UC Agriculture & Natural Resources Agriculture

Title Biological controls investigated to aid management of fruit in California

Permalink https://escholarship.org/uc/item/0dg816pn

Journal California Agriculture, 65(1)

ISSN 0008-0845

Authors Daane, Kent M Johnson, Marshall W Pickett, Charles H et al.

Publication Date 2011

Peer reviewed

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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 management (IPM) programs for . After fi nd­ ing that resident natural enemies did not provide adequate control, researchers began a worldwide search for , with explora­ Parasitoids imported into California for quarantine studies include braconid parasitoids reared tion in the Republic of South , from wild olive fruit fl y, (A)Psyttalia lounsburyi, (B) celer and (C) Utetes africanus, as well as braconid parasitoids reared on other fruit fl y species, including (D) 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 orchards (Collier and Van Steenwyk Before the 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 ) 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., ) and state. There was little opportunity to at- Department of Agriculture’s biotic (e.g., predators) factors. In an tempt a statewide eradication program, and 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). (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. rates ( 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. preda- ties of predators present and the soil a highly attractive bait (Johnson et al. tors such as lady 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 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) (: ), 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- 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 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) ( 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 ( 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 , 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 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. ponerophaga) and olives of southern Africa (Copeland et fl ying and walking natural enemies access Republic of South Africa (27.8% to 68.0% al. 2004). P. ponerophaga has a similar to pupae. Different letters above each bar indicate signifi cant differences (Tukey’s HSD parasitism by P. humilis, P. lounsburyi, long association with olive fruit fl y test, P < 0.05) (Orsini et al. 2007). B. celer and U. africanus during 3 years and is the only olive fruit fl y specialist

