Prospects for improving biological control of olive fruit fly, Bactrocera oleae (Diptera:...

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Prospects for improving biologicalcontrol of olive fruit fly, Bactroceraoleae (Diptera: Tephritidae), withintroduced parasitoids (Hymenoptera)Kim A. Hoelmer a , Alan A. Kirk a , Charles H. Pickett b , Kent M.Daane c & Marshall W. Johnson da USDA ARS, EBCL, Campus International de Baillarguet,Montferrier sur Lez, 34980, Franceb State of California, Food & Agriculture, 3288 Meadowview Rd,Sacramento, CA, 95832, USAc University of California, Berkeley, Environmental Science, Policyand Management, Berkeley, CA, 94720, USAd University of California, Riverside, Entomology, Riverside, CA,92521, USA

Available online: 14 Jun 2011

To cite this article: Kim A. Hoelmer, Alan A. Kirk, Charles H. Pickett, Kent M. Daane & MarshallW. Johnson (2011): Prospects for improving biological control of olive fruit fly, Bactrocera oleae(Diptera: Tephritidae), with introduced parasitoids (Hymenoptera), Biocontrol Science andTechnology, 21:9, 1005-1025

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FORUM ARTICLE

Prospects for improving biological control of olive fruit fly, Bactroceraoleae (Diptera: Tephritidae), with introduced parasitoids (Hymenoptera)

Kim A. Hoelmera*, Alan A. Kirka, Charles H. Pickettb, Kent M. Daanec and

Marshall W. Johnsond

aUSDA ARS, EBCL, Campus International de Baillarguet, Montferrier sur Lez, 34980 France;bState of California, Food & Agriculture, 3288 Meadowview Rd, Sacramento, CA 95832, USA;cUniversity of California, Berkeley, Environmental Science, Policy and Management, Berkeley,CA 94720, USA; dUniversity of California, Riverside, Entomology, Riverside, CA 92521, USA

(Received 6 March 2011; returned 21 April 2011; accepted 4 June 2011)

Olive fruit fly is a key pest of olive and consequently a serious threat to olive fruitand oil production throughout the Mediterranean region. With the establishmentof Bactrocera oleae in California a decade ago, interest was renewed in classical(introduction) biological control of the pest. Here we discuss the prospects ofidentifying natural enemies of B. oleae in Africa and Asia that may help reduceB. oleae populations in California and elsewhere. Based on the current under-standing of Bactrocera phylogenetics, early opinions that B. oleae originated inAfrica or western Asia rather than the Mediterranean region or the Near East aretaxonomically and ecologically supportable. Closely related to cultivated olive,the wild olive Olea europaea cuspidata is widely distributed in southern andeastern Africa, the Arabian Peninsula, and eastwards into Asia as far assouthwestern China. Little is known regarding the biology and ecology ofB. oleae in Africa and eastern Asia, especially in wild olives. While the diversity ofparasitoids of B. oleae in the Mediterranean region is low and unspecialized, adiverse assemblage of parasitoids is known from B. oleae in Africa. Conversely,regions in Asia have remained largely unexplored for B. oleae and its naturalenemies.

Keywords: olive fruit fly; Bactrocera oleae; natural enemies; parasitoids; biologi-cal control; foreign exploration

1. Introduction

The olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), is the most serious

pest of cultivated olives (Olea europaea ssp. europaea L.) throughout much of the

Mediterranean basin (southern Europe, the Near East, and northern Africa) where

the majority of the world’s olives are produced (Crovetti 1997; Costa 1998;

Tzanakakis 2006). Annual crop losses from insect pests of olive fruit have been

estimated to be at least 15%, equivalent to 800 million US dollars (Montiel Bueno

and Jones 2002); average crop losses due specifically to B. oleae range from 5 to 15%

in different countries when control measures are taken to an average of 40�50% if left

unmanaged. Losses may be much higher with susceptible cultivars (Haniotakis

2005). Approximately a decade ago it was accidentally introduced into Mexico and

*Corresponding author. Email: [email protected]

Biocontrol Science and Technology,

Vol. 21, No. 9, 2011, 1005�1025

ISSN 0958-3157 print/ISSN 1360-0478 online

This work was authored as part of Contributor’s official duties as an employee of the United States Government and is

therefore a work of the United States Governement. In accordance with 17 U.S.C. 105 no copyright protection is available

for such works under U.S. law.

DOI: 10.1080/09583157.2011.594951

http://www.informaworld.com

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http://www.informaworld.com

California, where olive production occurs in climates similar to the Mediterranean

region, and it rapidly became established throughout the olive-producing regions of

California (Rice 2000). Prior to the introduction of B. oleae into California, where

nearly all of the olives in the US are produced, the olive industry was generally free of

significant pests due to biological controls and cultural management methods that

had been developed for invasive scale insects (Daane, Rice, Zalom, Barnett, and

Johnson 2005). Olive trees were introduced to California hundreds of years ago bySpanish settlers (Taylor 2000) and since that time they have become extensively

distributed throughout rural and urban areas, where they serve as reservoirs for

continual re-invasion by B. oleae populations into commercial groves. Because of the

rapid spread of the fly in California, eradication was not an option, and the use of

insecticides to control flies in urban and wild areas was both expensive and

environmentally undesirable. Although at least one previously unknown parasitoid

was discovered attacking the fly in California (Kapaun, Nadel, Headrick, and

Vredevo 2010), surveys showed that indigenous natural enemies were incapable of

effectively suppressing B. oleae (CP, unpublished data). Olive fruit fly is currently

regarded as a serious threat to olive production in California (Rice 2000; Collier and

