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REVIEW ARTICLE ▼ Biological controls investigated to aid management of olive fruit fl y in California by Kent M. Daane, Marshall W. Johnson, A B C Charles H. Pickett, Karen R. Sime, Xin-Geng Wang, Hannah Nadel, John W. Andrews Jr. and Kim A. Hoelmer The widespread and rapid establish­ ment of the olive fruit fl y in Califor­ nia required immediate changes in D E F integrated pest management (IPM) programs for olives. After fi nd­ ing that resident natural enemies did not provide adequate control, researchers began a worldwide search for parasitoids, with explora­ Parasitoids imported into California for quarantine studies include braconid parasitoids reared tion in the Republic of South Africa, from wild olive fruit fl y, (A)Psyttalia lounsburyi, (B) Bracon celer and (C) Utetes africanus, as well as braconid parasitoids reared on other fruit fl y species, including (D)Diachasmimorpha Namibia, India, China and other longicaudata, (E) D. kraussii and (F) Fopius arisanus. countries. Parasitoids were shipped to California, and most were studied which serve as reservoirs and contrib- the immature stages are protected from in quarantine to determine the best ute to the fl y’s reinvasion of treated most generalist predators. species for release. Two parasitoid orchards (Collier and Van Steenwyk Before the larva pupates, it creates species — Psyttalia lounsburyi and 2003). Classical biological control — the a thin window on the fruit surface importation of natural enemies from through which it may be exposed to Psyttalia humilis — are now be­ the pest’s home range — offers the best predators. If the fruit is still fi rm, the ing released throughout the state’s opportunity to economically suppress larva will often pupate inside. However, olive­growing regions, and research­ olive fruit fl y populations in these situ- upon fruit maturation most fl y larvae ers are studying their effectiveness. ations. We review ongoing efforts in leave the older fruit, especially in the California to (1) document the natural late summer and fall, and drop to the enemies of olive fruit fl y already pres- ground to pupate in the soil beneath ent, (2) search for and import novel the tree (Tzanakakis 2006). Orsini et al. he olive fruit fl y was fi rst found in natural enemies from other countries (2007) placed fl y puparia (which enclose TSouthern California in 1998 (Rice et and (3) determine the effectiveness the fl y pupa) on the ground in olive al. 2003). Facilitated by longevity and and limitations of these natural enemy orchards and used different barriers the adults’ ability to fl y long distances, species. To date, California scientists around each to distinguish mortality the fl y dispersed rapidly throughout the have received approval from the U.S. levels due to abiotic (e.g., climate) and state. There was little opportunity to at- Department of Agriculture’s Animal biotic (e.g., predators) factors. In an tempt a statewide eradication program, and Plant Health Inspection Service August trial, olive fruit fl y exposed to so current research efforts emphasize (USDA-APHIS) for the release of sev- predators was reduced by about 60% long-term management practices. Bio- eral parasitoid species, and permits are compared to other treatments (fi g. 1). logical control may be a part of this pro- pending for two others (see page 26). Ants (e.g., Formica species) were the gram (Daane and Johnson 2010). most abundant predators on the ground Natural enemies in California How might natural enemies con- and were observed carrying and kill- tribute to the control of olive fruit fl y Although the olive fruit fl y is native ing olive fruit fl y pupae. Predation rates (Bactrocera oleae [Rossi])? Commercial to Africa and Asia (Nardi et al. 2005), vary among orchards, depending on orchards now rely upon a broad- some North American predators and factors such as the species and densi- spectrum insecticide combined with parasitoids may attack it. Insect preda- ties of predators present and the soil a highly attractive bait (Johnson et al. tors such as lady beetles and lacewings depth at which fl y pupae are located. 2006). The effectiveness of insecticide- are found in olive orchards, but because European studies similarly indicate that based programs is, however, limited the fl y’s eggs are embedded underneath arthropods can infl ict substantial mor- by the abundance of roadside and the fruit’s epidermis and the larvae feed tality on olive fruit fl y pupae (Daane residential olive trees in California, deep inside the fruit (Tzanakakis 2006), and Johnson 2010; Tzanakakis 2006). http://californiaagriculture.ucanr.org • JANUARY–MARCH 2011 21 A California-resident parasitoid has A B C also been found attacking olive fruit fl y. The parasitoid is similar to the European Pteromalus myopitae (Graham) (Hymenoptera: Pteromalidae), hence it is currently referred to as Pteromalus species near myopitae (P. sp. nr. myopi- tae). It has been reared from olive fruit fl y collected primarily in coastal coun- ties