22 CALIFORNIA AGRICULTURE • VOLUME 65, NUMBER 1 known from Pakistan (Wharton 1989). was introduced to the Hawaiian Islands Johnson 2010). Diachasmimorpha kraussii However, no systematic effort has been in the 1940s and provided excellent is native to , attacks a range of made to include these parasitoids in control of Oriental fruit fly Bactrocera( Bactrocera species and has been released European biological control (Wharton dorsalis [Hendel]). It now also contrib- in Hawaii to control Medfly (Bokonon- 1989), presumably because they have utes to Medfly control (Wang, Messing, Ganta et al. 2007); we have found no been difficult to import and rear. Bautista, et al. 2003). Following the reports of its use against , We found no reports of concerted success in Hawaii, F. arisanus was intro- but it has been reported attacking olive efforts to import or manipulate U. af- duced widely to control these and other fruit fly in Israel (C.H. Pickett, personal ricanus for biological control, although tephritid pests in Australia, Central communication). in some South African surveys it is an America, various Pacific and Indian Quarantine nontarget studies abundant olive fruit fly parasitoid in Ocean islands, and the Mediterranean wild olives (Hancock 1989). Similarly, Basin, though not all of these introduc- Before exotic natural enemies are B. celer is often the most commonly re- tions have been as effective. The few released in California, quarantine stud- ported parasitoid attacking olive fruit attempts to establish F. arisanus on olive ies are conducted to determine whether fly in commercial and wild olives in fruit fly in Europe were unsuccessful. or not they will attack insect species South Africa (Neuenschwander 1982), One study reported that F. arisanus other than the intended target (Hoelmer where it achieved parasitism rates as failed to reproduce on olive fruit fly and Kirk 2005). There are more than high as 87%. However, small-scale at- in field cages (Neuenschwander et al. 140 tephritids in California (Foote et al. tempts to rear and/or release B. celer 1983); however, more recent laboratory 1993), including some endemic species in Europe have been unsuccessful work has confirmed that F. arisanus can and others that were brought into the (Wharton 1989). reproduce on olive fruit fly (Calvitti et state for the biological control of weeds. Instead, biological control of olive al. 2002; Sime et al. 2008). Rather than test all of these species, fruit fly has focused on members of the D. longicaudata, a native of Southeast researchers assess parasitoid responses P. concolor species complex, which in- Asia (Wharton 1989), attacks a relatively to fruit fly species found in the three cludes P. concolor from northern Africa wide range of tephritid , including common habitats of fruit fly larvae ­— and P. humilis from sub-Saharan Africa, Medfly, Oriental fruit fly, Caribbean fruits, flower heads and stem galls — to especially after an efficient mass- fruit fly ( suspensa [Loew]) explore their tendency to specialize on rearing method was developed in the and Mexican fruit fly A.( ludens [Loew]) certain host habitats. Tested species are 1950s using Medfly reared on an arti- (Wang and Messing 2004). It has been selected to maximize both practicality ficial diet (Daane and Johnson 2010). used widely for biological control. One (ease of locating and/or rearing hosts) However, P. concolor has not provided attempt was made to rear and release and potential for host acceptance (re- adequate or consistent olive fruit fly it against olive fruit fly in Greece, but it semblance of infested plant structure to control in Europe and, where it has es- did not become established (Daane and olives in shape or size). Therefore, most tablished, repeated mass re- leases are required to boost TABLE 1. Fruit fly and parasitoids reared from field-collected wild olives for importation parasitism rates (Copeland into California, 2003–2007 et al. 2004). Nonetheless, we consider P. concolor and P. Species reared* humilis to be important to Diachas­ screen for use in California Bactrocera Psyttalia Psyttalia Psyttalia Psyttalia Utetes Bracon mi­morpha Country Year reared spp. humilis concolor lounsburyi ponerophaga africanus celer spp. biological control. Their na- tive range spans much of n ...... % ...... northern and eastern Africa Morocco 2004 318 85.4 0.0 14.6 0.0 0.0 0.0 0.0 0.0 (Wharton and Gilstrap 1983) Canary 2004 965 97.7 0.0 2.3 0.0 0.0 0.0 0.0 0.0 and, given the diversity of Islands habitats and en- Pakistan 2005 636 72.3 0.0 0.0 0.0 27.7 0.0 0.0 0.0 compassed, they likely com- La Réunion 2004 700 86.0 0.0 0.0 0.0 0.0 0.0 0.0 14.0 prise several biotypes, or Namibia 2004 597 69.2 18.1 0.0 0.0 0.0 3.7 9.0 0.0 even new species or geneti- 2007 874 58.1 31.3 0.0 9.0 0.0 1.6 0.0 0.0 cally differentiated popula- 2008 3,077 50.0 35.1 0.0 11.0 0.0 3.3 0.6 0.0 tions (Rugman-Jones et al. South Africa 2003 2,218 49.5 3.2 0.0 14.9 0.0 22.8 9.6 0.0 2009), some of which may 2004 794 32.2 2.2 0.0 14.3 0.0 46.1 5.2 0.0 be better suited to control 2005 377 72.2 0.0 0.0 15.1 0.0 12.7 0.0 0.0 olive fruit fly in California Kenya 2005 3,647 42.5 0.0 0.0 35.6 0.0 21.9 0.0 0.0 (Yokoyama et al. 2010). China 2007 438 97.5 0.0 0.0 0.0 0.0 0.0 0.0 2.5 F. arisanus is well known India 2006 0 — — — — — — — — as a generalist parasitoid of 2007 0 — — — — — — — — fruit-infesting tephritids. * Percentages of adult olive fruit fly and parasitoids reared are shown; does not include gall-formers or “unknown” parasitoid species that may Native to Southeast Asia, it have been reared from galls, from other fruit fly species or as hyperparasitoids on primary parasitoids of olive fruit fly.

