Abstract
This chapter is a demonstration of the wealth of African natural resources and their contribution to biological control of tephritid fruit flies (Diptera: Tephritidae). Africa is the native region of more than 900 species of fruit flies, many of which are significant agricultural pests. Highly diverse assemblages of indigenous hymenopteran parasitoid species have evolved with these fruit flies, which makes Africa a valuable source of parasitoids for use in classical biological control of fruit flies around the world. Interest in the use of parasitoids for biological control has recently increased due to advances in mass rearing techniques for exotic and native parasitoid species alongside the need to reduce synthetic insecticide use. Here we review the diversity of indigenous African parasitoid species and their role in classical biological control of fruit flies in other parts of the world; we also discuss their contribution to the management of native fruit flies in Africa. Likewise, the prospects and potential for using exotic parasitoids for management of newly-established invasive fruit flies in Africa is discussed, particularly for Batrocera zonata (Saunders), Bactrocera dorsalis (Hendel), Bactrocera latifrons (Hendel) and Zeugodacus cucurbitae (Coquillett). We cover the introduction and spread of exotic parasitoid species released in Africa for biological control of invasive fruit flies. The rich diversity of indigenous parasitoids of African fruit flies continues to be unraveled as more new species are discovered and recognized as potential biological control agents for fruit fly management.
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1 Introduction
Management of tephritid fruit flies requires an holistic IPM approach of which biological control is one of the essential components. Hymenopteran parasitoids are considered to be well suited to biological control of fruit flies because they are generally more host specific compared with predators and entomopathogens. For successful development endoparasitoids must deal with the host immune response and ectoparasitoids must deal with host mobility; for these reasons they are highly co-evolved with their particular hosts. Moreover, parasitoids are able to locate and attack the concealed immature stages of fruit flies inside fruits of both wild and cultivated plants.
Although the history of fruit fly biological control dates back to the beginning of the last century (Silvestri 1914a, b; Clausen 1978), it has recently received increasing attention (Wharton 1989; Knipling 1992; Headrick and Goeden 1996; Sivinski 1996; Purcell 1998). This has been facilitated by technological advances and ease in transportation of parasitoid consignments across the globe. Ovruski et al. (2000) attributed the renewed interest in using parasitoids for fruit fly biological control to the advances made in mass rearing techniques for exotic and native parasitoid species and their tephritid hosts. Increasing pressure to reduce the use of synthetic insecticides and the current drive towards conservation of biodiversity through the use of ecologically acceptable pest management tactics have made classical and augmentative biological control a desirable method to reduce fruit fly populations.
In almost all the published literature on biological control of fruit flies, Africa is highlighted as a source of parasitoids for use in classical biological control of fruit flies that are invasive pests elsewhere in the world; there is also a high species richness of fruit fly parasitoids in Africa (Silvestri 1914a, b, 1915; Clausen et al. 1965; Greathead 1976; Clausen 1978; Neuenschwander 1982; Wharton 1989 and reference there in; Waterhouse 1993; Mkize et al. 2008). In this chapter, we have compiled information on the diversity of indigenous African parasitoid species that attack fruit flies and their role in classical biological control in other parts of the world. Additionally, we highlight the contribution of these parasitoids in management of native fruit flies in Africa. Parasitoid species used for classical biological control of alien fruit flies that have invaded and become established in Africa are also reviewed in this chapter including four newly established Asian fruit flies: the peach fruit fly, Batrocera zonata (Saunders); the oriental fruit fly, Bactrocera dorsalis (Hendel); the solanaceous fruit fly, Bactrocera latifrons (Hendel); and the melon fly, Zeugodacus cucurbitae (Coquillett).
2 Diversity of the Indigenous Parasitoids of African Fruit Flies
Africa is the native range of several genera and more than 1000 species of fruit flies in the subfamily Dacinae (Diptera: Tephritidae), many of which are of significant agricultural importance as pests of commercial fruits and vegetables in sub-Saharan and Afrotropical regions (White and Elson-Harris 1992; Thompson 1998; De Meyer and Ekesi 2016). It is not surprising that a highly diverse assemblage of native hymenopteran parasitoid species have evolved with these fruit flies. However, much of our knowledge on the species composition of indigenous African parasitoids of tephritids is derived from the information generated during foreign explorations for natural enemies of African fruit flies that had invaded and become pests in other parts of the world, namely the Mediterranean fruit fly (medfly), Ceratitis capitata (Wiedemann), and the olive fruit fly, Bactrocera oleae (Rossi) (White and Elson-Harris 1992; CABI 2016).
A comprehensive record of indigenous African fruit fly parasitoids was first documented as early as 1912 by the prominent Italian entomologist Filippo Silvestri during his exploration for natural enemies in the West Coast of Africa (between 1912 and 1913) and Australia for use in biological control in the State of Hawaii (Territory of Hawaii at that time; Silvestri (1914a, b, 1915). He reported a high diversity of hymenopteran parasitoid species attacking fruit flies (Ceratitis species were attacked by ten species of parasitoids and Dacus species were attacked by seven parasitoid species) in the families Braconidae, Eulophidae, Chalcididae and Diapriidae from West Africa and South Africa (Table 16.1). However, the members of the family Braconidae (14 species), particularly in the subfamily Opiinae, were the most numerous in his collection. Additional information on the African parasitoid fauna is also reported from surveys by the earlier Hawaiian explorers e.g. D.T. Fullaway 1914; J.C. Bridwell 1914; F.A. Bianchi and N.L.H. Krauss 1936–1937 (reported in Bianchi and Krauss 1936) in Kenya; R.H. Van Zwaluwenburg in West Africa 1936; J.M. McGough 1949 in Kenya, Congo, Uganda and South Africa; F.E. Skinner 1948 in Kenya, Congo and South Africa; D.W. Clancy 1951 in Congo (reported by Clausen et al. 1965; Greathead 1976; Clausen 1978; Wharton 1989; Waterhouse 1993; Ovruski and Fidalgo 1994). In Hawaii the parasitoids collected were mass reared and introduced into many countries around the world for biological control of invasive fruit flies, where they subsequently became established (Table 16.1).
In contrast, invasions of the African continent by exotic fruit flies in the genus Bactrocera prompted many scientists in Africa to carry out inventories of the indigenous parasitoid species as a prerequisite prior to introduction of coevolved natural enemies from the native region of the exotic pest. Records from the indigenous parasitoid species inventories can be found in Appiah (2012) and Vayssières et al. (2011, 2012). Also Fischer and Madl (2008) provided a review for the Opiinae parasitoids of the Malagasy sub-region, most of which are of unknown biology or attack other non-tephritid hosts.
The rich diversity of the African tephritid parasitoid fauna continues to be unravelled as more new species are described and careful studies on their biology and host specificity are made. For example, Fopius ceratitivorus Wharton was first described by Wharton in 1999 and recognized as an important egg-larval parasitoid of C. capitata (Wharton 1999a); Fopius okekai and Rhynchosteres mandibularis were described in 2002 (Kimani-Njogu and Wharton 2002). More recently, two new Kenyan species have been described: Psyttalia halidayi Wharton (from the Natal fruit fly, Ceratitis rosa Karsch) and Psyttalia masneri Wharton (from an uncommon tephritid, Taomyia marshalli Bezzi, in cornstalk dracaena, Dracaena fragrans [L.] Ker Gawl) (Wharton 2009). In general, coffee, Coffea arabica L. and wild olive, Olea europaea ssp. cuspidate (Wall. ex G. Don) Cif, the closest relative to cultivated olives, supported the greatest diversity of parasitoid fauna (Clausen et al. 1965; Greathead 1972; Steck et al. 1986; Wharton et al. 2000; Copeland et al. 2004; Hoelmer et al. 2004, 2011).
It is important to note that some taxa reported in these early records have undergone several taxonomic revisions and changes in nomenclature (Fischer 1972, 1977, 1987; Wharton 1983, 1987; Wharton and Gilstrap 1983). Lists of synonyms and previously used combinations have been produced for the Braconidae and Opiinae (Wharton 1989) and for the superfamily Chalcidoidea (Noyes 2012).