van Steenwyk 2003; Daane and Johnson 2010). In the absence of effective biological

control agents olive growers rely primarily on treatments with spinosad insecticide in

protein food baits (Johnson et al. 2006); although these are less environmentally

disruptive than organophosphate cover sprays, they require as many as a dozen

applications per year (Burrack, Connell, and Zalom 2008). Growers in Mediterra-

nean regions also rely on cover sprays, or baited insecticidal traps to reducepopulations of adults (Haniotakis 2005). Baits sometimes incorporate pheromones;

mass trapping with baited traps is believed to have some potential to control low

populations (Petacchi, Rizzi, and Guidotti 2003; Speranza, Bellocchi, and Pucci

2004; Miranda, Miquel, Terrassa, Melis, and Monerris 2008). Effective male lures

that are helpful in managing other Bactrocera species are not currently available for

B. oleae.

Efforts to incorporate biological control into management of B. oleae were

initially begun in southern European countries. Indigenous parasitoids do not

significantly impact B. oleae populations in the region. A braconid larval-pupal

parasitoid, Psyttalia concolor (Szepligeti) was introduced into Europe in the early

1900s from North Africa but failed to widely establish in the temperate-climate areas

of the fly’s range (Crovetti 1997; Miranda et al. 2008). Efforts to utilize P. concolor in

augmentative release programs were tested extensively, but proved too expensive

for widespread adoption. Exploration for other parasitoids of B. oleae was

conducted in southern and eastern Africa (Silvestri 1914a, 1914b; Greathead 1976;

Neuenschwander 1982), but attempts to establish the African species in southernEurope were unsuccessful for reasons that will be discussed further below. Thus, olive

fruit fly management in Mediterranean olive production zones has for many decades

been based largely on cultural controls, insecticides, insecticide-baits and traps

(Aversenq 2002; Neuenschwander, Bigler, Delucchi, and Michelakis 1983).

Olive fruit fly has been considered of lesser importance in South Africa than in

the Mediterranean area although the climate is similar. It was long supposed locally

that natural enemies held the pest in check (Annecke and Moran 1982; Costa 1998).

In fact, in commercial olive orchards, cover sprays are not widely used due to the risk

of upsetting biological control of other olive insects such as black scale and olive

1006 K.A. Hoelmer et al.

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psylla (Annecke and Moran 1982), and typically the fly is managed with a few early

season insecticide-bait sprays. Olive fruit fly is most often a problem in areas

receiving summer rainfall, especially where the humidity is high, while drier

provinces experience fewer problems with B. oleae (Costa 1998). In the West Cape,high levels of natural enemy activity have been reported in commercial groves

(Neuenschwander 1982; Costa 1998), but the reasons for the increased activity

(inherent efficiency of the parasitoids, influence of the climate, etc.) are unknown

because this subject has received minimal attention in South Africa. Olive fruit fly

also occurs in other areas where its status as a pest is either uncertain or

unimportant, such as the Artvin province of Turkey adjacent to Georgia (Guclu,

Hayat & Ozbek 1995).

With the establishment of B. oleae in California, there was a renewed interest inclassical biological control of the pest. In this article, we review and discuss

contemporary efforts at foreign exploration and the prospects of finding new, non-

indigenous natural enemies of B. oleae in Africa and Asia that may be helpful in

reducing B. oleae populations in California and elsewhere.

2. Distribution of host olives

The genus Olea includes more than 40 plant species distributed from southern Africanorthwards to southern Europe, and eastwards into Asia, with the highest species

diversity in east-central Africa and southeastern Asia. Various theories about the

origins of O. europaea in the Mediterranean region have been proposed, but there is

abundant archaeological evidence that cultivation arose 5000�6000 years ago from

wild progenitors in the eastern Mediterranean basin (Browicz and Zielinski 1990;

Zohary 1994). Evidence of human use, including olive pits and relics associated with

oil usage, has been found associated with human dwellings as long as 8000�9000

years ago. Wild forms of O. europaea ssp. europaea are commonly referred to as‘oleasters’ and are often assumed to be simply cultivated olives that have gone feral.

Oleaster fruit tends to be more elongate in shape and smaller than most cultivated

varieties. However, the existence of genetically distinct, wild indigenous forms at a

number of sites throughout the western Mediterranean region was recently

documented (Lumaret and Ouazzani 2001), lending support to the idea of a long

residency of ancestral O. europaea in the region clearly distinct from subspecies

occurring in southern Africa and Asia (Besnard, Rubio de Casas, and Vargas 2007).

Both forms occur throughout the Mediterranean basin (Figure 1) and are regardedas classic indicators of ‘Mediterranean’ climates in other parts of the world (Zohary

1994; Dallman 1998). Several other subspecies with highly localized disjunctive

distributions in the Canary Islands, the Madeira archipelago, Morocco, and in the

Sahara are also recognized, such as O. e. ssp. cerasiformis G. Kunkel & Sunding

(Green 2002).