http://californiaagriculture.ucanr.org • JANUARY–MARCH 2011 23 of the imported parasitoids were either small cages (about 12 square inches) to were limited to the weed biological- sent directly to the UC Berkeley quar- isolate female parasitoids with either control agents — C. succinea (yellow antine facility, or to the collaborating target (olive fruit fly) or nontarget hosts starthistle fly) and P. regalis (Cape ivy laboratory in France and then to the UC for 48 hours in a no-choice test. Target fly) — and no fruit-infesting fly spe- Berkeley facility. and individual nontarget species were cies were tested. In no-choice tests, P. Olive fruit fly belongs to the tephritid then placed together for a choice test ponerophaga adults probed into galls subfamily , which is not native for the next 48 hours. The number of on Cape ivy and produced parasitoid to . California’s native searching events (i.e., parasitoids on offspring from this nontarget host, but and introduced fruit fly species fall the host plant) and probing events (i.e., did not probe or reproduce in yellow into two other subfamilies, parasitoids inserting their to starthistle (table 2). and (Foote et al. 1993). For place an egg into the fruit, flower head P. concolor and P. humilis. P. concolor a nontarget, fruit-feeding Trypetinae, or gall) were recorded during discrete should be viewed as a “species com- researchers selected the native black observation periods. Afterward, the plex,” as previously mentioned. While cherry fly Rhagoletis( fausta [Osten host material was isolated and held for similar, there may be biological differ- Sacken]), which infests fruit of bitter parasitoid or fly emergence. ences that influence their effectiveness cherry. For a flower-head feeder, they in California. For example, researchers Parasitoids and olive fruit fly selected Chaetorellia succinea (Costa), an found that even P. humilis colonies from imported Tephritinae used to control P. lounsburyi. P. lounsburyi was the different locations had slightly differ- yellow starthistle (Centaurea soltitialis L.). only parasitoid tested that probed only ent levels of host specificity (table 2). For a gall-former, researchers selected into infested olives and reproduced However, P. concolor and P. humilis pop- another Tephritinae biological control solely on olive fruit fly (table 2). That ulations tested were able to reproduce agent, regalis (Munro), P. lounsburyi is relatively specialized on on nontarget Cape ivy fly. In other labo- which forms stem galls in Cape ivy. The olive fruit fly is supported by the fact ratory studies, P. concolor was similarly testing of C. succinea and P. regalis ad- that it had been reared only from olive reared from numerous fruit fly species dressed the risk posed to beneficial spe- fruit fly in decades of field collections of (Wharton and Gilstrap 1983). However, cies by the candidate parasitoids. Unless African fruit flies (Copeland et al. 2004; small-cage trials are artificial, and olive stated otherwise, these three species Wharton et al. 2000). In addition, its fruit fly and Medfly are the primary were common to all UC Berkeley quar- geographic range is entirely contained hosts of P. concolor and P. humilis in their antine studies; other nontarget fruit within that of olive fruit fly. native African range (Copeland et al. flies were tested when available. P. ponerophaga. It has been sug- 2004; Wharton et al. 2000). There was some variation in the gested that P. ponerophaga specializes B. celer. B. celer also attacked materials and methods used to test on olive fruit fly because the parasitoid and reproduced on Cape ivy fly, but the different species, but procedures has only been reported from this spe- surprisingly did not reproduce on the were generally as described by Daane cies (Sime et al. 2007). Quarantine- black cherry fly, the fruit-infesting et al. (2008). Briefly, researchers used screening studies of nontarget impacts fly tested with this species (table 2). However, B. celer did probe on host ma- terials for all fruit flies presented except TABLE 2. Host-specificity trials — searching, probing and reproduction by imported parasitoids on olive fruit fly and nontarget fruit fly species currant fly. To date, B. celer has been reported only as a parasitoid of olive Yellow fruit fly and Medfly in field surveys Olive Cherry Apple Cape starthistle Currant (Wharton et al. 2000), with an addi- Parasitoids* fruit fly fly maggot ivy fly fly fly Reference tional, unconfirmed record on Ceratitis Psyttalia concolor (Italy) S/P/R† S/P S/P S/P/R S/P NI Unpublished data nigra Graham. Psyttalia humilis (Kenya) S/P/R S/P S/P S/P/R NI S Unpublished data U. africanus. One of the most com- Psyttalia humilis (Namibia) S/P/R — — S/P/R NI — Unpublished data monly recovered species in the South Psyttalia “unknown sp. A” S/P/R S/R NI S/P/R NI NI Unpublished data African collections, U. africanus was Psyttalia ponerophaga S/P/R — — S/P/R NI — Unpublished data difficult to rear in quarantine. It repro- Psyttalia lounsburyi S/P/R NI NI S NI NI Daane et al. 2008 duced on olive fruit fly, as expected, Diachasmimorpha S/P/R S/P/R S/P S/P/R NI NI Unpublished data but this parasitoid was never observed longicaudata to show any interest (by searching or Diachasmimorpha kraussii S/P/R S/P/R S S/P/R S/P/R S/P Unpublished data probing) in either the target or nontar- Bracon celer S/P/R S/P NI S/P/R S/P NI Nadel et al. 2009 get host during tests (table 2). Utetes africanus R NI — NI NI — Unpublished data The literature indicates that U. africanus Fopius arisanus S/P/R — — NI NI — Sime et al. 2008 has been reared from olive fruit fly, * Target host was olive fruit fly; nontarget hosts were cherry fly (Rhagoletis fausta [Osten Sacken]), (Rhagoletis Medfly, Oriental fruit fly, coffee fruit pomonella [Walsh]), Cape ivy fly (Parafreutreta regalis [Munro]), yellow starthistle fly Chaetorellia( succinea [Costa]) and currant fly ( canadensis [Loew]). fly ( coffeae Bezzi) and natal † S = host plant searched by parasitoid; P = host plant probed by parasitoid; R = parasitoid successfully reproduced in host; fly Ceratitis( rosa Karsch) (Wharton and NI = parasitoid showed no interest in host plant or host during observation period; — = not tested. Gilstrap 1983).