3 Contribution of Indigenous Parasitoids to Fruit Fly Management
The level of parasitism achieved by indigenous parasitoid species in various fruit fly species on cultivated fruits is variable but generally quite low (<5 %) (Steck et al. 1986; Lux et al. 2003; Vayssières et al. 2012). For example, Vayssières et al. (2012) reported combined parasitism by seven parasitoid species of various wild and cultivated crops to be just 2.4 %. These observations may not entirely reflect the field situation as some parasitized larvae might have already left the sampled fruits to pupate in the soil, thus escaping observation (Lux et al. 2003). Also, unripe fruits collected during the surveys are likely to yield fewer larval parasitoids than ripe fruits, especially of Psyttalia species which have short ovipositors and prefer mature larvae close to the surface of ripe and fallen fruits. Wong and Ramadan (1987) working in Maui Island, Hawaii reported 19 % parasitism of C. capitata and B. dorsalis larvae in green fruit samples compared with 43 % in ripe and fallen fruits. Similar relationships between fruit ripeness and rates of parasitism have been reported for Psyttalia fletcheri (Silvestri) (Purcell and Messing 1996).
Of all the cultivated crops, coffee not only supported the highest diversity of parasitoids attacking fruit flies, but also high levels of parasitism. Steck et al. (1986) recorded a combined percent parasitism by Psyttalia perproximus (Silvestri), Fopius caudatus (Szépligeti) and Fopius caudatus auc C, Diachasmimorpha fullawayi (Silvestri), Fopius desideratus (Bridwell) and an undescribed species of Opius that ranged between l0 and 56 %; the average was 35 % parasitism in a research plantation and 17 % parasitism in a commercial plantation. This could be because coffee has a relatively small fruits compared with mango, Mangifera indica L., guava, Psidium guajava L., and papaya, Carica papaya L.. Opiine larval parasitoids do not enter the infested fruits to locate fruit fly larvae and their success is, therefore, limited by the length of their ovipositor and the size of the fruit. Moreover, in coffee ripe fruits remain on the tree allowing for full larval exposure to parasitoids.
Other tephritid host plants that support high levels of parasitism are members of the family Oleaceae, e.g. Olea europaea ssp. cuspidata (Wall. ex G. Don). During the 1999–2003 survey for insects associated with fruits of indigenous species of Oleaceae in Kenya, the rates of parasitization of B. oleae by Psyttalia lounsburyi (Silvestri) alone exceeded 30 % in some of the collections (Copeland et al. 2004). In a recent study by Mkize et al. (2008) on wild olives in the Eastern Cape Province, South Africa, the combined percent parasitism of B. oleae and Bactrocera biguttula (Bezzi) by Psyttalia concolor (Szépligeti), P. lounsburyi, Utetes africanus (Szépligeti) and Bracon celer Szépligeti, was in some instances as high as 83 %, leading to very low infestation levels (1–8 %). The authors indicated that these parasitoids were more closely associated with B. oleae as the number of B. oleae recovered was far smaller than the number of B. biguttula recovered. They also argued that fruit flies might not have become economic pests of commercial olives in the Eastern Cape due to the activity of these natural enemies. In Egypt, El-Heneidy et al. (2001) reported parasitism rates for P. concolor and Pnigalio agraules (Walker) (= Pnigalio mediterraneus (F.)), attacking B. oleae of 39% and 11%, repectively.
The performance of native parasitoids on different fruit fly species has been evaluated under laboratory conditions; high to moderate rates of parasitism were achieved in some host species. For example, Mohamed et al. (2003) reported parasitism rates of 37 and 46 % by Psyttalia cosyrae (Wilkinson) in C. capitata and the mango fruit fly, Ceratitis cosyra (Walker), respectively. In a different study the same authors, reported parasitism rates by P. concolor of 46 and 28 % in C. capitata and C. cosyra, respectively (Mohamed et al. 2007). Both parasitoid species were unable to develop on the C. rosa, Ceratitis fasciventris (Bezzi), Ceratitis anonae (Graham) and Z. cucurbitae (Mohamed et al. 2003, 2007) (Fig. 16.1). In contrast, the Eulophid Tetrastichus giffardii Silvestri achieved parasitism rates of 44.3 and 41.8 % on C. capitata and the lesser pumpkin fly, Dacus ciliatus Loew, respectively. Although members of the genus Tetrastichus are known to be rather generalist parasitoids, T. giffardii achieved zero parasitism on all members of the Ceratitis FAR group (C. fasciventris, C. annonae and C. rosa) as well as on the exotic Bactrocera species (Z. cucurbitae and B. dorsalis) (Fig. 16.1).
Although the role of pupal parasitoids in biological control of fruit flies cannot be denied, no systematic studies to evaluate their impact on fruit fly populations have been made, and hence no accurate statistics are available on their role as biological control agents. They are not host specific and may also attack nontarget Diptera in the suborder Cyclorhapha (e.g. Agromyzidae, Drosophilidae, Muscidae). Also they are difficult to evaluate in the field as they need to be collected by sifting the soil to retrieve fruit fly pupae, compared with collecting and incubating fruits to evaluate parasitoid species attacking the egg and larval stages of their hosts (M.M. Ramadan unpublished data; Wang and Messing 2004a, b).
4 Exploration for Fruit Fly Parasitoid Species in Africa for Introduction Elsewhere
Numerous species of hymenopteran fruit fly parasitoids have been recorded from native African tephritids since Silvestri’s famous survey in 1912 (Table 16.1). The table includes parasitoid species reared from fruit-infesting Tephritidae but excludes parasitoids specialized on tephritids infesting flowerheads (e.g. the African Psyttalia vittator group), stem and gall forming tephritids, various African opiines from agromyzid leafminers (e.g. Opius importatus Fischer and Opius phaseoli Fischer imported from Africa into Hawaii in 1969), and seed feeders (e.g. Psyttalia sanctamariana [Fischer] reared from the seed tephritid and Spathulina acroleuca [Schiner]). Parasitoids without confirmed host records, doubtful hosts, or doubtful identifications (e.g. Psyttalia insignipennis [Granger] from Madagascar and Singapore), are not reported here.
The African fruit fly species, C. capitata, has invaded and become established in many parts of the world including Western Australia and the Hawaiian Islands from as early as 1897 and 1910, respectively (Froggatt 1909; Compere 1912; both cited in Headrick and Goeden 1996). Being an alien pest, and lacking resident parasitoids in these countries, it continued to cause massive yield losses on various types of fruit. This prompted searches for efficient natural enemies of this devastating pest. The first classical biological control attempt was directed against C. capitata by George Compere when he was hired by the government of Western Australia between 1902 and 1907 to search for natural enemies of C. capitata (Wharton 1989). However, Compere was unable to determine the native range of C. capitata, and hence the parasitoids that he introduced to Australia from Brazil and India never established in C. capitata populations. A decade later, following the accidental introduction and establishment of C. capitata in Hawaii (then the Territory of Hawaii), Filippo Silvestri travelled to Africa and Australia, on behalf of the Hawaiian Board of Agriculture and Forestry, to search for efficient natural enemies of C. capitata (Silvestri 1914a, b). He identified 21 species of African hymenopteran parasitoids as having potential as biological control agents of C. capitata; he made collections from fruit infested with ten Ceratitis species and seven Dacus species. However, few parasitoids survived his long steamship trip and he returned to Hawaii with only Dirhinus giffardii Silvestri, Coptera silvestrii (Kieffer), Psyttalia humilis (Silvestri) and Psyttalia perproximus (Silvestri) from Africa, and Diachasmimorpha tryoni (Cameron) from Australia.
Silvestri returned from Hawaii to Italy in 1913 with some D. giffardii and C. silvestrii for biological control of B. oleae. A year later, he travelled back to East Africa (Eritrea), this time in search of more parasitoids for classical biological control of B. oleae in his homeland of Italy. He found 14 species attacking B. oleae, ten of which were reared and released in Italy although none became established. Fullaway, travelled to Nigeria in 1914 to re-collect parasitoid species that had not survived Silvestri’s expedition and he returned with Tetrastichus giffardianus Silvestri and Diachasmimorpha fullawayi (Silvestri), which were then released and established in Hawaii (Fullaway 1914).
