ذبابة ثمار الزيتون fruit oleae (Rossi) (Diptera: ) Other Scientific Names Bactrocera (Daculus) oleae

Daculus oleae (Gmelin) Dacus oleae (Gmelin) Musca oleae (Gmelin)

Introduction The olive fruit fly, Bactrocera oleae (Rossi) (formerly Dacus oleae), is a serious pest of in most of the countries around the Mediterranean sea. The larvae are monophagous, and feed exclusively on olive fruits. Adults feed on nectar, honey dew, and other opportunistic sources of liquid or semi-liquid food. The damage caused by tunneling of larvae in the fruit results in about 30 percent loss of the olive crop in Mediterranean countries, and especially in Greece and Italy where large commercial production occurs. In Jordan, during heavy infestations more loss occur.

Figure 1. Third instar of the olive fruit fly, Bactrocera oleae (Rossi). Photograph by Giancarlo Dessì, Istituto Professionale Statale per l'Agricoltura e l'Ambiente "Cettolini" di Cagliari.

مناطق االنتشار Distribution Mediterranean basin. Northern, eastern and southern Africa, Canary Islands, India, western Asia, and apparently wherever olives (the genus ) occur in the Eastern Hemisphere. In the Western Hemisphere, it is currently restricted to California in the United States, and Baja California in Mexico (Rice 2000). The olive fruit fly is generally a serious pest of cultivated olives throughout its range. It was detected in California in October, 1998 in the Los Angeles area, and spread to the rest of California (Zalom, Van Steenwyk, Burrack and Johnson 2009).

Distribution Maps Eppo 2015

وصف الحشرة Description Immature stages are similar in appearance to those of other tephritid fruit , especially Bactrocera spp. The adult female is approximately 5 mm long, and has a wing expanse of approximately 10 mm. The wings are mostly transparent and marked with brown, including a spot at the wing tips.

Figure 2. Adult olive fruit fly, Bactrocera oleae (Rossi). Photograph by Natasha Wright, Florida Department of Agriculture and Consumer Services.

Bactrocera oleae (olive fruit fly); aculeus, dorsal view (optical section) of apex. ©CAB International دورة الحياة Life Cycle and In the Mediterranean region, two to five generations of flies occur yearly. The winter is spent in the pupal stage several cm below the soil and leaf litter, and adult flies emerge from March to May, depending upon the latitude and temperature. Under summer conditions, a preoviposition period of 6 to 10 days elapses before mating, with longer time required earlier when temperatures are not as high. During the preoviposition period the female is maturing the ovary and a first set of eggs. Beginning in June females actively seek and oviposit in early maturing olive fruits. From 10 to 12 eggs/day, usually one per olive fruit, and about 200 to 250 are laid in a lifetime. The female punctures the fruit with the and deposits an egg beneath the skin. Eggs are laid just under the fruit's skin, often creating a dimple or brown spot. Multiple generations occur throughout summer and fall. The legless larva (maggot) feeds upon the fruit tissue, causing the fruit to drop off the tree. The egg last 2 to 4 days larva 10 to 14 days about 10 days In summer in Yugoslavia. Duration of the life cycle varies from one to six or seven months. Male flies produce an auditory stridulatory sound or signal during courtship. Courtship and mating occur at dusk, near the end of the daylight period. Females of the olive fruit fly produce a multicomponent pheromone, and are the only tephritid females known to produce a sex pheromone. Males produce the pheromone in other tephritids that have been studied. The major component of the pheromone is 1,7- dioxaspiro[5.5]undecane and it is a relatively long-range attractant for males. Male flies also produce this compound, and attract males, but females are not attracted to the compound from either sex. Feral females likely mate several times during their lifetime.

Hosts Olives - Olea spp.

Olive sectioned to show the egg and the wound caused by the. .

Olive opened to show olive fruit fly maggot and brown internal decay. Photo by Jack Kelly Clark

Olive opened to show olive fruit fly pupa and brown internal decay. Photo by Jack Kelly Clark.

Pupae at soil surface

Olive fruit fly adult exit hole, epidermis 'window' from larval feeding. Photo by Jack Kelly Clark.

Larvae produced during late fall pupate in the soil, where they spend the winter. Although the olive fruit fly does not have a true diapause.

Damage Larvae are the main stage causing damage. egg laying "stings"

Brown spots on olive fruit made during egg-laying by olive fruit fly. Fruit drop, or direct pulp destruction by larvae that renders fruit useless for canning.