24 CALIFORNIA AGRICULTURE • VOLUME 65, NUMBER 1 Diachasmimorpha species. D. lon- determine the best combination of more time probing olives with larger gicaudata and D. krausii were the most species for release in California’s cli- third-instar maggots (fig. 2A), but more aggressive of the quarantine-screened matically varied olive-growing regions. offspring were produced from olives parasitoids, probing nearly all host Parasitoid host-stage preference, de- containing smaller second- and third- material presented and producing off- velopment time, adult longevity and instar maggots (fig. 2B). Many parasit- spring from nontarget, fruit-infesting fecundity (offspring per female) were oids locate hidden hosts by detecting species as well as the beneficial species determined when colony numbers substrate vibrations. For example, adult (table 2). This result was not surprising permitted these additional quarantine P. concolor are thought to respond more because in total they have been reared studies (table 3). from more than 20 fruit fly species Host-stage preference. Newly in- 8 (Wharton and Gilstrap 1983). fested olives were held for different (A) Parasitoids b F. arisanus. While F. arisanus is con- lengths of time to create fruit with 6 sidered more of a generalist, it is not various olive fruit fly host “age cat- attracted to either C. succinea eggs on egories” (i.e., different immature fly 4 ab yellow starthistle buds, or P. regalis stages). These infested olives were eggs in Cape ivy stems or the associ- placed with mated female parasitoids, 2 a a a ated galls (table 2). These results are and the amount of time the parasitoids Observed on olives consistent with studies in Hawaii that searched and probed on the different 0 show F. arisanus only attacking fruit- age categories was recorded. After the Egg–1st 1st–2nd 2nd–3rd 3rd Late 3rd feeding tephritids (Wang, Bokonon- exposure period, the olives were held Ganta, et al. 2004). The host range in F. to rear either adult parasitoids or flies. 50 arisanus is probably constrained by its These experiments established that P. (B) Adult offspring b 40 host-searching behavior: females are lounsburyi, P. ponerophaga, P. concolor, P. b generally stimulated to search for host humilis, D. longicaudata and D. kraussii 30 eggs by fruit odors; smooth, round fruit were internal parasitoids that preferred b surfaces; and oviposition punctures to oviposit into second- or third-instar 20 ab