Although Silvestri and Fullaway collected many parasitoid species belonging to different genera and families, only a few survived the long voyage to Hawaii. Amongst those that survived, four species were released and established of which three were from Africa. These were, P. humilis from South Africa and, D. fullawayi and D. giffardii both from West Africa. The two former species are koinobiont larval parasitoids while the latter is an idiobiont pupal parasitoid. Two decades after introduction in to Hawaii the combined parasitism rates achieved by P. humilis and another introduced Australian parasitoid, D. tryoni in C. capitata populations ranged from 46 to 94 % (Willard and Mason 1937). The two parasitoid species achieved approximately equal levels of parasitism in C. capitata populations. As a result, C. capitata infestations were significantly reduced on coffee and, to a lesser extent, on other fruits; success was not so good against C. capitata in large sized fruits such as mangoes (http://paroffit.org/public/site/paroffit/home). Subsequently, P. humilis was mass reared and redistributed from Hawaii to several other countries with tephritid fruit fly problems (Table 16.1). However, this parasitoid has not been recorded in Hawaii since 1933, even in recent surveys (M.M. Ramadan unpublished data) and is thought to be extinct there (http://paroffit.org/public/site/paroffit/home). Similarly, although it did establish after introduction, D. fullawayi has only rarely been recorded in Hawaii since 1949 (Bess 1953; Bess et al. 1961). From Hawaii, D. fullawayi and P. humilis were also introduced into Spain, Puerto Rico and Australia, without success (Table 16.1). Following its introduction into Hawaii, D. giffardii became established in C. capitata populations; it was later introduced from Hawaii into Australia in 1956, Mexico in 1955, Puerto Rico in 1935 and Bolivia in 1971 (Bennett and Squire 1972), and Israel in 1956 for biological control of C. capitata and other resident tephritids (Table 16.1).
During a separate expedition at around the same time, the gregarious parasitoid, T. giffardianus was also introduced into Hawaii from West Africa by D.T. Fullaway and J.C. Bridwell in 1914, where it became established (Clausen et al. 1965). Subsequently, this species was mass-reared and redistributed from Hawaii to the Pacific Islands and Latin American countries. For example, it was imported into Brazil in 1937 where it established (Ovruski and Schliserman 2012), and from there it was also imported into Argentina in 1947 (Flávio et al. 2013) (Table 16.1).
Africa was also targeted in world-wide surveys for parasitoids made during the Hawaiian biological control campaign against B. dorsalis, in the 1950s. Import of African fruit flies into Hawaii (from South Africa in 1949, from Kenya in 1949–1950, from Congo in 1950–1951, and from Cameroon in 1951) with the purpose of collecting any parasitoids that emerged, was comprised of 571,995 pupae from 26 different tephritid species (Clausen et al. 1965). At least 22 different parasitoid species were recovered from these shipments, propagated and evaluated for their ability to develop on, B. dorsalis, Z. cucurbitae and C. capitata. Only six parasitoid species were released (D. giffardii, T. giffardii, T. giffardianus, Fopius bevisi (Brues), Psyttalia phaeostigma (Wilkinson) and an Opius sp. (Clausen et al. 1965).
Within the framework of a USDA grant (2001–2004) through the Texas A&M University entitled ‘Facilitating Identification and Suppression of African Fruit-infesting Tephritidae (Diptera): Invasive Species That Threaten U.S. Fruit and Vegetable Production’ the recently described parasitoid species, Fopius ceratitivorus Wharton and a related species, Fopius caudatus (Szépligeti) were imported from Kenya into the USDA-APHIS/MOSCAMED quarantine facility in Guatemala (Lopez et al. 2003), and from Guatemala into Hawaii. They where both evaluated for potential effects on non-target hosts and found not to parasitize eggs or larvae of the non-target tephritids, Procecidochares alani Steyskal, a biological control agent of the invasive weed, Ageratina riparia (Regel), and the native Hawaiian tephritid Trupanea dubautia (Bryan) found in the flowerheads of the endemic shrub, Dubautia raillardioides Hillebr. (Bokonon-Ganta et al. 2007; Wang et al. 2004). Under the same initiative P. phaeostigma and P. halidayi were, respectively, sent to St. Helena for control of D. ciliatus (2000–2001) and La Réunion (2000–2001) for control of C. rosa (S.A. Mohamed unpublished data). However, no follow up on their release and establishment has been made.
Psyttalia concolor a parasitoid of North African origin that is similar to the South African P. humilis, was initially imported from Tunisia (Monastero 1931; Silvestri 1939), and then released in Italy in 1913 for control of B. oleae, where it only became established at low densities. Since then, biological control of B. oleae in southern European countries has been almost exclusively based on importation and repeated releases of P. concolor (Raspi 1995; Raspi and Loni 1994). This parasitoid also parasitizes C. capitata in the Mediterranean basin.
In Israel, classical biological control targeting C. capitata and B. oleae has a relatively long history (Argov and Gazit 2008 and references therein). Between 2002 and 2004 four parasitoid species were imported from Hawaii and released against C. capitata. Two of these parasitoid species, the egg-larval parasitoid, F. ceratitivorus and the larval parasitoid, P. concolor were originally from Kenya. Of the African parasitoid species, F. ceratitivorus has shown signs of long-term establishment in Israel (Argov and Gazit 2008). A few years later (2009–2010), two other African parasitoid species were imported in to Israel, this time targeting B. oleae. These were P. lounsburyi (from Kenya and South Africa), and Psyttalia sp. nr. concolor (also called P. humilis) (from Namibia). A total of 37,000 and 97,000 wasps of the former and the later species, respectively were released in Israeli olive groves.
In 1998 B. oleae was detected in Californian olive groves (Rice et al. 2003). On the recommendation of earlier explorers highlighting the high diversity of B. oleae-associated parasitioids in Africa (e.g. Silvestri 1914a, b; Neuenschwander 1982), more expeditions across Africa were made to study these parasitoid species further. The parasitoid, P. concolor, was obtained from tephritid fruit flies infesting coffee in Kenya, reared on C. capitata in Guatemala by USDA-APHIS, PPQ, and then imported and released in Californian olive groves for biological control of B. oleae. Following this further exploration was attempted, this time for parasitoids that were more specific to B. oleae on wild African olives. Robert Copeland, an American entomologist based at icipe, Nairobi, Kenya, was contracted by USDA-APHIS to search for parasitoids attacking B. oleae in Kenya. He collected P. concolor, P. lounsburyi and Utetes africanus for importation into California via the USDA-ARS European Biological Control Laboratory (EBCL) in Montferrier, Montpellier, France (Copeland et al. 2004). This was followed by more expeditions to Kenya, South Africa, Namibia, La Réunion and Morocco. During these expeditions, P. lounsburyi, P. humilis, P. concolor, Bracon spp. and U. africanus were reared from wild olives and shipped to California for release via France (Hoelmer et al. 2011).
In Central America, African parasitoids were also the main focus for classical biological control of C. capitata. For example, in Costa Rica two African parasitoids, D. giffardii and P. concolor were introduced following the invasion by C. capitata in 1955 (Purcell 1998). A further six African parasitoid species were obtained by Gary Steck during his exploration for natural enemies of C. capitata in Togo and Cameroon between 1980 and 1982 (Steck et al. 1986). Following mass-rearing in Guatemala, F. ceratitivorus from Kenya was released on a large scale against C. capitata in the coffee-growing highlands along the Mexican borders (Sivinski and Aluja 2012). Detailed information regarding African parasitoid introductions for classical biological control of tephritid fruit flies in other countries is given in Table 16.1.
5 Introduction of Exotic Parasitoid Species into Africa for Biological Control of Invasive Fruit Flies
The first, though unsuccessful, attempt at classical biological control of exotic, invasive fruit flies in Africa was done in 1905. During this period, Charles Lounsbury and Claude Fuller, entomologists from South Africa, travelled to South America (Sao Paulo and Bahia, Brazil) to collect natural enemies for control of C. capitata in South Africa because, at the time, the native range of C. capitata was unknown (Lounsbury 1905 as cited in Ovruski et al. 2000). They collected the braconid, Opius trimaculatus Spinola and another unidentified parasitoid, from fruits infested by Anastrepha fraterculus (Wiedemann) and Anastrepha serpentina (Wiedemann) (Table 16.2). According to Wharton and Gilstrap (1983) this braconid could have been a misidentification of Opius bellus Gahan, Utetes anastrephae (Viereck), or a Doryctobracon sp. Opius trimaculatus was an important species to collect as field parasitism rates ranged from 7 % in large guava fruits to 38 % in the smaller fruits of Surinam cherry, Eugenia uniflora L. Because of the length of the trip from Brazil to South Africa via England, none of the imported braconid parasitoids survived the journey. Three years later, from a laboratory-reared colony in Australia, G. Compere sent to South Africa 20,000 Aceratoneuromyia indica (Silvestri) parasitoids, which he had initially collected from India during his expedition for natural enemies of C. capitata in Western Australia (Table 16.2). However, this parasitoid never became established in South Africa (Clausen 1956). Other failed attempts included the introduction of Diachasmimorpha longicaudata (Ashmead), Opius sp., Psyttalia incisi (Silvestri) and P. phaeostigma into Mauritius; and D. tryoni into both Mauritius and La Réunion (Fischer and Madl 2008).