Closely related to cultivated olive, Olea europaea ssp. cuspidata (Wall ex G. Don)

Cif. (�O. africana Mill., chrysophylla Lam. or verrucosa (Willd.) in Africa and

O. ferruginea Royle in Asia in older literature) is widely distributed in southern andeastern Africa, the Arabian peninsula and eastwards into Asia as far as southwestern

China (Figure 1); it is often found in proximity to cultivated olives in these regions

(Palgrave 1977; Green and Kupicha 1979; Green and Wickens 1989; Browicz and

Zielinski 1990; Green 2002). The tree occurs in a wide variety of habitats on rocky

Biocontrol Science and Technology 1007

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hillsides, along stream banks and in woodlands, and extends from low elevations

near sea level to 2500�3000 m along the flanks of the Himalaya into southwestern

China. Its distribution in Africa and Asia parallels that of B. oleae but includes areaswhere the fly has not previously been recorded in literature, such as Nepal and

China. Because the distribution of O. europaea ssp. cuspidata is relatively widespread

it seems likely that the fly occurs in places where it has not been reported. It is also

likely that the native range of B. oleae lies somewhere within the distribution of its

wild hosts. The rich diversity in recorded natural enemies from southern and eastern

Africa, compared with the relatively depauperate fauna in the Mediterranean basin,

also argues against a Mediterranean or Near Eastern origin for B. oleae. We will

discuss this further below.

3. Association of Bactrocera oleae with olives

Bactrocera oleae was described in 1790 by both Rossi and Gmelin (priority of

authorship is now attributed to Rossi), although it has been recognized as an olive

pest since antiquity. Fly larvae infesting olives that were mentioned by Pliny theElder two thousand years ago in his Treatis on Natural History (Book 17, on the art

of planting trees and vines) were clearly olive fruit flies. Thus, the fly is not a

historically recent invader of cultivated olives in the Mediterranean region, where the

crop has long been an integral part of agriculture, commerce, and culture in the

Figure 1. Natural (unmanaged) distribution of Olea europaea ssp. europaea and O. e.

cuspidata (areas in black). Due to its association with these hosts (discussed in text), the

distribution of Bactrocera oleae is essentially concurrent. The apparent discontinuous

distribution in Asia and Africa is probably due partly to lack of records in some regions.

Distribution information compiled primarily from Green and Wickens (1989) and Browicz

and Zielinski (1990), and other sources.


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region. This long historical association led to a common assumption that B. oleae

itself was indigenous to the Mediterranean region or the Near East. However, besides

its distribution throughout the Mediterranean basin and the Canary Islands, B. oleae

has also been reported in South Africa, Kenya, Eritrea, Sudan, India, and Pakistan(Munro 1984). In their treatise on pestiferous tephritids, Carroll et al. (2002) listed

the distribution of B. oleae as Eritrea, Kenya, Angola, South Africa, possibly Sudan,

and North Africa, but noted it as ‘introduced’ in the Mediterranean region and Asia.

Throughout its range it is known only from fruit of O. europaea ssp. europaea (which

includes both commercial olives and wild or naturalized ‘oleasters’) and the related

African and Asian wild olive, O. europaea ssp. cuspidata (Carroll et al. 2002).

Bactrocera oleae was also reared from recent collections in the Canary Islands from

O. e. ssp. guanchica P. Vargas et al. and in Morocco from O. e. ssp. maroccana

(Greuter and Burdet) P. Vargas et al. (AK, unpublished data). This reported host

specificity is convincing given the extensive literature on management of the fly and

the comprehensive surveys of potential host fruits of related species of Olea and

other Oleaceae in Kenya (Copeland, White, Okumu, Machera, and Wharton 2004)

and of a wide range of host plants of tephritid species distributed widely throughout

Africa (Silvestri 1914b; Munro 1984).

The olive fruit fly has not been reported from any other African Olea

species, many of which are sympatric in distribution so they would be expected tobe hosts if they were suitable for development of B. oleae. A related tephritid,

Bactrocera biguttula (Bezzi), has been recorded from O. europaea ssp. cuspidata,

O. woodiana Knobl., O. capensis L. and Chionanthus foveolata (E. Meyer) Stearn

(Neuenschwander 1982; Munro 1984; Mkize, Hoelmer and Villet 2008). The closely

related Bactrocera munroi White was recorded from O. europaea ssp. cuspidata and

O. welwitschii (Knobl.) Gilg & Schnellenb. in Kenya (Copeland et al. 2004). Very

little is known regarding the biology and ecology of B. oleae in Africa, especially in

wild olives (Greathead 1976; Annecke and Moran 1982; Costa, pers. comm., March2001), and even less in central and eastern Asia, where B. oleae has been recorded

only from NW India (now Pakistan) (Pruthi 1937, Silvestri 1916). Geographic gaps

in the reported distribution of B. oleae in Asia could well be the result of inadequate

sampling of wild olives in areas where commercial olives are not cultivated. Recent

exploratory surveys in China located small populations of B. oleae (Pickett and Kirk

2006).

4. Distribution and center of diversity of Bactrocera species

Widely cited in the literature as Dacus oleae Gmelin or D. oleae Rossi until recently,

the species was placed in Bactrocera in a revision by Drew (1989). Based on the

current understanding of Bactrocera phylogenetics, early opinions that B. oleae

originated in Africa or western Asia rather than the Mediterranean region or the

Near East (Silvestri 1915; Annecke and Moran 1982; Clausen 1978) are taxonomi-

cally and ecologically supportable. The center of diversity of Bactrocera, a large

genus with ca. 500 recognized species, is in southeastern Asia. Only a dozen or sospecies occur in Africa (some of which were introduced) and only three, B. oleae,

B. biguttula, and B. munroi, are known to have host associations with Olea in Africa,

suggesting they may be indigenous. Notably, the only species of the genus occurring

in Europe and the Mediterranean region is B. oleae. In Australia, the highly


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polyphagous B. tryoni (Froggatt) was reported infesting O. europaea ssp. europaea

that was introduced into Australia, and B. nigra (Tryon) infests O. paniculata R. Br.

that is native to Australia (White and Elson-Harris 1994). Raspi and Canale (1998)

pointed out that only B. oleae occurs widely in subtropical climates characterized bydry (‘Mediterranean’) summers, whereas damp subtropical climates are typical for

the rest of the genus.