left by flies (Wang and Messing 2003). olive fruit fly (table 3). B. celer is an Emergence (%) a Introducing F. arisanus to California external-feeding parasitoid that prefers 10 still requires evidence that native, fruit- late third-instar maggots. F. arisanus is 0 feeding are unlikely to be an egg-larval parasitoid that inserts its Egg–1st 1st–2nd 2nd–3rd 3rd Late 3rd attacked. Sixteen tephritid species na- eggs into olive fruit fly eggs, and the Host stage (instar) tive to California feed in fruit (Foote et parasitoid completes its life cycle in the al. 1993), but at least eight are found at larval olive fruit fly. F. arisanus females Fig. 2. Host-stage preference as mean higher elevations where F. arisanus, a may sometimes lay their eggs in first- percentage (± SEM) of (A) adult female Psyttalia lounsburyi on olives containing tropical species, is unlikely to flourish. instar olive fruit fly. hosts of a given age category during timed Host-stage preference did not always observations and (B) P. lounsburyi offspring Parasitoid studies correlate with reproductive success. that emerged from different host-stage categories. Different letters above each bar Researchers studied the biology This was most clearly seen in trials indicate significant differences (one-way of imported natural enemies to help with P. lounsburyi, where adults spent ANOVA, P < 0.05) (Daane et al. 2008).

TABLE 3. Key biological parameters for parasitoids of olive fruit fly studied in UC Berkeley quarantine facility

Development time Offspring per Parasitoid species tested Host-stage preference (egg to adult) Adult longevity female Reference

...... days ...... n P. lounsburyi Second to third instar 22.8 ± 0.8 (75°F) 61.8 ± 8.2 10.2 ± 2.6 Daane et al. 2008 P. ponerophaga Second to third instar 20.5 ± 1.5 (77°F) 36.2 ± 4.9 18.7 ± 2.9 Sime et al. 2007 P. concolor (Italy) Second to third instar — 68.8 ± 16.4 22.5 ± 5.1 Sime, Daane, Messing, et al. 2006 P. humilis (Kenya) Second to third instar — 77.6 ± 15.3 28.7 ± 4.1 Sime, Daane, Messing, et al. 2006 P. humilis (Namibia) Second to third instar 16.4 ± 0.6 (77°F) 36.0 ± 7.3 35.2 ± 4.1 Daane/Sime, unpublished data P. concolor (South Africa) Second to third instar 18.1 ± 0.4 (77°F) 53.2 ± 6.6 48.8 ± 8.5 Daane/Sime, unpublished data B. celer Third instar 35.5 ± 0.8 (72°F) 51.0 ± 11.7 9.7 ± 7.2 Sime, Daane, Andrews et al. 2006 U. africanus Second to third instar* 20.5 ± 1.0 (75°F) — — Daane/Sime, unpublished data D. longicaudata Second to third instar 20.8 ± 0.9 (77°F) 59.2 ± 5.0 23.6 ± 5.3 Sime, Daane, Nadel, et al. 2006 D. kraussii Second to third instar 21.6 ± 1.7 (77°F) 64.1 ± 7.8 22.7 ± 5.5 Sime, Daane, Nadel, et al. 2006 F. arisanus Egg — — 4.4 ± 0.8 Sime et al. 2008 *Few replicates were completed with U. africanus, and only 10 adults were reared from olive fruit fly during the trial.