Apart from the initiatives already mentioned, and despite the fact that Africa has been invaded by four Asian Bactrocera species (see De Meyer and Ekesi 2016), for which the first records date back to the 1930s (White and Elson-Harris 1992), classical biological control programmes for invasive fruit flies in Africa have not been taken up in the same way as in other continents that have been invaded by exotic species. For example, in Hawaii where C. capitata and three species in the genus Bactrocera have become established as key pests of fruits and vegetables, several expeditions were undertaken to various parts of the world in search of co-evolved natural enemies of these pests for introduction in to Hawaii. This resulted in the most successful classical biological control programme ever undertaken against tephrtids fruit flies (Wharton 1989; Purcell 1998).
In Africa, the earliest record of successful classical biological control of an exotic fruit fly species was in 1995, when P. fletcheri was introduced from Hawaii for biological control of Z. cucurbitae on the island of La Réunion (Quilici et al. 2004) (Table 16.2). The parasitoid is currently well established on the island though rates of parasitism of Z. cucurbitae are quite variable ranging from 1 to 75 % on bitter gourd, Momordica charantia L (Cucurbitaceae) (Quilici et al. 2008). This was followed by introduction of another parasitoid species, the egg-larval parasitoid Fopius arisanus (Sonan) for biological control of another alien invasive pest, B. zonata, on the same island (Rousse et al. 2006). A survey conducted on Indian almond, Terminalia catappa L., on which B. zonata is the dominant species, found that the level of parasitism on this host-fruit could reach 70–80 % (Quilici et al. 2008).
The most prominent fruit fly classical biological control programme in Africa to date was directed against B. dorsalis after it proved to be lacking resident parasitoid species capable of regulating its populations; all indigenous parasitoid species evaluated failed to form new associations with this pest due to its strong immune system, resulting in encapsulation and melanization of parasitoid eggs (Mohamed et al. 2006; S.A. Mohamed unpublished data). For example, two solitary larval parasitoids, P. cosyrae and P. phaeostigma and one gregarious parasitoid, T. giffardii were evaluated. Bactrocera dorsalis was readily accepted as a potential host by adult female T. giffardii and to a lesser extent by females of the two Psyttalia species. However, all eggs of the two Psyttalia species and nearly all the eggs of T. giffardii were encapsulated within larvae of B. dorsalis (Mohamed et al. 2006; S.A. Mohamed unpublished data). None of the T. giffardii progeny that escaped encapsulation were able to complete development to the adult stage. Furthermore, 34,430 kg of various host fruits of B. dorsalis were sampled in East Africa (Rwomushana et al. 2008) and West Africa (Vayssières et al. 2012; R. Hanna unpublished data), but not a single parasitoid species was recovered, confirming the fact that the indigenous African parasitoids were unable to parasitize B. dorsalis. These findings paved the way for identification and introduction of efficient parasitoids that had a shared history and origin with B. dorsalis. In this regard, the subsequent and logical approach was exploration for co-evolved parasitoid species in the pest’s presumed native range of Sri Lanka. Three expeditions were made between 2005 and 2008 by scientists from the International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya, the International Institute of Tropical Agriculture (IITA) and the University of Bremen, Germany, in collaboration with staff from the Horticultural Crop Research and Development Institute (HORDI), Peradeniya, Sri Lanka within the framework of the Mango IPM BMZ-funded project. Eight parasitoid species from different guilds (one egg-larval, five larval and two pupal) including F. arisanus, D. longicaudata and P. fletcheri were recovered from the sampled fruits and evaluated in the laboratory against target hosts (Billah et al. 2008; S.A. Mohamed unpublished data). Despite this, none were introduced into Africa due to issues relating to the Convention on Biological Diversity (CBD) to which Sri Lanka is a signatory. Thereafter, contacts were made between scientists on the icipe-led African Fruit Fly Programme and scientists at the USDA-ARS Pacific Basin Agricultural Research Center at Hilo, Hawaii and the University of Hawaii at Manoa. This led to introduction of the egg-larval parasitoid F. arisanus and the larval parasitoid, D. longicaudata into Africa (Table 16.2). These parasitoid species had been credited with outstanding success in the biological control of B. dorsalis following its invasion and establishment in Hawaii in 1944/1945 (Fullaway 1949). The two parasitoid species were imported into the icipe quarantine facility in 2006, following the FAO code of conduct for the importation and release of exotic biological control agents (IPPC 2005), and were later released in Kenya in 2008, in Tanzania in 2010, and in Mozambique in 2012. Fopius arisanus was also released in the Comoros Islands in 2015. In Western Africa and under the umbrella of the same collaborative project, IITA released F. arisanus in Benin, Cameroon and Togo from a colony initially obtained from icipe in 2006 and subsequently maintained by IITA at Yaoundé, Cameroon and Cotonou, Benin. A detailed account of the release, establishment and spread of this parasitoid in Benin is given in Gnanvossou et al. (2016).
The post release assessment of colonization of these parasitoid species so far indicates that F. arisanus has established in all the countries where it was released but to varying degrees; the rates of B. dorsalis parasitism achieved on cultivated fruits was 33–40 % in Kenya at the Northern Coast region of Kilifi (elevation > 400 masl) (Ekesi et al. 2010, 2016; S. Ndlela, unpublished data). On wild host fruit rates of B. dorsalis parasitism reached 46.5 % on bush mango, Irvingia gabonensis (Aubry-Lecomte), in Benin (Gnanvossou et al. 2016). While establishment of D. longicaudata has been reported only in Kenya, at Embu in the Eastern Province (elevation range of 694M–1509 masl) and the Coast region (elevation < 400masl) with parasitism rates of up to 17 % and 15.4 %, respectively. Under a separate initiative, yet still targeting B. dorsalis, USDA-APHIS in collaboration with the Senegalese Plant Protection Department introduced F. arisanus into Senegal from Hawaii (Vargas et al. 2016). Between 2013 and 2014 14 shipments of 66,000 parasitoids were received in Senegal and released in the Casamance region (Vargas et al. 2016). This resulted in 20–30 % parasitism of B. dorsalis. The authors indicated that additional parasitoid shipments were sent from Hawaii and released in other regions of Senegal to improve control during the mango fruiting season (Vargas et al. 2016).
In southern Africa, within the framework of the BONAZAZI FAO-funded project for suppression of B. dorsalis, both F. arisanus and D. longicaudata have recently been introduced into Botswana, Namibia, Zambia and Zimbabwe. However, a post evaluation survey to evaluate their establishment will only be undertaken during the 2016/2017 mango fruiting season.
In North Africa there has been a control programme targeted at another exotic invasive species, B. zonata. This species was first detected in 1997 and has since become widespread over most of the Egyptian governorates causing serious damage to many fruit crops. The Agricultural Research Centre (ARC), Giza, Egypt in collaboration with the State of Hawaii Department of Agriculture, have imported five parasitoid species from Hawaii for evaluation and release in Egypt (El-Heneidy and Ramadan 2010). These are Aganaspis daci (Weld), F. arisanus, D. kraussii, D. tryoni and D. longicaudata (Table 16.2). The five species were evaluated in the laboratory against B. zonata. Surprisingly, F. arisanus, which achieved high rates of parasitism on B. zonata in La Réunion, performed poorly on the same host in Egypt (El-Heneidy personal communication).
Following the promising performance in the laboratory evaluation of A. daci against B. zonata, this parasitoid has been released in the El-Arish district, North Sinai Governorate, during the guava season of 2010, and was recovered 1 month after release. Post-release assessment in the El-Arish district indicated 9.7 % parasitism. Further studies on its natural dispersal and effectiveness in suppressing B. zonata and other tephritid fruit fly populations in Egypt, are still in progress (El-Heneidy unpublished data). This parasitoid is an important candidate for B. zonata control, especially in large sized fruits (mango, peach, and guava), as it uses an ingress and sting strategy (i.e it enters the fruits to parasitize the larvae). All opiines use only drill and sting strategies; therefore, their accessibility to the host inside the fruit can be limited by the length of their ovipositors.