from San Luis Obispo to San Diego, Pteromalus species near myopitae is resident to California and has been reared from olive fruit although it has also been collected in fl y collected primarily in coastal counties. The adult (A) oviposits onto second- or third-instar fl y larvae, placing an egg (B) on the outside of the larva, where the parasitoid larva (C) develops as a Alameda, Butte, Fresno, Solano and solitary, external parasitoid. Yolo counties. This parasitoid is solitary (one per fl y larva) and feeds externally search started in Africa, where olive of collections). Although P. concolor was on third-instar olive fruit fl y. An olive fruit fl y probably originated and there the only olive fruit fl y parasitoid found fruit fl y survey in San Luis Obispo is a rich diversity of fruit fl y parasi- in Morocco and the Canary Islands, County reported an average parasit- toids. Olive fruit fl y parasitoids were parasitism rates were limited to 14.6% ism level of 2.98% by P. sp. nr. myopitae reported in Africa as early as 1912 by and 2.3%, respectively. Similarly, in the (Kapaun et al. 2010). Parasitism levels the renowned Italian entomologist Republic of South Africa, P. humilis ac- varied considerably, ranging from 0% Filippo Silvestri during surveys for counted for less than 4% of parasitism. to 33% (based on collections of 100 parasitoids of Mediterranean fruit fl y However, in Namibia P. humilis was infested fruit per week) with activ- (Medfl y) Ceratitis( capitata [Wiedemann]) the dominant parasitoid and attained ity highest in August and September. (Wharton 1989). parasitism levels from 18.1% to 35.1%. Because P. sp. nr. myopitae has never Members of the USDA Agricultural In China, few olive fruit fl ies were col- been reported elsewhere, it is likely a Research Service’s European Biological lected, although one (unidentifi ed) North American parasitoid of native Control Laboratory, the California Diachasmimorpha species was obtained, fruit fl ies; it opportunistically parasit- Department of Food and Agriculture, and in India no olive fruit were found izes olive fruit fl y but has never been UC researchers and cooperators ex- on wild olive trees during the 2006 and collected on any native fruit fl y species plored the Republic of South Africa, 2007 explorations (Alan Kirk, personal despite numerous surveys. Namibia, Kenya, La Réunion (an is- communication). land east of Madagascar), the Canary Numerous fruit fl y parasitoids are Foreign exploration Islands, Morocco, Pakistan, India and known to attack other fl ies in the ge- Imported material. Resident natu- China. Collections for “specialists” (i.e., nus Bactrocera. A few of these more ral enemies do not adequately sup- natural enemies that primarily attack “generalist” parasitoids (i.e., natural press olive fruit fl y populations below one species) were made from wild olive enemies that attack numerous spe- damaging levels. For this reason, fruit (Olea europaea ssp. cuspidata) from cies) were also imported to California. California researchers began seeking south to northeast Africa, and from These were Fopius arisanus (Sonan), natural enemies abroad in 2003. The southwest Asia to central China. The Diachasmimorpha kraussii (Fullaway) parasitoids reared from olive fruit fl y and D. longicaudata (Ashmead). All included Psyttalia lounsburyi (Silvestri), were supplied by Russell Messing at a a b 100 Psyttalia concolor (Szépligeti), Psyttalia University of Hawaii, where they had humilis (Szépligeti), Psyttalia ponerophaga been reared on Medfl y. Similarly, colo- 80 (Silvestri), Utetes africanus (Silvestri) and nies of P. humilis maintained on Medfl y 60 Bracon celer Szépligeti. in Guatemala were sent to California, c The greatest yield of parasitoids (% ± SEM) 40 supplied by Pedro Rendon of the USDA came from collections made in South APHIS Plant Protection and Quarantine 20 Africa, Namibia and Kenya (table 1). program (Yokoyama et al. 2008, 2010). Olive fruit y pupae recovered 0 The most common species were Reported efforts. A parasitoid’s Laboratory Total Predator Exposed U. africanus, P. lounsburyi and P. humilis performance in other regions provides control exclusion exclusion (table 1). The highest levels of parasitism insights for researchers when determin- Fig. 1. Mean percentage (± SEM) of olive fruit were found in Kenya collections where ing which natural enemy species should fl y pupae recovered after 4 days (August 2005) P. lounsburyi and U. africanus together be released. P. lounsburyi was identifi ed when held in laboratory control, and placed in parasitized more than 57% of collected nearly 100 years ago as an olive fruit fl y an olive orchard where treatments were “total exclusion” of all natural enemies; “predator fl ies. The next highest parasitism lev- parasitoid and is often reported as the exclusion,” preventing walking predators from els were in collections from Pakistan most effective natural enemy in wild reaching pupae; and “exposed,” allowing both (27.7% parasitism by P.

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