http://californiaagriculture.ucanr.org • JANUARY–MARCH 2011 25 relatively cool coastal and hot inland per female F. arisanus when reared on 80 a areas, resulting in different seasonal the Oriental fruit fl y (Ramadan et al. a D. kraussii development of the fl y (Yokoyama et al. 1992). D. longicaudata 2006). Overall patterns of adult longev- 60 Releasing natural enemies ity for all parasitoids tested showed a negative correlation with temperature, California researchers received 40 as shown for the Kenya and Italy colo- USDA-APHIS approval for the release b nies of P. humilis (fi g. 4). of P. lounsburyi and limited release of 20 Lifetime fecundity. Researchers P. humilis; approval is pending for c Mean longevity (days) c studied the parasitoids’ reproductive P. ponerophaga; and permits for the potential by providing newly emerged limited release of F. arisanus are being 0 Honey Olives/ Hosts/ Water Nothing and mated adult females with an over- prepared. To date, P. lounsburyi has been water honey honey water water abundance of infested olives every 2 released and recovered in fi eld-cage days (table 3). All species tested depos- studies, but has not yet been shown to Fig. 3. Adult female Dichasmimorpha kraussii ited most of their eggs during the fi rst overwinter. More work has been done and D. longicaudata longevity given different food provisions. Different letters above each third or half of their life span (fi g. 5). with P. humilis, which is easier to rear, bar indicate signifi cant treatment differences Surprisingly, the two specialists and levels of up to 60% parasitism have (Tukey’s HSD test, P < 0.05) (Sime, Daane, (P. lounsburyi and P. ponerophaga) had been reported from cage studies (Wang, Nadel, et al. 2006). the lowest lifetime fecundity of the Johnson, Daane, Yokoyama 2009; larval endoparasitoids, which develop Yokoyama et al. 2008, 2010). However, strongly to the third than the second in- inside the host (table 3). One hypothesis as with P. lounsburyi, there is no clear star because the larger instar produces to explain these low fecundity rates evidence to date that P. humilis can stronger or more frequent vibrations concerns the relative lengths of their while feeding (Canale and Loni 2006). (see below). Another expla- However, the third-instar olive fruit nation concerns the chemical cues used 120 fl y maggots feed deeper in olives and to orient to and identify host larvae and Kenya, female may be beyond the reach of the short the host/plant complex. Domestic ol- 100 Kenya, male P. lounsburyi ovipositor (less than 2 ives differ chemically from wild olives. Italy, female millimeters). These differences could disrupt the 80 Italy, male Development time . The egg-to-adult parasitoid’s host-searching, host- 60 developmental rates of P. lounsburyi, identifi cation or ovipositional behav- P. ponerophaga, P. concolor, D. kraussii and iors, or impede larval development. 40 D. longicaudata were relatively similar, Quarantine studies also reported Adult longevity (days) about 22 days at constant temperatures low lifetime fecundity for B. celer, the 20 near 77°F (25°C), while B. celer required external parasitoid, and F. arisanus, the 0 nearly 40% more time (table 3). Olive egg-larval parasitoid (table 3), although 50 59 68 77 86 95 fruit fl y requires about 23 days at 77°F in each case researchers suggest that Temperature (°F) (25°C), suggesting that (except for B. experimental conditions may have Fig. 4. Adult P. humilis longevity declined with celer) these parasitoids could have gen- negatively infl uenced natural egg de- increasing constant temperature for each eration times similar to olive fruit fl y. position. In the UC Berkeley quarantine gender and culture. Within each culture, no Adult longevity. When provisioned studies, researchers found up to 80% signifi cant differences were found between with water and honey, examined adult mortality of olive fruit fl y eggs exposed female and male longevity at any temperature tested (Sime, Daane, Messing, et al. 2006). parasitoid species lived 36 to 78 days at to F. arisanus (Sime et al. 2008). Similar temperatures around 77°F (25°C) (table fi ndings have previously been reported 3). For all tested species, adults lived on olive fruit fl y (Calvitti et al. 2002) 10 for less than 5 days without food, as and other hosts (Moretti and Calvitti 8 shown for D. longicaudata and D. kraussii 2003). Most likely this direct mortality