Currently, efforts are underway to introduce F. arisanus and D. longicaudata from icipe into Sudan for control of B. zonata and Ethiopia and South Africa for control of B. dorsalis.
6 Prospects and Potential Use of Parasitoids for Fruit Fly Management in Africa
Since the turn of last century, considerable advances have been made in both classical and augmentative biological control of fruit flies. However, this has not progressed at the same pace in Africa.
In general, parasitoids are unlikely to provide complete control of tephrid fruit flies because they act in a density dependant manner. Furthermore, the majority of susceptible produce is high-value fruit, making the damage threshold extremely low to ensure that the consumers’ zero tolerance to blemished fruits is achieved. Nevertheless, parasitoids can significantly reduce fruit fly populations when used within the framework of an area-wide IPM approach. This is evidenced by the outstanding success of biological control programmes using parasitoids against the same and/or related tephritid fruit fly species in other parts of the world. Undeniably, the outcome of B. dorsalis and C. capitata control in Hawaii, and B. dorsalis, B. kirki and B. tryoni control in French Polynesia using F. arisanus and D. longicaudata (Vargas et al. 2007) are good examples of success that can be achieved and could be replicated in Africa. Indeed, the earlier explorers such as Silvestri (1914a, b) and van Zwaluwenburg (1937) indicated that C. capitata was rare in West Africa; the former author attributed the paucity of C. capitata in West Africa to the role of parasitoids. Also Steck et al. (1986) stated that C. capitata was of no economic importance in Central and West Africa due to the action of natural enemies. Similar observations of low infestation levels on olives in the Eastern Cape, South Africa have also been attributed to the action of parasitoids (Hancock 1989; Mkize et al. 2008).
Although Bactrocera invadens (as B. dorsalis was initially called in Africa) was recently synonymized with Bactrocera dorsalis sensu stricto (Schutze et al. 2015) populations in the native range could still be phenotypically different to populations in Africa with respect to their susceptibility to parasitoids; for example, African populations of B. dorsalis performed differently compared with the Hawaiian population where there are no reports of host immunity to D. longicaudata and F. arisanus (Mohamed et al. 2006, 2008). Therefore, more expeditions to the pest’s area of origin are needed in Southeast Asia to evaluate the parasitoid species that did not establish in Hawaii during the B. dorsalis biological control programme in 1950s. Although Z. cucurbitae was presumed to have invaded Africa in the 1930s, no parasitoid species were introduced for its control. Considering that Z. cucurbitae mounts a strong immune response against almost all African parasitoid species and only P. fletcheri from its native range is capable of overcoming its immune system, it would be worthwhile to source this parastoid species from its native range and release it in Africa. Indeed, this parastoid species has been imported and released for classical biological control in several countries with promising results. For example, the release of P. fletcheri in Hawaii resulted in up to 29.8 and 96.9 % rates of parasitism of Z. cucurbitae on cucumber and wild bitter gourd, respectively (Willard 1920). Other parasitoids that are promising candidates for classical biological control of Z. cucurbitae need to be considered for importation into Africa and include four opiine parasitoids: Diachasmimorpha albobalteata (Cameron) from North Borneo, Diachasmimorpha dacusii (Cameron) from North India, Diachasmimorpha hageni (Fullaway) from Fiji and Fopius skinneri (Fullaway) from Thailand. Fopius skinneri should be considerd due to its tendency to parasitize tephritid larvae in cucurbits rather than other fruits (Waterhouse 1993). The larval-pupal parasitoid, A. daci, introduced into Hawaii from Queensland, Australia and Malaysia in 1949, has been reported as a primary parasitoid of Z. cucurbitae as has an Aceratoneuromyia sp. from northern Thailand (Ramadan and Messing 2003). However, a strain of A. daci from Greece was unable to develop in Z. cucurbitae (M.M. Ramadan unpublished data).
Although B. latifrons is of less economic importance than some species it can be a serious pest on solanaceous crops in the absence of natural enemies. Its management in Africa would greatly benefit from introduction of a co-evolved and efficient exotic parasitoid species from its native range. Laboratory experiments showed that most of the parasitoid species that attack B. dorsalis and C. capitata can survive in B. latifrons. Diachasmimorpha kraussii was released in Hawaii after it was successfully reared on B. latifrons, but subsequently it was rarely recovered from B. latifrons in wild fruits in the field. Exploration for parasitoids attracted to infested solanaceous fruits in the Indo-Malaysian region is required.
The introduction of F. arisanus for biological control of B. zonata resulted in mixed outcomes. This also calls for exploration and evaluation of more efficient parasitoid species from its native range. Such expeditions should aim at finding parasitoid species attacking both egg and larval stages of B. zonata to maximize the chances of pest suppression. Moreover, A. daci which has been promising for B. zonata control in Egypt should be evaluated further as a potential candidate for classical biological control of B. zonta in other African countries that are affected.
The native fruit fly, C. rosa, and its close relatives in the FAR complex, were immune to all the indigenous solitary and gregarious parasitoid species evaluated (Mohamed et al. 2003, 2006, 2007); furthermore, the two introduced parasitoids, F. arisanus and D. longicaudata, performed very poorly on Ceratitis species in the FAR complex (Mohamed et al. 2008, 2010). For these reasons a search for efficient parasitoids against these pests is urgently needed. Fortunately, the recently described P. halidayi was reared from field-collected C. rosa developing in fruits of Lettowianthus stellatus Diels in coastal Kenya (Wharton 1996b) and its efficiency against C. rosa was further confirmed in laboratory studies (S.A. Mohamed unpublished data). Therefore, this parasitoid is a promising candidate that could be developed for biological control of C. rosa in mainland Africa; it could also be introduced for classical biological control in La Réunion and Mauritius where C. rosa has invaded. There is also a need for further research to identify parasitoid species that can overcome the immune response and develop successfully in C. fasciventris and C. anonae which cause significant yield losses in many tropical fruits (White and Elson-Harris 1992; Copeland et al. 2006).
Augmentation of parasitoid populations should also be considered to boost the efficiency of introduced parasitoids. In the same way, the role of native parasitoids in controlling native fruit flies could be enhanced by augmentative releases. This calls for involvement of the private sector in mass rearing of these parasitoids.
Parasitoid conservation, whether introduced or indigenous, is a fundamental pillar in ensuring the success of biological control programmes. It is, therefore, essential to make fruit and vegetable growers in Africa more aware of how to conserve parasitoids by using more eco-friendly management approaches rather than expensive blanket cover sprays of insecticide. Additionally, growers should be encouraged to practice habitat management that provides refuges and food sources for parasitoids in the areas surrounding orchards and gardens. Finally, the role of pupal parasitoids, particularly for biological control of native species should not be overlooked.
References
Appiah EF (2012) Evaluation of introduced parasitoids against Bactrocera invadens and their interaction with indigenous natural enemies (Ph.D. thesis). University of Ghana
Argov Y, Gazit Y (2008) Biological control of the Mediterranean fruit fly in Israel: Introduction and establishment of natural enemies. Biol Cont 46:502–507
Bennett FD, Squire FA (1972) Investigations on the biological control of some insect pests in Bolivia PANS (Pest Articles and News Summaries) 18:459–467
Bess HA (1953) Status of Ceratitis capitata in Hawaii following the introduction of Dacus dorsalis and its parasites. Proc Hawaii Entomol Soc 15:221–233
Bess HA, van den Bosch R, Haramoto RH (1961) Fruit fly parasites and their activities in Hawaii. Proc Hawaii Entomol Soc 17:367–378
Bianchi FA, Krauss NH (1936) Report on the United States Department of Agriculture East-African fruit fly expedition of 1935–1936. United States Department of Agriculture, Washington, DC
Billah MK, Ekesi S, Hanna R, Goergen G, Bandara KANP (2008) Exploration for natural enemies of Bactrocera invadens in Sri Lanka for classical biological control of the pest in Africa. First meeting of TEAM. Palma of Mallorca, Spain. 7–8th April 2008
Bokonon-Ganta AH, Ramadan MM, Messing RH (2007) Reproductive biology of Fopius ceratitivorus (Hymenoptera: Braconidae), an egg–larval parasitoid of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Biol Cont 41:361–367
Boucek Z (1963) A taxonomic study in Spalangia. Acta Entomol Mus Nat Prague 35:430–512
Bridwell JC (1918) Descriptions of new species of hymenopterous parasites of muscoid Diptera with notes on their habits. Proc Hawaiian Entomol Soc 4:166–179
CABI (2016) Invasive species compendium. CAB International, Wallingford. Available:http://cabi.org/isc/datasheet. (January 2016)
Clausen CP (1956) Biological control of fruit flies. J Econ Entomol 49:176–178
Clausen CP (1978) Tephritidae (Trypetidae, Trupaneidae), pp 320–335. In: Clausen CP (ed) Introduced parasites and predators of arthropod pests and weeds: a world review. United States Department of Agriculture, Agriculture Handbook 480. U.S. Government Printing Office, Washington, DC, 545 p.