Olive with internal decay and feeding tunnels of olive fruit fly larvae. Photo by Jack Kelly Clark Larval feeding allows microorganisms to invade the fruit, causing rot and lower oil quality. In areas of the world where olive fruit fly is established and not controlled, its damage has been responsible for losses of up to 80% of oil value because of lower quantity and quality, and in some varieties of table olives, this pest is capable of destroying 100% of the crop. Some European districts cannot grow table olives because control of olive fruit fly is not economical. The expense of treatments and the likely crop damage have the potential for eliminating olive culture in home orchards or as a viable commercial industry in California.

Hosts/Species Affected This species has a very narrow host range, being restricted to Olea spp. In Europe, it attacks cultivated olives but in Africa it is associated with wild olives. In a study of host trees infested by B. oleae in California, USA, Athar (2005) noted that olives were the preferred host, but trees in the families Rosaceae, Rutaceae, Anacardiaceae, Fabaceae, Lythraceae and Malpighiaceae were also infested. The hosts were mainly fruit trees, with the exceptions of Brazilian pepper tree (Schinus terebinthifolia), carob (Ceratonia siliqua), crape myrtle (Lagerstroemia indica) and ornamental plum (Prunus domestica).

Brazilian pepper tree (Schinus terebinthifolia)

Carob (Ceratonia siliqua)

Crape myrtle (Lagerstroemia indica)

المكافحة Management In the Eastern Hemisphere, insecticides are used in bait-sprays or as sprays from the air to control the olive fruit fly. More environmentally benign techniques that are being tested or used in limited areas are use of radiation sterilized males and pheromones. Both sexes can be sterilized when late pupae are exposed to the irradiation. Synthesis of 1,5,7-trioxaspiro[5.5]undecane, an analog of the major pheromone component, has been synthesized and tested, and under optimal conditions it was as attractive as the natural compound, but it did not last as long in traps as the natural material. Small plywood rectangles dipped in 0.1% (a.i.) aqueous solution of deltamethrin for 15 minutes and added to bait stations containing either sex pheromone or ammonium bicarbonate, a food attractant, gave cost-effective control in a large test orchard. In California, management depends on bait sprays, trapping of adult flies, harvest timing, fruit sanitation after harvest, biological control (Van Steenwky et al. 2003). A recent (2008) introduction of a hymenopteran , Psyttalia cf. concolor, (: ) from Kenya has raised hopes for effective biologicial control of the olive fruit fly. The wasp appears to be a more effective natural enemy than other olive fly brought to California in the early 2000s. Early results showed that the wasp's rate was variable in some hot, dry, inland groves, where the olive fruit fly is sparse, but in a coastal orchard heavily infested with the flies, parasitism was very high (Wood 2009).

Figure 4. The parasitoid Psyttalia cf. concolor was discovered in Kenya, reared in a laboratory in Guatemala, and imported into California for biological control of olive fruit fly. Photograph by Peggy Greb, USDA.

Technician Gina Miller prepares a cage of parasitoids to release into olive trees infested with olive fruit fly in a suburban area of San Jose, California. Photo by Peggy Greb.

Agricultural engineers Eric Jackson (left) and Ron Haff examine x-ray images in efforts to develop a sorting machine to detect olives infested with the olive fruit fly. Photo by Peggy Greb.

Olive fruit fly adult caught with other in a yellow sticky trap. Photo by Jack Kelly Clark.

Surveying fruit for infestation can give some indication of the severity of an infestation. Looking for maggots infesting fruit that has fallen from trees in late winter and spring is useful, as it will give some indication of overwintering olive fly numbers. Adult fruit flies can be monitored with McPhail, Olipe or yellow sticky traps. Plastic McPhail traps have proven to be more effective than yellow sticky traps in catching larger numbers of olive fruit flies and catching them earlier in the season. However, yellow sticky traps baited with a pheromone lure or ammonium bicarbonate may be easier to use.

Biological Control Native parasites (in California) have been observed attacking olive fruit fly pupae, but these wasps appear to be generalists that are only present when fly numbers are high. Paphiopedilum concolor, a non-native parasite that can be raised in culture has been released for other fruit flies including the Mediterranean fruit fly. Preliminary releases have been attempted in California with limited success to date.

Opius concolor parasitizing larvae The female of this hymenopterous deposits its egg in the larva through the skin of the olive.

