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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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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
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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
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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)
Eulophidae Larval parasitoid
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
Bracon celer Szepligeti Braconidae Larval ectoparasitoid
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)
Bracon celer Szepligeti Braconidae Larval ectoparasitoid
Utetes (Opius) africanus (Szepligeti) Braconidae Larval-pupal endoparasitoid
Psyttalia (Opius) dacicida (Silvestri) Braconidae Larval-pupal endoparasitoid
Psyttalia (Opius) lounsburyi
(Silvestri)
Braconidae Larval-pupal endoparasitoid
Microdontomerus sp. Torymidae ?
Tetrastichus sp. Eulophidae Larval-pupal endoparasitoid (TAMU)
Closterocerus (Chrysonotomyia)
formosa erythraea (Westwood)
Eulophidae Larval parasitoid
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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)
Braconidae Larval-pupal endoparasitoid
Psyttalia (Opius) ponerophaga
(Silvestri)
Braconidae Larval-pupal endoparasitoid
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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