Clausen CP, Clancy DW, Chock QC (1965) Biological control of the oriental fruit fly (Dacus dorsalis Hendel) and other fruit flies in Hawaii. US Dept Agric Tech Bull 1322:1–102
Cochereau P (1970) Les mouches des fruits et leurs parasites dans la zone Indo-Australo-Pacifique et particulierement en ouvelle-Caledonie. Cah ORSTOM Ser Bio 12:15–50
Copeland RS, White IM, Okumu M, Machera P, Wharton RA (2004) Insects associated with fruits of the Oleaceae (Asteridae, Lamiales) in Kenya, with special reference to the Tephritidae (Diptera). Bishop Mus Bull Entomol 12:135–164
Copeland RS, Wharton RA, Luke Q, De Meyer M, Lux S, Zenz N, Machera P, Okumu M (2006) Geographic distribution, host fruit, and parasitoids of African fruit fly pests Ceratitis anonae, Ceratitis cosyra, Ceratitis fasciventris, and Ceratitis rosa (Diptera: Tephritidae) in Kenya. Anns Entomol Soc Am 99:261–278
Daiber CC (1966) Notes on two pumpkin fly species and some of their host plants. S Afr J Agri Sc 9:863–876
De Meyer M, Ekesi S (2016) Exotic invasive fruit flies (Diptera: Tephritidae): In and out of Africa. In: Ekesi S et al (eds) Fruit fly research and development in Africa – towards a sustainable management strategy to improve horticulture. Springer International Publishing, Cham. doi:10.1007/978-3-319-43226-7_7
Delucchi V (1957) Les parasites de la mouche del olives. Entomophaga 2:107–118
Ekesi S, Billah MK (eds) (2006) A field guide to the management of economically important tephritid fruit flies in Africa. The International Centre of Insect Physiology and Ecology (ICIPE). ICIPE Science Press-Nairobi, Nairobi
Ekesi S, Mohamed S, Hanna R (2010) Rid fruits and vegetables in Africa of notorious fruit flies. Technical Innov. Brief No. 4. CGIAR SP-IPM. http://www.spipm.cgiar.org/c/document_library/get_file?p_l_id=17830&folderId=18484&name=DLFE-882.pdf
Ekesi S, De Meyer M, Mohamed SA, Virgilio M, Borgemeister C (2016) Taxonomy, ecology and management of native and exotic fruit fly species in Africa. Ann Rev Entomol 61:219–238
El-Heneidy AH, Ramadan MM (2010) Bacterocera zonata (Saunders) status and its natural enemies in Egypt. 8th international symposium on fruit flies of economic importance, Valencia, Spain, 26 Sept–10 Oct 2010
El-Heneidy AH, Omar AH, El-Sherif H et al (2001) Survey and seasonal abundance of the parasitoids of the olive fruit fly, Bactrocera (Dacus) oleae Gmel. (Diptera: Trypetidae). Egypt Arab J Plant Prot 19:80–85
Etienne J (1973) Lutte biologique et apercu sur les etudes entomologiques diverses effectuees ces dernieres annees a la Réunion. L’Agronomie Tropicale 6–7:683–687
Fischer M (1971) Index of entomophagous insects. Hymenoptera Braconidae. World Opiinae. Le François, Paris, 189 pp
Fischer M (1972) Hymenoptera Braconidae (Opiinae I). Das Tierreich 91:1–620
Fischer M (1977) Hymenoptera Braconidae (Opiinae II-Amerika). Das Tierreich 96:1–1001
Fischer M (1987) Hymenoptera: Opiinae III – athiopische, orientalische, australische und ozeanische region. Das Tierreich 104:1–734
Fischer M, Madl M (2008) Review of the Opiinae of the Malagasy Subregion (Hymenoptera: Braconidae). Linzer Biolog Beitr 40:1467–1489
Flávio R, Garcia M, Ricalde MP (2013) Augmentative biological control using parasitoids for fruit fly management in Brazil. Insects 4:55–70. doi:10.3390/insects4010055
Fry JM (1987) Natural enemy databank. A catalogue of natural enemies of arthropods derived from records in the CIBC Natural Enemy Databank. CAB International, Oxon, pp 34–35
Fullaway DT (1914) Report of the work of the insectary pp 143–151. In: Report of the board of commissioners of agriculture and forestry of the territory of Hawaii, Honolulu Star Bulletin LTD, Honolulu, pp 246 https://books.google.com/books?id=YVZJAAAAMAAJ&dq
Fullaway DT (1949) Dacus dorsalis Hendel in Hawaii. Proc Hawaii Entomol Soc 13:351–355
Ghani MA (1972) Final report: studies on the ecology of some important species of fruit flies and their natural enemies in West Pakistan. Pakistan Station, CIBC, Rawalpindi, 1–42
Gilstrap FE, Hart WG (1987) Biological control of the Mediterranean fruit fly in the United States and Central America. US Dep Agric Agric Res Serv 56:68
Gnanvossou D, Hanna R, Bokonon-Ganta AH, Ekesi S, Mohamed SA (2016) Release, establishment and spread of the natural enemy Fopius arisanus (Hymenoptera: Braconidae) for control of the invasive oriental fruit fly Bactrocera dorsalis (Diptera: Tephritidae) in Benin, West Africa. In: Ekesi S et al (eds) Fruit fly research and development in Africa – towards a sustainable management strategy to improve horticulture. Springer International Publishing, Cham. doi:10.1007/978-3-319-43226-7_26.
Greathead DJ (1972) Notes on coffee fruit-flies and their parasites at Kawanda. Commonwealth Inst. Biol Cont CAB 13:11–18
Greathead DJ (1976) Report on a survey for natural enemies of olive pests in Kenya and Ethiopia, September–December 1975. Commonwealth Institute of Biological Control, Delemont, Switzerland. 24p.