Information regarding the population structure and genetic variability present in

populations of B. oleae demonstrated significantly more genetic diversity among

African populations than Mediterranean populations (Nardi, Carapelli, Dallai,

Roderick, and Frati 2005; M.C. Bon, pers. comm., May 2011), which suggests that

an African origin is more likely than one in the Mediterranean region. Recent

analyses of B. oleae mitochondrial genomes further support the idea that theevolutionary histories of O. europaea and B. oleae are closely linked (Nardi et al.

2010). Populations from Pakistan appear distinct from African populations; few

Asian populations of B. oleae have heretofore been available for comparative study.

5. Aspects of B. oleae biology relating to host availability

Individual fruit of O. europaea ssp. cuspidata are notably smaller than oleaster fruit,and are much smaller than cultivated olives. Fruit of O. e. cuspidata are usually

round, 5�6 mm in diameter, with pulp (mesocarp) thickness of only about 1�2 mm,

thus only a small amount of pulp is available for ingestion by a fly larva feeding in

the fruit (Wang et al. 2009b). Although multiple ovipositions will occur under

conditions of high fly densities and limited supply of host fruit (such as may occur in

some habitats highly favorable to B. oleae), female flies will often lay just one egg per

fruit (Crovetti 1997). A habit of single egg ovipositions rather than large egg clutches

would clearly be adaptive for flies in regions where only very small fruits weretypically available.

It has been noted that B. oleae females exhibit two reproductive peaks, April and

October, in southern Europe, which are determined by their response to changes in

photoperiod and has been suggested as an adaptation for surviving dry summers

(Raspi, Canale, and Felicioli 1997; Raspi, Iacono, and Canale 2002). Fruit on

cultivated olives is rare or absent during April in the Mediterranean region (and also

in California) when the first reproductive peak occurs and is not available until early

fall. This may result in extended periods when the bulk of the B. oleae populationsurvives as adults, creating a period with few fly larvae available for the parasitoids.

In contrast, in regions such as southern Africa where large populations of wild olives

may carry fruit at different times, a bimodal peak in egg availability would be

adaptive, allowing an additional generation early in the year (Raspi et al. 2002) and

providing continuous availability of B. oleae larvae for the parasitoids.

6. Natural enemies of B. oleae

6.1 Parasitoids

In southern Europe, five parasitoid species are commonly recorded from B. oleae

(Delucchi 1957; Laudeho, Canard, and Liaropoulos 1979): four chalcidoid wasps:

Eupelmus urozonus Dalman (Hym.: Eupelmidae), Pnigalio mediterraneus Ferriere &


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Delucchi (Hym.: Eulophidae), Eurytoma martellii Domenichini (Hym.: Eurytomi-

dae) and Cyrtoptyx latipes (Rondani) (Hym.: Pteromalidae), and the single imported

braconid, P. concolor (Table 1). Except for E. martellii, the chalcidoid species are not

specific to B. oleae and are somewhat to highly polyphagous, attacking unrelated

hosts in several different insect orders. This lack of coadapted, relatively specific

enemies also argues for an origin of B. oleae outside of the Mediterranean region.

Eupelmus urozonus is also a facultative hyperparasitoid of other parasitoids includingP. agraules (Walker) (Noyes 2011). Pnigalio epilobii Boucek, Teleopterus erxias

Walk., and Pachycrepoideus vindemiae (Rondani) have also been noted (Neuensch-

wander et al. 1986), but appear less common than the four previously mentioned

chalcidoids. This complex does not provide effective biological control of the fly

(Bigler, Neuenschwander, Delucchi, and Michelakis 1986). The opiine braconid

P. concolor was discovered in Tunisia in 1910 and was repeatedly introduced into

Europe (Delucchi 1957), but without subsequent widespread establishment. Unlike

most of the chalcidoids, it is apparently restricted to attacking tephritid flies; in

addition to B. oleae, it also attacks the tephritids Ceratitis capitata (Wiedemann),

Carpomya incompleta (Becker), and Capparimyia savastani (Martelli) in North

Africa and Sicily. In northern Africa, these alternate hosts may help it to survive

periods when B. oleae and olives are unavailable.

The natural enemy fauna attacking B. oleae in the eastern Mediterranean region

(Israel, Lebanon, and Jordan) is less well documented than in Europe, but several

reports list the presence of the same or closely related species of chalcidoids found inEurope, as well as P. concolor (Mechelany 1969; Mustafa and Al-Zaghal 1987; El-

Heneidy, Omar, El-Sherif, and El-Khawas 2001). Psyttalia concolor and Tetrastichus

sp. were reported to be the two most common species in Lebanon (Mustafa and Al-

Zaghal 1987), and Abdelwali (1993) reported that parasitism by P. concolor reached

peak levels of 12�16% in mid-September. In Egypt, all parasitoids found in recent

surveys other than P. concolor were recorded there for the first time. Parasitism levels

reached 39 and 11% by P. concolor and P. agraules, respectively (El-Heneidy et al.

2001). In Israel, P. concolor and C. latipes were the two most common parasitoids

found attacking B. oleae, as reported by Avidov and Harpaz (1969); since that survey,

Diachasmimorpha kraussii (Fullaway), which was previously released and established

in Israel against C. capitata (Mediterranean fruit fly), has also been recorded

attacking B. oleae (Argov, Tabic, Hoelmer, Kuslitzky, and Zchori-Fein 2008). The

relative abundance of these various parasitoids varies throughout regions according

to time of season, climate zone, and other factors such as olive variety.