(fi g. 3). For most species studied, there results from the egg being repeatedly 6 was also a reduction in longevity when probed (i.e., stabbed) by the F. arisanus adults were provided hosts in infested ovipositor. Olive fruit fl y lays a single 4 olives, suggesting that the parasitoids egg per fruit puncture, whereas the expended energy while handling hosts typical host of F. arisanus, the Oriental 2 Offspring per female Offspring and that the parasitoids were able to fruit fl y, deposits up to 100 eggs per distinguish host-infested olives from puncture (Ramadan et al. 1992). The 0 those lacking hosts. tendency of F. arisanus to probe repeat- 0 10 20 30 40 50 Time (days) Tolerances for high and low tempera- edly within an oviposition puncture tures may be critical for parasitoid es- may be an evolutionary consequence Fig. 5. Mean lifetime production of offspring tablishment in California because olive of its use of this host. By comparison, (± SEM) produced by P. humilis from a Kenyan fruit fl y infestations are found in both more than 100 progeny can be obtained culture (Sime, Daane, Messing, et al. 2006).

26 CALIFORNIA AGRICULTURE • VOLUME 65, NUMBER 1 establish and thrive without repeated augmentation. There is a risk with the release of each natural enemy species that some nontarget species will be attacked, but the benefits often outweigh the risks (Hoddle 2004). Also, not all pest species are prime targets for classical biological control — there are potential problems with olive fruit fly and natural enemy biology that may limit the levels of con- trol achieved. Seasonal host availability. The olive Ripe wild olives, left, collected in Africa, where olive fruit fly is considered to be native, are much fruit fly’s survival is limited in regions smaller than the cultivated European varieties used throughout the world. Right, springbok and kudu graze among wild olive trees on a South Africa hillside. The African parasitoids that with high or low temperature extremes specialize on olive fruit fly found in small wild olives tend to have relatively short ovipositors (Wang, Johnson, Daane, Opp 2009). The that may not reach fly maggots deeper in the pulp of cultivated olives. fruit also may not be developed enough for olive fruit fly to survive early in in cultivated olives, B. celer. with its Repeated sprays of GF-120 Naturalyte the summer; young, hard fruit are not much longer ovipositor, predominates, NF Fruit Fly Bait (Dow AgroSciences, preferred for oviposition (Burrack and and the other species tend to be rare Indianapolis, Ind.) are used to control Zalom 2008). Moreover, olive fruit fly (Neuenschwander 1982). In the UC olive fruit fly. Although this spinosad populations are scarce in some inte- Berkeley quarantine studies, both D. bait is classified as a reduced-risk ma- rior valley regions with high summer longicaudata and D. kraussii reproduced terial, its frequent use may disrupt temperatures (Wang, Johnson, Daane, well on cultivated olives, and these biological control. Nadel et al. (2007) Nadel 2009) (see page 29). These facts more generalist parasitoids have very investigated the impact of GF-120 on suggest that parasitoid survival might long ovipositors (Sime, Daane, Messing, a green lacewing (Chrysoperla carnea also be difficult in some regions where et al. 2006). Among the favorable char- [Stephens]), and showed that ingestion their host, the olive fruit fly larvae, is acteristics of F. arisanus as a parasitoid clearly poses some risk to lacewing scarce during some seasonal periods. of B. oleae are its relatively long oviposi- populations due to adult mortality and Wild versus domestic olives. The tor and the fact that it usually oviposits reduced fecundity. Laboratory studies domestic olive is a distinct subspecies into eggs. Both features may help it cir- indicated that several important braco- of wild olive, which has smaller fruit cumvent the difficulties encountered by nid parasitoids of fruit flies — F. arisa- than most cultivated olives. As a result, some larval parasitoids attacking nus, Diachasmimorpha tryoni (Cameron) fly maggots tunnel deeper inside the B. oleae in larger olive cultivars. and Psyttalia fletcheri (Silvestri) — would larger domestic olive. The ovipositors Natural enemy interactions. For best not feed on fresh GF-120 residues, but of specialized parasitoids (P. lounsburyi results natural enemies should coexist, when the insecticide was directly ap- and P. ponerophaga) are too short to but sometimes they interfere with each plied there were high mortality rates reach fly maggots feeding deep within other. For example, the unexpected (Wang et al. 2005). the larger olives (Sime et al. 2007; Wang, appearance of P. sp. nr. myopitae could Expectations in California Johnson, Daane, Yokoyama 2009; Wang, potentially create a conflict with classi- Nadel, Johnson, et al. 2009). The length cal biological control efforts. Parasitoids Biological control can be a practical, of the ovipositor relative to the depth of that immobilize the host, including P. safe and economically effective means the maggot within the fruit apparently sp. nr. myopitae and B. celer, may have a of fruit fly control, and its importance limits the biocontrol agent’s ability to competitive advantage over larval para- continues to grow in regions where pes- successfully parasitize certain hosts, a sitoids that allow the host to continue ticide use is less desirable (e.g., sustain- problem that has been well documented to develop and grow after parasitoid able agriculture) or more restricted (e.g., for other fruit fly parasitoids (Sivinski et oviposition, such as Psyttalia species. urban trees). The research programs al. 2001). Therefore, African parasitoids In quarantine experiments, research- that we describe provide background of olive fruit fly may fail to success- ers found that the egg-larval parasitoid information on natural enemy biology, fully establish on fruit flies in fleshier F. arisanus prevailed in competition and identify specific natural enemies European cultivars, because their short against two species of larval-pupal par- for importation and evaluation, and for ovipositors are adapted for foraging in asitoids, D. kraussii and P. concolor (Sime possible release into California. Over small, wild, African olives. et al. 2008). The intrinsic competitive su- the coming years, researchers will bet- Surveys in wild and cultivated periority of F. arisanus over larval-pupal ter understand the level of controls African olives provide support for parasitoids must be taken into consider- expected from imported natural en- this hypothesis. P. lounsburyi, U. afri- ation for its use in California. emies, and will improve IPM programs canus and B. celer are most commonly Insecticides and biological control. to integrate biological controls with reared from wild olives (Copeland et al. Insecticide use affects biological con- the insecticides currently used in olive 2004; Neuenschwander 1982), whereas trol programs (Mills and Daane 2005). management.