Greathead DJ, Greathead AH (1992) Biological control of insect pests by insect parasitoids and predators: the BIOCAT database. Biocontrol News Inf 13:61N–68N
Hancock DL (1989) Pest status: southern Africa. In: Robinson A, Hooper G (eds) World crop pests: fruit flies—their biology, natural enemies and control, 3A:51–58. Elsevier, Amsterdam
Headrick DH, Goeden RD (1996) Issues concerning the eradication or establishment and biological control of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), in California. Biol Cont 6:412–421
Hoelmer KA, Kirk A, Wharton R, Pickett CH (2004) Foreign exploration for parasitoids of the olive fruit fly, Bactrocera oleae. In: Woods D (ed) Biological control program annual summary, 2003. California Department of Food & Agriculture, Sacramento, pp 12–14
Hoelmer KA, Kirk AA, Pickett CH, Daane KM, Johnson MW (2011) Prospects for improving biological control of olive fruit fly, Bactrocera oleae (Diptera: Tephritidae), with introduced parasitoids (Hymenoptera). Biocont Sci Tech 21:1005–1025. doi:10.1080/09583157.2011.594951
IPPC (2005) International plant protection convention: international standards for phytosanitary measures No. 3 – Guidelines for the export, shipment, import and release of biological control agents and other beneficial organisms. International Plant Protection Convention, Rome, 32 pp
Kapatos E, Fletcher BS, Pappas S, Laudeho Y (1977) The release of Opius concolor and O. concolor var. siculus against the spring generation of Dacus oleae on Corfu. Entomophaga 22:265–270
Kimani-Njogu SW, Wharton RA (2002) Two new species of Opiinae (Hymenoptera: Braconidae) attacking fruit-infesting Tephritidae (Diptera) in western Kenya. Proc Entomol Soc Wash 104:79–90
Kimani-Njogu SW, Trostle MK, Wharton RA, Woolley JB, Raspi A (2000) Biosystematics of the Psyttalia concolor species complex (Hymenoptera: Braconidae: Opiinae): the identity of populations attacking Ceratitis capitata (Diptera: Tephritidae) in coffee in Kenya. Biol Cont 20:167–174
Knipling EE (1992) Principles of insect parasitism analyzed from new perspectives. Practical implications for regulating insect populations by biological means. US Dep Agric Agric Res Serv Agric Handb 693:1–335
Lopez M, Sivinski J, Rendon P, Holler T, Bloem K, Copeland R, Trostle M, Aluja M (2003) Colonization of Fopius ceratitivorus, a newly discovered African egg-pupal parasitoid (Hymenoptera: Braconidae) of Ceratitis capitata (Diptera: Tephritidae). Fl Entomol 86:53–60
Lux SA, Ekesi S, Dimbi S, Mohamed S, Billah M (2003) Mango infesting fruit flies in Africa – perspectives and limitations of biological approaches to their management. In: Neuenschwander P, Borgemeister C, Langewald J (eds) Biological control in integrated pest management systems in Africa, pp 277–293. CAB International, Wallingford, 414 pp. ISBN: 0-85199-639-6
Mkize N, Hoelmer KA, Villet MH (2008) A survey of fruit-feeding insects and their parasitoids occurring on wild olives, Olea europaea ssp. cuspidata, in the Eastern Cape of South Africa. Biocont Sci Tech 18:991–1004
Mohamed SA, Overholt WA, Wharton RA, Lux SA, Eltoum EM (2003) Host specificity of Psyttalia cosyrae (Hymenoptera: Braconidae) and the effect of different host species on parasitoid fitness. Biol Control 28:155–163
Mohamed SA, Wharton RA, von Mérey G, Schulthess F (2006) Acceptance and suitability of different host stages of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) and seven other tephritid fruit fly species to Tetrastichus giffardii Silvestri (Hymenoptera: Eulophidae). Biol Cont 39:262–271
Mohamed SA, Overholt WA, Lux SA, Wharton RA, Eltoum EM (2007) Acceptability and suitability of six fruit fly species (Diptera: Tephritidae) for Kenyan strains of Psyttalia concolor Szépligeti (Hymenoptera: Braconidae). Biocont Sci Tech 17:247–259
Mohamed SA, Ekesi S, Hanna R (2008) Evaluation of the impact of Diachasmimorpha longicaudata on Bactrocera invadens and five African fruit fly species. J Appl Entomol 132:789–797
Mohamed SA, Ekesi S, Hanna R (2010) Old and new host-parasitoid associations: parasitization of the invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) and five other African fruit fly species by Fopius arisanus, an Asian opiine parasitoid. Biocont Sci Tech 10:183–196
Monaco R (1978) Note sui parassiti del Dacus oleae Gmel. (Dipt. Tephritidae) in Sud Africa. Proceedings XI Congresso Nazionale Italiano di Entomologia, Portici-Sorrento 11:303–310
Monastero S (1931) Un nuovo parassita endofago della mosca delle olive trovato in Altavilla Milcia (Sicilia) Atti della Reale Accademia della Scienze. Lettere e Belle Arti di Palermo 16:195–201
Narayanan ES, Chawla SS (1962) Parasites of fruit fly pests of the world. Beitrage zur Entomologie 12:437–476
Neuenschwander P (1982) Searching for parasitoids of Dacus oleae in South Africa. J Appl Entomol 94:509–522
Neuenschwander P, Bigler F, Delucchi V, Michelakis SE (1983) Natural enemies of preimaginal stages of Dacus oleae Gmel. (Dipt., Tephritidae) in Western Crete. Bionomics and phenologies. Boll Lab Entomol Agrar Filippo Silvestri 40:3–32
Nixon GEJ (1930) The Ethiopian representatives of the Genus Galesus, with descriptions of new species. Ann Ma N Hist Ser 10(6):399–414
Noyes JS (2012) Universal chalcidoidea database. Natural History Museum, London. http://www.nhm.ac.uk/our-science/data/chalcidoids/
Orian AJE, Moutia LA (1960) Fruit flies of economic importance in Mauritius. Revue Agricole et Sucriere de L’Ile Maurice 39:142–150
Ovruski SM, Fidalgo P (1994) Use of parasitoids (Hym.) in the control of fruit flies (Dip.: Tephritidae) in Argentina: bibliographic review (1937–1991). Bull IOBC West Palearctic Reg Sec 17:84–92
Ovruski SM, Schliserman P (2012) Biological control of tephritid fruit flies in Argentina: historical review, current status, and future trends for developing a parasitoid mass-release program. Insects 3:870–888. doi:10.3390/insects3030870
Ovruski SM, Aluja M, Sivinski J, Wharton RA (2000) Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: diversity, distribution, taxonomic status and their use in fruit fly biological control. Int Pest Manag Rev 5:81–107
Purcell MF (1998) Contribution of biological control to integrated pest management of tephritid fruit flies in the tropics and subtropics. Int Pest Manag Rev 3:63–83
Purcell MF, Messing RH (1996) Ripeness effects of three vegetable crops on abundance of augmentatively released Psyttalia fletcheri (Hym.: Braconidae): improved sampling and release methods. Entomophaga 41:105–116
Quilici S, Brevault T, Hurtrel B (2000) Major research achievements in Réunion within the Indian Ocean. In: Price NS, Seewooruthun I (eds) Proceedings of the Indian Ocean commission, regional fruit fly symposium, Flic en Flac, 5–9 June 2000
Quilici S, Hurtrel B, Messing RH, Montagneux B, Barbet A, Gourdon F, Malvotti A, Simon A (2004) Successful acclimatization of Psyttalia fletcheri (Braconidae: Opiinae) for biological control of the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae), on Réunion Island. In: Barnes BN (ed) Proceedings of the 6th international symposium on fruit flies of economic importance, Stellenbosch, 6–10 May 2002, Isteg Scientific Publication, Irene, pp 457–459
Quilici S, Rousse P, Deguine JP, Simiand C, Franck A, Gourdon F, Mangine T, Harris E (2008) Successful acclimatization of the ovo-pupal parasitoid Fopius arisanus in Réunion island for the biological control of the peach fruit fly, Bactrocera zonata. First Meeting of TEAM. Palma of Mallorca, Spain. 7–8 April 2008
Ramadan MM, Messing RH (2003) A survey for potential biocontrol agents of Bactrocera cucurbitae (Diptera: Tephritidae) in Thailand. Proc Hawaii Entomol Soc 36:115–122
Raspi A (1995) Lotta biological in olivicoltura pp 483–495. In: Atti del convegno su: Techniche, norme e qualita’ in olivicolture. Potenza (Italia), 15–17 Dicembre 1993
Raspi A, Loni A (1994) Alcune note sull’allevamento di Opius concolor Szépl. (Hymenoptera Braconidae) e su recent tentativi d’introduzione della specie in Toscana ed in Liguria. Frustula Entomol 17:135–145
Rice RE, Phillips PA, Stewart-Leslie J, Sibbett GS (2003) Olive fruit fly populations measured in central and southern California. Calif Agric 57:122–127
Rivnay E (1968) Biological control of pests in Israel (a review 1905–1965). Isr J Entomol 3:1–156
Rogg H, Camacho E (2000) History of fruit flies and their control in Bolivia. Santa Cruz de la Sierra, SANINET-IICA, Bolivia, 9 pp