Silvestri (1914b), an early proponent of the idea that B. oleae probably originated

in Africa or Asia, traveled to southern Africa during 1912�1913, where he recoveredfive parasitoid species from B. oleae as part of his extensive survey of tephritid

natural enemies in west and south Africa, and one species from medfly that could be

reared on B. oleae, none of which occurred in the Mediterranean (Table 1). In 1914

he traveled to Eritrea (Ethiopia) where he recovered 14 species (Table 1) of B. oleae

parasitoids (Silvestri 1914a, 1915). Neuenschwander (1982) visited South Africa

again in 1981. He reared many of the same species found by Silvestri, and in

addition, small numbers of the encyrtid Tachinaephagus zealandicus Ashmead and a

single specimen of a Tetrastichus sp. In his survey, Bracon celer Szepligeti was the

most abundant species reared. Other attempts were made to obtain additional

material in South Africa (Monaco 1976) and Kenya and Ethiopia (Greathead 1976)


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Table 1. Parasitoids recorded in literature from Bactrocera oleae prior to its invasion of

California.

Species Family Biology (known or presumed)

African explorations of Prof. Silvestri

(Silvestri 1914b, 1915)

Ethiopia

Utetes (Opius) africanus (Szepligeti) Braconidae Egg or larval-pupal endoparasitoid

Psyttalia (Opius) dacicida Silvestri Braconidae Larval-pupal endoparasitoid

Bracon celer Szepligeti Braconidae Larval ectoparasitoid

Triaspis (Sigalphus) daci (Szepligeti) Braconidae Record thought to be doubtful

(TAMU)

Eupelmus afer Silvestri Eupelmidae Larval & pupal

ectoparasitoid (TAMU)

Halticoptera daci Silvestri Pteromalidae Larval or egg larval endoparasitoid

(TAMU)

Mesopolobus (Eutelus) modestus

(Silvestri)

Pteromalidae ?

Cirrospilus (Atoposoma) variegatus

(Masi)

Eulophidae Regarded as a dubious record by

Neuenschwander (1982)

Closterocerus (Achrysocharis)

formosus erythraea Westwood

Eulophidae Larval parasitoid

Closterocerus (Teleopterus)

notandus (Silvestri)

Eulophidae ?

Entedon (Metriocharis) viridis

(Silvestri)

Eulophidae ?

Entedon (Metriocharis) atrocyanea

(Silvestri)

Eulophidae ?

Euderus (Allomphale) cavasolae

(Silvestri)


Tetrastichus maculifer Silvestri Eulophidae ?

South Africa

Utetes (Opius) africanus (Szepligeti) Braconidae Larval-pupal endoparasitoid

Psyttalia (Opius) dacicida (Silvestri) Braconidae Larval-pupal endoparasitoid

Psyttalia (Opius) lounsburyi

(Silvestri)

Braconidae Larval-pupal endoparasitoid


Triaspis (Sigalphus) daci (Szepligeti) Braconidae TAMU doubtful record

Coptera (Galesus) silvestrii (Kieffer) Diapriidae Pupal parasitoid of Ceratitis; lab

reared on B. oleae

South African surveys of

Neuenschwander (1982)


Utetes (Opius) africanus (Szepligeti) Braconidae Larval-pupal endoparasitoid

Psyttalia (Opius) dacicida (Silvestri) Braconidae Larval-pupal endoparasitoid

Psyttalia (Opius) lounsburyi

(Silvestri)


Microdontomerus sp. Torymidae ?

Tetrastichus sp. Eulophidae Larval-pupal endoparasitoid (TAMU)

Closterocerus (Chrysonotomyia)

formosa erythraea (Westwood)



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but were unsuccessful due to the failure to locate fruiting olives. There is only one

report of parasitism of B. oleae in India and Pakistan: an opiine braconid, Psyttalia

ponerophaga Silvestri, was reported and described from infested wild olives (Silvestri

1916). Based upon Silvestri’s work, recent foreign explorations begun in 2000 in

support of a classical biological control project in California were initially focused on

central and southern Africa, with surveys conducted in South Africa, Namibia,

Reunion Island and Kenya. Collections were made primarily of wild olives in a

variety of habitats and parasitoids, most previously reported by Silvestri, were

Table 1 (Continued )

Species Family Biology (known or presumed)

Tachinaephagus zealandicus

Ashmead

Encyrtidae Larval-pupal endoparasitoid

Eupelmus urozonus Dalman Eupelmidae Larval & pupal ectoparasitoid

(TAMU)

Eupelmus afer Silv. Eupelmidae Larval & pupal ectoparasitoid

(TAMU)

Halticoptera daci Silvestri Pteromalidae Larval or egg larval parasitoid

(TAMU)

Pteromalus semotus (Walker) Pteromalidae Ectophagous parasitoid of B. celer

(TAMU)

Europe and Asia � various sources

(refer to text)

Psyttalia (Opius) concolor

(Szepligeti)


Psyttalia (Opius) ponerophaga

(Silvestri)


Eupelmus urozonus Dalman Eupelmidae Larval & pupal ectoparasitoid

(TAMU)

Pnigalio mediterraneus Ferriere &

Delucchi

Pteromalidae Larval ectoparasitoid

Pnigalio agraules (Walker) Pteromalidae Possible misidentification

Pnigalio epilobii Boucek Pteromalidae Possible misidentification; northern

Eur. distribution (CD)

Eurytoma martellii Domenichini Euytomidae Larval ectoparasitoid

Cyrtoptyx latipes (Rondani) Pteromalidae Larval parasitoid

Closterosterus (Teleopterus) erxias

(Walker)