http://californiaagriculture.ucanr.org • JANUARY–MARCH 2011 27 X.-G. Wang is Associate Specialist, Department of Director, USDA Agricultural Research Service, Eu- K.M. Daane is Cooperative Extension Specialist, Environmental Science, Policy and Management, ropean Biological Control Laboratory, Montpellier, Department of Environmental Science, Policy UC Berkeley; H. Nadel is Supervisory Entomolo- France. and Management, UC Berkeley; M.W. Johnson is gist, U.S. Department of Agriculture (USDA), We thank CDFA for funding this review; and Cooperative Extension Specialist and Entomolo- Animal and Plant Health Inspection Service, Plant the California Olive Committee, CDFA Biological gist, UC Riverside; C.H. Pickett is Research Ento- Protection and Quarantine program, Buzzards Control Program (in collaboration with USDA) and mologist, Biological Control Program, California Bay, MA; J.W. Andrews Jr. was Quarantine Man- USDA Cooperative State Research, Education, and Department of Food and Agriculture (CDFA); K.R. ager, College of Natural Resources, UC Berkeley; Extension Service’s Pest Management Alternatives Sime is Assistant Professor, SUNY Oswego, N.Y.; and K.A. Hoelmer is Research Entomologist and Program for funding olive fruit fly research.

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28 CALIFORNIA AGRICULTURE • VOLUME 65, NUMBER 1