Rousse R, Gourdon F, Quilici S (2006) Host specificity of the egg pupal parasitoid Fopius arisanus (Hymenoptera: Braconidae) in La Réunion. Biol Cont 37:284–290
Rwomushana I, Ekesi S, Gordon I, Ogol CKPO (2008) Host plants and host plant preference studies for Bactrocera invadens (Diptera: Tephritidae) in Kenya, a new invasive fruit fly species in Africa. Anns Entomol Soc Am 101:331–340
Schutze MK, Aketarawong N, Amornsak W, Armstrong KF, Augustinos AA, Barr NB, Bo W, Bourtzis K, Boykin L, Cáceres CE, Cameron SL, Chapman TA, Chinvinijkul S, Chomič A, De Meyer M, Drosopoulou E, Englezou A, Ekesi S, Gariou-Papalexiou A, Geib SM, Hailstones DL, Hasanuzzaman M, Haymer DS, Hee AKW, Hendrichs J, Jessup AJ, Ji Q, Khamis FM, Krosch MN, Leblanc L, Mahmood K, Malacrida AR, Mavragani-Tsipidou P, Mwatawala MW, Nishida R, Ono H, Reyes J, Rubinoff DZ, San Jose M, Shelly TE, Srikachar S, Tan K, Thanaphum S, Haq IU, Vijaysegaran S, Wee S, Yesmin F, Zacharopoulou A, Clarke AR (2015) Synonymization of key pest species within the Bactrocera dorsalis species complex (Diptera: Tephritidae): taxonomic changes based on a review of 20 years of integrative morphological, molecular, cytogenetic, behavioural and chemoecological data. Systemat Entomol 40:456–471. doi:10.1111/syen.12113
Silvestri F (1914a) Viaggio in Eritrea per cercare parassiti della mosca dell olive. Bollettino del Laboratorio di Zoologia Generale e Agraria della R. Scuola Superiore d’Agricoltura, Portici 9:186–226
Silvestri F (1914b) Report of an expedition to Africa in search of the natural enemies of fruit flies (Trypaneidae) with descriptions, observations and biological notes Territory of Hawaii Board of Agriculture and Forestry. Div Entomol Bull 3:1–146
Silvestri F (1915) ‘Contributo alla Conoscenza degli Insetti dell’Olivo dell’Eritrea e dell’ Africa Meridionale’, Bollettino del Laboratorio di zoologia generale e agrarian. Portici 9:240–334
Silvestri F (1939) La lotta biologica contro le mosche dei frutti della famiglia Trypetidae. Verhandlungen der VII Internationaler Kongress der Entomologie (Berlin) 4:2396–2418
Sivinski JM (1996) The past and potential of biological control of fruit flies, pp 369–375. In: McPheron BA, Steck GJ (eds) Fruit fly pests: a world assessment of their biology and management. St. Lucie Press, Delray Beach, 586 p
Sivinski J, Aluja M (2012) The roles of parasitoid foraging for hosts, food and mates in the augmentative control of Tephritidae. Insects 3:668–691. doi:10.3390/insects3030668
Steck GJ, Gilstrap FE, Wharton RA, Hart WG (1986) Braconid parasitoids of Tephritidae (Diptera) infesting coffee and other fruits in west-central Africa. Entomophaga 31:59–67
Stibick JNL (2004) Natural enemies of true fruit flies (Tephritidae). United States Department of Agriculture APHIS. PPQ. 86 pp
Thompson WR (1943) A catalogue of the parasites and predators of insect pests. Parasites of the dermaptera and diptera. Imperial Agricultural Bureaux, Slough, 2:99
Thompson FC (1998) Fruit fly expert identification system and systematic information database, the international journal of the North American dipterists’ society, vol 9. Backhuys Publishers, Leiden, p 524
van Achterberg C, Salvo A (1997) Reared Opiinae (Hymenoptera: Braconidae) from Argentina. Zool Med Leiden 71:189–214
van Noort S, Buffington M, Forshage M (2015) Afrotropical Cynipoidea (Hymenoptera). ZooKeys 493:1–176
van Zwaluwenburg RH (1937) West African notes. Hawaiian Plant Rec 41:57–83
Vargas RI, Leblanc L, Putoa R, Eitam A (2007) Impact of introduction of Bactrocera dorsalis (Diptera: Tephritidae) and classical biological control releases of Fopius arisanus (Hymenoptera: Braconidae) on economically important fruit flies in French Polynesia. J Econ Entomol 100:670–679
Vargas R, Badji K, Mckenney M, Leblanc L, Dieng EO (2016) Releases of Fopius arisanus against Bactrocera dorsalis (Hendel) in French Polynesia and Senegal. 3rd international symposium of TEAM (Working group on tephritids of Europe, Africa and the Middle East), 11–14 April 2016, Stellenbosch, South Africa
Vayssières J-F, Wharton RA, Delvare G, Sanogo F (2002) Diversity and pest control potential of hymenopteran parasitoids of Ceratitis spp. on mangos in Mali. In: Proceedings of 6th international fruit fly symposium, Stellenbosch, South Africa pp 461–464
Vayssières J-F, Wharton R, Adandonon A, Sinzogan A (2011) Preliminary inventory of parasitoids associated with fruit flies in mangoes, guavas, cashew, pepper and wild fruit crops in Benin. Biocontrol 56:35–43
Vayssières J-F, Adandonon A, N’Diaye O, Sinzogan A, Kooymann C, Badji K, Rey J-Y, Wharton RA (2012) Native parasitoids associated with fruit flies (Diptera: Tephritidae) in cultivated and wild fruit crops in Casamance, Senegal. Afr Entomol 20:308–315
Wang X-G, Messing RH (2004a) The ectoparasitic pupal parasitoid, Pachycrepoideus vindemmiae (Hymenoptera: Pteromalidae), attacks other primary tephritid fruit fly parasitoids: host expansion and potential non-target impact. Biol Contr 31:227–236
Wang X-G, Messing RH (2004b) Potential interactions between pupal and egg- or larval-pupal parasitoids of tephritid fruit flies. Environ Entomol 33:1313–1320
Wang XG, Bokonon-Ganta AH, Ramadan MM, Messing RH (2004) Egg-larval opiine parasitoids (Hym., Braconidae) of tephritid fruit fly pests do not attack the flowerhead-feeder Trupanea dubautiae (Dip., Tephritidae). J Appl Entomol 128:716–722
Waterhouse DF (1993) Biological control: pacific prospects – Supplement 2. ACIAR Monogr 20:138
Wharton RA (1983) Variation in Opius hirtus Fischer and discussion of Desmiostoma Foerster (Hymenoptera, Braconidae). Proc Entomol Soc Washington 85:327–330
Wharton RA (1987) Changes in nomenclature and classification of some opiine Braconidae (Hymenoptera). Proc Entomol Soc Washington 89:61–73
Wharton RA (1989) Classical biological control of fruit-infesting Tephritidae. In: Robinson AS, Hooper G (eds) Fruit flies, their biology, natural enemies and control, vol 3B. Elsevier, Amsterdam
Wharton RA (1999a) A review of the old world genus Fopius, with description of two new species reared from fruit-infesting Tephritidae. J Hymen Res 8:48–64
Wharton RA (1999b) The status of two species of Psyttalia (Hymenoptera: Braconidae: Opiinae) reared from fruit-infesting Tephritidae (Diptera) on the Indian Ocean Island of Réunion and Mauritius. Afric Entomol 7:85–90
Wharton RA (2006) The species of Sternaulopius Fischer (Hymenoptera: Braconidae, Opiinae) and the braconid sternaulus. J Hymen Res 15:317–347
Wharton RA (2009) Two new species of Psyttalia Walker (Hymenoptera, Braconidae, Opiinae) reared from fruit-infesting tephritid (Diptera) hosts in Kenya. ZooKeys 20:349–377
Wharton RA, Gilstrap FE (1983) Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus s. l. (Diptera: Tephritidae). Anns Entomol Soc Am 76:721–742
Wharton RA, Trostle MK, Messing RH, Copeland RS, Kimani-Njogu SW, Lux S, Overholt WA, Mohamed S, Sivinski J (2000) Parasitoids of medfly, Ceratitis capitata, and related tephritids in Kenyan coffee: a predominantly koinobiont assemblage. Bull Entomol Res 90:517–526
White IM, Elson-Harris MM (1992) Fruit flies of economic significance: their identification and bionomics. International Institute of Entomology, London, xii + 601 p
Willard HF (1920) Opius fletcheri as a parasite of the melon fly in Hawaii. J Agr Res 20:423–438
Willard HF, Mason AC (1937) Parasitization of the Mediterranean fruit fly in Hawaii, 1914–33. US Dep Agric Circ 439:1–17
Wong TTY, Ramadan MM (1987) Parasitization of the Mediterranean and oriental fruit flies (Diptera: Tephritidae) in the Kula area of Maui, Hawaii. J Econ Entomol 80:77–80
Yoder MJ, Wharton RA (2002) Nomenclature of African Psilini (Hymenoptera: Diapriidae) and status of Coptera robustior, a parasitoid of Mediterranean fruit fly (Diptera, Tephrididae). Can Entomol 134:561–576
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Funding for the icipe fruit fly activities came from GIZ/BMZ, Biovision, the EU and DFID.
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Mohamed, S.A., Ramadan, M.M., Ekesi, S. (2016). In and Out of Africa: Parasitoids Used for Biological Control of Fruit Flies. In: Ekesi, S., Mohamed, S., De Meyer, M. (eds) Fruit Fly Research and Development in Africa - Towards a Sustainable Management Strategy to Improve Horticulture. Springer, Cham. https://doi.org/10.1007/978-3-319-43226-7_16
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