Eulophidae Egg or early larval parasitoid

Pachycrepoideus vindemiae

(Rondani)

Pteromalidae Ectoparasitic pupal parasitoid

(TAMU)

Tetrastichus sp. Eulophidae Larval-pupal endoparasitoid (TAMU)

Species known to be phytophagous seed wasps or hyperparasitoids of primary B. oleae parasitoids havebeen excluded from the table, but species about which there remains some doubt are included. Notes onbiology are from the original author unless otherwise indicated. Species names have been updated whereneeded, referencing Wharton and Yoder (2011) for braconids (TAMU) and Noyes (2011) (CD) forchalcidoids. The Universal Chalcidoidea Database (Noyes 2011) lists a number of additional recordswhich cannot be confirmed. Chalcididae: Dirhinus giffardii Silvestri; Encyrtidae: Allocerellus inquirendus;Eulophidae: Cirrospilus afer, Eulophus larvarum, Pnigalio longulus, Pnigalio pectinicornis, Pnigalio soemius,Thripastichus gentilei; Eupelmidae: Eupelmus vesicularis; Eurytomidae: Eurytoma aethiops, Eurytomanigrita, Eurytoma rosae, Eurytoma rufipes; Pteromalidae: Psilocera concolor, Pteromalus sp., Trichomalusrobustus.


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obtained from all of these locations. Additional visits were also made to Tunisia and

Morocco in North Africa and the Canary Islands in the Atlantic. In Asia, new

surveys in Pakistan with the assistance of the CSIRO Pakistan station resulted in

collection and shipments of P. ponerophaga to California. New explorations have also

been initiated in India although no parasitoids have been reared to date from fruit of

Olea spp. collected. Recent explorations in China located wild olives in remote parts

of Yunnan and Szechuan provinces, and one collection yielded specimens of a

Diachasmimorpha species in the longicaudata complex (unpublished data). Based

upon the success of other biological control programs against tephritid fruit flies

using braconids, and the apparent dominance of braconids over chalcidoid and other

parasitoids, interest in new species as candidate agents for biological control has been

focused on braconids. The braconid parasitoids obtained from these exploratory

surveys are listed in Table 2. Parasitoid species composition varies widely among the

various regions, although it is evident that exceptional diversity occurs in southern

Africa. Although most of the collections were made during short visits during the

fruiting season and may not represent the full diversity present at a site, several

studies surveyed the parasitoid fauna of wild olives at sites during the course of

entire seasons (Mkize, Hoelmer, and Villet 2008; Daane et al. 2011).

With few exceptions, parasitoids of B. oleae have been obtained primarily by

rearing adults from infested fruit or pupae collected after exiting fruit, both of which

favor discovery of species that attack the immature stages of fly inside the fruit.

Parasitoids that locate and attack B. oleae in the soil after larvae drop from fruit, or

following pupation, have been underrepresented in surveys to date. Pupal parasitoids

of other tephritid pests are known (e.g., Ovruski, Aluja, Sivinski, and Wharton

2000), so this approach merits more attention than it has received thus far.

6.2 Predators

A variety of predators attack B. oleae in southern Europe. These include many

staphylinid and carabid beetles, earwigs, the cecidomyiid Prolasioptera berlesiana

Paoli, chrysopids and other neuropterans, many species of ants, diplurans,

spiders and myriapods (Neuenschwander, Bigler, Delucchi, and Michelakis 1983;

Neuenschwander, Michelakis, and Kapatos 1986). Some studies have been published

regarding the predatory role of P. berlesiana, which may also act as a pest due to

introduction of decay agents in addition to feeding on fly eggs. However, the role of

P. berlesiana as both predator and pest was disputed by Harpaz and Gerson (1966),

so more study of this species is clearly needed. Except in a few localities, such as

Crete where extensive studies were conducted (Neuenschwander et al. 1983), the roles

of other predators are virtually unknown though it seems likely that predators may

be important mortality factors on B. oleae after larvae drop to the soil to pupate. For

example, weaver ants were shown to significantly reduce fruit fly infestations of

mango in Benin (van Mele, Vayssieres, van Tellingen, and Vrolijks 2007). The ants

were observed preying on larvae in soil and were also thought to interfere with adult

fly oviposition on fruit. In a recent study by Orsini, Daane, Sime, and Nelson (2007),

Formica aerata (Francoer) ants contributed significantly to mortality of B. oleae

pupae in the soil in California.


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Table 2. Braconid parasitoids reared from B. oleae in contemporary surveys during 2003�2007 of wild olives in Africa and Asia for importation and

evaluation in California.

Proportion of braconid species reared from each region of collection

Country Year

Psyttalia

lounsburyi

Psyttalia

humilis

Psyttalia

concolor

Bracon

spp.

Utetes

africanus

Psyttalia

ponerophaga

Diachasmimorpha

spp.

Morocco 2004 � � 1.0 � � � �Canary Is. 2004 � � 1.0 � � � �Pakistan 2005 � � � � � 1.0 �La Reunion 2004 � � � � � � 1.0

Namibia 2004 � 0.58 � 0.30 0.12 � �2007 0.23 0.57 � 0.15 0.05 � �2008 0.21 0.65 � 0.07 0.07 � �

South

Africa

2003 0.29 0.06 � 0.20 0.45 � �

2004 0.21 0.03 � 0.08 0.68 � �2005 0.54 � � � 0.46 � �

Kenya 2004 0.98 � � � 0.02 � �Kenya 2005 0.62 � � � 0.38 � �Kenya 2007 0.92 0.01 � � 0.07 � �China 2007 � � � � � � 1.0

Numbers indicate the proportion of each species represented in collections from each country.

