley. The peach fruit (total of 12 species including the medfly, Pest fruit flies may enter California by ei- fly and melon fly have both been recovered Mexican fruit fly, and oriental fruit fly); and ther ”jump dispersal” or simple diffusion. previously in California. (3) species that have never been recovered The first refers to movement across long Irrigation complicates the picture, because in the state but are thought to have a high distances in a short time, usually across it allows the production of crops that would probability of establishment if introduced inhospitable areas such as oceans or deserts. not ordinarily grow in the state. Fruit fly (including species found in dry, hot sum- This method of entry is the most serious species that specialize in these hosts may or mer climates such the Ethiopian fruit fly. threat, in part because of its unpredictabil- may not be able to survive the climate, but Species not considered serious threats ity. For example, infested fruit may be one of the basic conditions is met-host include ones such as the olive fly, whose brought into the state in the mail, by road or plant availability. hosts-raw olives-are seldom carried by railroad, and by air. Air travelers from air travelers. Speciesconsidered unlikely to overseas are among the greatest potential Effect on agriculture become established, even if introduced, are sources of infestations, because (1) fruits Fruit flies affect agriculture both directly those found exclusively in the tropics that and vegetables carried by airplane passen- through larval damage to the crop and indi- specialize in hosts not grown in the state- gers are often still fresh when they enter the rectly through quarantine restrictions. In the papaya fruit fly, for example. state, so that fruit flies are able to survive, many parts of the world, fruit flies destroy The motive for import restrictions on and (2) the sheer numbers of travelers place 100%of the crop. For example, star fruit is a commodities from an infested region is a heavy load on regulation at ports of entry. profitable export for Malaysia, but oriental For example, in 1987 nearly 7 million air fruit flies destroy every fruit not protected passengers entered California through the with paper bags. Virtually all unprotected Los Angeles International Airport, over a mature peaches grown in backyards in million of whom arrived from Hawaii-a Hawaii become infested with fruit flies. state with four serious pest species. If, as a The quarantine restrictions placed on purely hypothetical number, one passenger commodities because of the presence of ina thousand carried fresh fruit, 7,000 could fruit flies are perhaps even more important. have been brought in during 1987alone. Major markets in other parts of the United In simple diffusion, fruit fly populations States, such as Florida, Arizona, and Texas, move gradually across hospitable terrain and other countries, such as Japan, either over many generations. For example, the totally restrict affected imports or require Mexican fruit fly or related species may post-harvest disinfestation treatments. eventually enter the state near San Diego. California crops susceptible to fruit fly Movement of the apple maggot through infestations are valued at over $4.5 billion diffusion from Oregon may partly account and include stone fruit, citrus, safflower, for its establishment in northern California. and nuts. Several aspects of this situation merit comment. First, almost every major Climatic requirements cropin thestateissubject toattackby oneor There was controversy during the 1980-82 more species. For example, cotton is not medfly eradication campaign over whether noted to be a prime host for any species, but the medfly could survive the winter in the it could serve as a marginal host in the ab- northern part of the state. Some people sence of more favorable hosts for fruit fly maintained that the population might die species such as the Ethiopian fruit fly. Sec- out naturally even without an eradication ond, not all commodities would be affected program. Part of the problem was that the in the same way or to the same degree. A results of laboratory temperature studies generalist species such as the medfly would

CALIFORNIA AGRICULTURE, MAY-JUNE 1989 39 Exotic fruit fly pests (continued) Most major fruit fly pests fall into four genera. Representatives of the four are, from left: Mexican fruit fly (Anastrepha),apple maggot fly (Rhago- letis),melon fly (Dacus),and Mediterranean fruit fly (Cerafitis).(Photos by Jack Kelly Clark)

uncertainty about the extent of direct dam- and bait traps (for all others including Anas- direct mating competition between labora- age that a fruit fly species would cause if it treplta spp.). The sex lure traps are the most tory-sterile males and wild, fertile males for were to become established. This unpre- species-specific but also are sex-specific wild, fertile females and through "dilution" dictability extends beyond the obvious (mostly males captured). The major short- of the numbers of wild males. Large num- cases. For example, melon flies are a more coming is the lack of attractants of any kind bers of sterile males decrease the proportion severe pest of tomatoes in Malaysia now for a large number of exotic pest fruit fly of all males that are fertile. It is a nonpol- than a decade ago because of a trend to species. luting technique that is increasingly effec- grow tomatoes hydroponically. Plants Eradication strategies are based on the tive as pest population levels decrease. grown by this method tend to have softer, simple premise that the death rate of the Parasitoid inundative release has received more succulent stems than do plants rooted target pest must exceed its birth rate for a only limited attention so far. Massive in soil. Melon flies in Malaysia now attack sustained period. This can be accomplished numbers of parasitoids are required, and not only the tomato fruit but also the sof- by increasing deaths, by decreasing births, technologies for their large-scale produc- tened main stem, killing the entire plant. It or by a combination of the two. Basically tion are just now being developed. would have taken a true visionary to have four tactics are available for controlling or fully anticipated this problem. Similarly eradicating fruit flies: chemical control, Conclusions unpredictable situations could arise in Cali- male annihilation, the sterile- tech- Two aspects of the fruit fly problem are fornia with the introduction of certain pest nique, and parasitoid inundative release. fairly predictable: (1) future fruit fly intro- species. Chemical control of fruit flies entails ap- ductions are inevitable because of the It is also difficult to estimate the serious- plying soil drenches against soil-inhabiting worldwide distribution and abundance of ness of a pest in its native region to predict pupae or bait sprays against adults. For the large numbers of important species; and (2) how serious it might be if it became estab- bait sprays, a pesticide such as malathion is the number of introductions is likely to rise lished elsewhere. The true pest status of mixed with protein hydrolysate and ap- as the number of travelers entering the state flies is frequently unclear in their native plied by air or by ground rig. Flies are at- and commodity imports increase. regions. For example, the citrus fly is not a tracted to the bait, feed, and are killed. This Fruit fly eradication programs are con- major pest in southern China where citrus approach is more selective than broad-spec- strained technically in the same way as all orchards are common. But many orchards trum spraying. pest management programs. Progress in are sprayed with miticides up to 20 times The second method uses a sex lure com- detection and control technologies will be annually. Without controlled studies, it is bined with a pesticide to attract and kill almost certainly be made in steps rather impossible to say whether the citrus fly is males on contact. If a large enough portion than in large technologicaljumps. Research not a serious pest because of these sprays or of the male population is killed, females will strategies designed to deal with introduced for some other reason. Anecdotal informa- not find mates and thus will not produce pests must be tailored accordingly to ensure tion is all that is available for many species. fertile eggs. This method is effective only if that no major exotic fruit fly pest becomes a powerful attractant for males is available. established in the state. Detection and eradication It is most commonly used against the orien- CDFA currently budgets $7 million for tal fruit fly, which is attracted to an insecti- James R. Carey is Associate Professor, Depart- fruit fly trapping alone. Three types of traps cide-laced methyl eugenol lure. ment of Entomology, University of California, are used to detect fruit flies: sex lure traps The sterile-insect technique eradicates the Davis,and Robert V.Dowel1 is Senior Economic (for medfly, oriental fruit fly, and melon target pest through the release of large Entomologist, California Department of Food fly); color sticky traps (for apple maggot); numbers of sterile flies. It works through and Agriculture, Sacramento.

40 CALIFORNIA AGRICULTURE, MAY-JUNE 1989