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6.3 Pathogens

Pathogens of tephritid fruit flies have received comparatively little attention to date.

Several bioassay studies report varying levels of toxicity of the bacteria Bacillus

thuringiensis Berliner against B. oleae (Karamanlidou et al. 1991; Navrozidis, Vasara,

Karamanlidou, Salpiggidis, and Koliais 2000) and other tephritids (Robacher,

Martinez, Garcia, Diaz, and Romero 1996; Robacher, Garcia, and Martinez 2000).

Widely occurring, common soil-borne fungal entomopathogens have shown high

levels of pathogenicity in other tephritids including Metarhizium anisopliae

(Metchnikoff) Sorokin against Anastrepha ludens (Loew) (Lezama-Gutierrez et al.

2000) and M. anisopliae, Isaria (Paecilomyces) fumosoroseus Wize, and Beauveria

bassiana (Bals.-Criv.) Vuill. against Bactrocera zonata (Saunders) and B. cucurbitae

(Coquillett) (Sookar, Bhagwant, and Awuor Ouna 2008). In similar preliminary

trials, four isolates of B. bassiana and one of Metarhizium sp., all obtained from soil

samples under olive trees in Greece, were highly virulent against late instar B. oleae

larvae when tested in laboratory bioassays (KAH, unpublished data). Beauveria

bassiana, B. brongniartii (Saccardo) Petch and isolates of Mucor and Penicillium

species were also reported to cause high levels of mortality of B. oleae in laboratory

assays (Konstantopoulou and Mazomenos 2005). There are also several reports of

viruses capable of infecting B. oleae in which representatives of several families

of insect viruses were tested for growth and pathogenicity in the fly. Two viruses, one

of the picornaviruses (cricket paralysis virus (CrPV)) and the iridovirus (type 21 from

Heliothis armigera Hubner), were found to replicate in adult flies (Manousis and

Moore 1987). Entomogenous nematodes are found in several tephritid fly species

(Lindegren and Vail 1986, Lindegren, Wong, and McInnis 1990) and the

entomopathogenic nematode Steinernema feltiae (Filipjev) was shown to attack

larval olive fruit flies in soil and within fruit (Sirjani, Lewis, and Kaya 2009). Because

entomopathogens such as Beauveria, Metarhizium, and Paecilomyces spp. are

widespread in soils, and a large proportion of the B. oleae larval population

typically enters the soil before pupation, further investigations of pathogens are

warranted.

7. History of biological control efforts against B. oleae

7.1 Introduction (classical) biological control

Returning to Europe following his explorations, Silvestri was unsuccessful in

establishing cultures of most of the parasitoid species collected during his trips to

western Africa and Ethiopia (1914a, 1914b, 1915), but he released small numbers

of many of them in the field; however, these did not establish (Neuenschwander

1982). Releases of Dirhinus giffardii Silvestri, a central African parasitoid of

Ceratitis and other Bactrocera species were also made, but without establishment

(Neuenschwander et al. 1983). The discovery of P. concolor in northern Africa in

1910 also led to its introduction in southern Europe although without widespread

establishment. Following Neuenschwander’s (1982) South African surveys in which

B. celer was the most abundant parasitoid obtained in surveys, this species was

imported into Greece, but for undetermined reasons it could not be reared. He

concluded that further studies of this species were desirable, but no novel releases

for classical biological control of B. oleae were conducted in Europe until the


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recent availability of African parasitoids as a result of the program in California.

For example, Psyttalia lounsburyi (Silvestri) was imported and released in

California (Daane et al. 2008), and material from these initial colonies was later

released in France (Malausa et al. 2010) and Israel (Argov, Kuslitzky, and Hoelmer

in press).

Besides parasitoids of B. oleae, opiine braconids reared from Bactrocera

passiflorae (Froggatt), B. xanthodes (Broun) and B. distinctus (Malloch) in Fiji

were sent to France to be evaluated against B. oleae, but they proved ineffective

(Arambourg and Onillon 1970). Other parasitoids that had been utilized against pest

species such as medfly were also introduced for B. oleae, but without success

(Clausen 1978; Neuenschwander 1982).

As a result of the recent explorations in Africa and Asia, importation of B. oleae

parasitoids into California has led to host range and efficacy evaluations of P.

lounsburyi, P. concolor/P. humilis (Silvestri) (various populations, possibly including

cryptic species), P. ponerophaga (Silvestri), Utetes africanus (Szepligeti), and B. celer

(Daane et al., 2008; Sime, Daane, Messing, and Johnson 2006a; Sime et al. 2006b;

Sime, Daane, Kirk, Andrews, Johnson, and Messing 2007; Daane and Johnson 2010;

Daane et al. 2011). Several parasitoids of other tephritid flies have also been

evaluated, including Fopius arisanus (Sonan), Diachasmimorpha kraussi (Fullaway),

and D. longicaudata (Ashmead) (Calvitti, Antonelli, Moretti and Bautista 2002; Sime

et al. 2006c, 2008) and P. humilis (�cf. concolor) from Kenya originally obtained

from Ceratitis spp. (Yokoyama, Rendon, and Sivinski 2008; Wang, Johnson,

Yokoyama, Pickett, and Daane 2011). Research has also demonstrated that increased

olive size may have a negative influence on the efficacy of parasitoids with shorter

ovipositor lengths (Wang et al. 2009b; Wang, Johnson, Daane, and Yokoyama

2009a); ovipositors of braconid parasitoids of B. oleae range from very short (U.

africanus) to quite long (B. celer). Beginning in 2005, field releases of P. lounsburyi

and P. humilis in California were started, and as of summer 2010 several geographic

populations each of P. humilis and P. lounsburyi have been released in California, but

without conclusive evidence yet of establishment (Daane et al. 2011).

7.2 Mass rearing and augmentation

Considerable research has been directed at increasing parasitism by P. concolor in

olive groves through augmentative release programs in France, Italy, Spain, Greece,

Lebanon, and (the former) Yugoslavia. Although some success was demonstrated

with these projects (Arambourg 1979; Raspi 1993), they were not regarded as viable

due to their relatively high cost (Neuenschwander et al. 1986). However, the studies

proved that medfly is a useful alternate host for mass rearing the parasitoid (Raspi

and Loni 1994). Because B. oleae is difficult to rear on artificial diet (Tzanakakis

1989) and medfly rearing is easier and highly cost effective, there are advantages in

using this alternate host. Recently, P. humilis were successfully reared on irradiated

medfly larvae for field release against B. oleae in California (Yokoyama et al. 2010).

During the past several years, there has been a revived interest in mass-rearing B.

oleae (Genc and Nation 2008; Franz and Robinson 2011), which would reopen

possibilities for cost-effective mass rearing of B. oleae parasitoids, even if only to

support classical biological control programs.


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8. Discussion

The potential benefits of introducing exotic parasitoids of tephritid flies into infested

regions have been advanced by various researchers (Gilstrap and Hart 1987;

Greathead and Waage 1983; Wharton 1989; Sivinski et al. 1996). Although biological

control of tephritid fruit flies has mixed results to date, it is increasingly viewed as a

safe and economically effective technique for fruit fly management (Messing 1996;

Vargas et al. 2001), especially when used in concert with other area-wide methods.

Moreover, biological control will continue to grow in importance as pesticide use

becomes more restricted. The potential of parasitoids to suppress fruit fly populations

has been documented in Hawaii, where F. arisanus kills �90% of the Oriental fruit fly

eggs in some crops (Newell and Haramoto 1968), and in Florida with Anastrepha

suspensa (Lowe) (Sivinski et al. 1996). Key biological features of B. oleae, such as its

host specificity and tendency to deposit single eggs in fruits, should contribute to

greater success with parasitoids against this species than many other tephritids.

An additional benefit of the importation of new B. oleae parasitoids may be a

greater arsenal of natural enemies made available for testing against medfly and

other tephritid pests of fruits. There is reason to believe that parasitoid species

collected in Africa will also attack other species of Bactrocera and Anastrepha. We

have evidence of this cross-genus efficacy: D. longicaudata (collected on Bactrocera in

southeast Asia) successfully attacks the Caribbean fruit fly, A. suspensa in Florida

and Mexico and other Anastrepha species in Latin America and the southern US

(Ovruski et al. 2000), and several Ceratitis species in Kenya (Mohamed, Ekesi and

Hanna 2008); and D. tryoni (collected on Bactrocera tryoni (Froggatt) in Australia)

attacks the medfly in Hawaii (Duan, Messing, and Dukas 2000). The egg parasitoid

F. arisanus, collected on Bactrocera in Asia, attacks medfly (Vargas, Stark, Uchida,

and Purcell 1993) in the Nearctic and several other Ceratitis species in Africa, and

has been tested against B. oleae (Calvitti et al. 2002). Significantly, recent

comparative studies have shown that it displays a preference for, and experiences

lower encapsulation rates, in Bactrocera spp. (Mohamed, Ekesi, and Hanna 2010).

On the other hand, this potential for flexibility in host preference has increasingly

become a barrier to the introduction of effective natural enemies because of the

potential for impact on non-target organisms. In the case of an olive fruit fly

program, endemic species of tephritids and introduced species valued as natural

enemies of weeds would have to be demonstrated to be outside the range of

candidate agents (Duan, Purcell, and Messing 1996; Follett, Duan, Messing, and

Jones 2000).

In the last two decades, advances in the taxonomy and bionomics of braconids

(the most important family containing tephritid parasitoids) have resulted in

numerous nomenclatural changes, and it is likely that a study of known species

and newly-collected African and Asian material will result in revisions and discovery

of new species (Wharton 1989; Kimani-Njogu, Trostle, Wharton, Woolley, and

Raspi, 2001; Rugman-Jones, Wharton, van Noort, and Stouthamer 2009). This has

been especially true with the genus Psyttalia. Similar uncertainties exist in

other groups of tephritid parasitoids. There are indications that B. celer may

comprise several cryptic species (unpublished data) that warrant further investiga-

tion. Further complications are introduced by cross-breeding that may occur

between closely related species, as shown for several Psyttalia species (Billah et al.


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2008). Comparative evaluation of several populations of P. humilis and P. lounsburyi

under different environmental conditions in California also revealed differences in

efficacy (Wang et al. 2011). Detailed biological studies are thus needed to clarify the

relationship between parasitoid ecology, behavior and efficacy, including the

influence of the olive host on the parasitoid. Field studies of B. oleae and its

natural enemies in Africa and Asia will improve our ability to identify and evaluate

useful parasitoids of B. oleae. To this end, the foreign exploration for natural enemies

of B. oleae that was initiated following the fly’s introduction into California

may continue to provide new material for efficacy and host specificity testing,

including pupal parasitoids. Although exploration in Africa may be regarded

as largely complete, further specialized research could identify new species and

recover additional live material previously identified by earlier explorers necessary

for further studies in California and elsewhere. Continued exploration in Asia

extending east into China is also recommended for discovery of previously unknown

populations of B. oleae and its natural enemies.

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