Natural Enemies

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Biological Natural enemy Type Life stages Specificity References Biological control in control on

Asecodes erxias Parasite

Belonuchus Predator Italy olives rufipennis Biosteres Parasite Greece olives longicaudatus

Bracon celer Parasite Larvae Italy olives

Carabus banonii Predator

Cirrospilus Parasite Larvae Italy olives variegatus

Coptera silvestrii Parasite cricket paralysis Pathogen virus

Cyrtoptyx latipes Parasite

Diachasmimorpha Parasite Greece olives tryoni

Euderus cavasolae Parasite Larvae Italy olives

Biological Natural enemy Type Life stages Specificity References Biological control in control on

Eupelmus afer Parasite Italy olives

Eupelmus ater Parasite Larvae Italy olives

Eupelmus urozonus Parasite Larvae Greece; Corfu olives

Eurytoma Parasite Larvae/Pupae

Eurytoma martellii Parasite

Halticoptera daci Parasite Larvae Italy olives

Iridovirus Pathogen

Mesopolobus Parasite Larvae Italy olives modestus Neochrysocharis Parasite Larvae formosa Nucleopolyhedrosis Pathogen virus Crete; France; Greece; Palestine; Italy; Khalki; Mediterranean

Opius concolor Parasite olives region; Sicily; Spain; Yugoslavia

Opius dacicida Parasite Larvae Italy olives

Opius lounsburyi Parasite

Opius tephritivorus Parasite Larvae Italy olives

Biological Natural enemy Type Life stages Specificity References Biological control in control on

Opius trimaculatus Parasite Italy olives

Pnigalio agraules Parasite Greece; Corfu olives

Crete;France;Greece;Israel;Italy;Khalki;Mediterranean

Psyttalia concolor Parasite Larvae olives region;Sicily;Spain;Yugoslavia

Pterostichus creticus Predator

Scolopendra cretica Predator

small RNA viruses Pathogen

Tetrastichus Parasite

Triaspis daci Parasite Larvae Italy olives

Trichosteresis glabra Parasite

Belonuchus rufipennis

Carabus banonii

Psyttalia concolor Cultural Control Sanitation is important in reducing overall fly densities. Remove old fruit remaining on trees following harvest and destroy all fruit that are on the ground by either burying at least 10 cm inchs deep or taking to the landfill. Extremely high fly populations can occur in fruited varieties of landscape trees and in unmaintained ornamental situations. These can be a significant source for invasion of commercial groves. Prevent fruiting on landscape trees in spring by using a chemical such as naphthaleneacetic acid (NAA; Olive Stop) or destroy fruit on the ground in fall to reduce this invasion pathway. An areawide approach is needed to reduce olive fly densities where commercial plantings are near ornamental or unmaintained trees. Olive fruit fly adults feed on honeydew. Reducing black scale populations may reduce a food source needed during high summer temperatures. Organically Acceptable Methods Cultural controls, the use of GF-120 Naturalyte Fruit Fly Bait (spinosad), sprays of kaolin clay, and mass trapping are acceptable for use in an organically certified crop.

Monitoring and Treatment Decisions Traditionally, there is zero tolerance for damage on table fruit. About 10% for oil olives. But after sensory evaluation it was determined that the 10% threshold is very conservative. Orchards can tolerate damage up to 100% if the damage is caused by stings or tunnels in unripe fruit and there is less than 1% fruit rot. Olives can be used for processing into oil as long as the fruit is not rotten (brown, soft, or showing decay). The most important aspect of damage levels for oil olives is that the fruit should be harvested early to avoid rot. Olives damaged by fruit fly larvae develop ripe fruit flavors even when fruits are still green. This makes it possible to harvest fruit early, but still produce tasteful . Rotten fruit, not just the presence of olive fly larvae, leads to off flavors in the oil. Flavor is affected when between 1 to 3% of the fruit is spoiled. Process infested fruit as soon as possible after harvest (24 hours or less) or hold in cold storage until processed. While there is no relationship between fruit damage and the number of insects found in traps, surveying trap catches can evaluate treatment efficacy by comparing trap catches before and after treatment (when less flies should be caught). Mass trapping and monitoring devices Adult fruit flies can be monitored with McPhail, Olipe or yellow sticky traps.

 For all trap types, place traps in fruiting trees by March 1 in warmer locations.

 Place traps in the second tree row, or further in, to reduce dust accumulation in the traps.

 Hang the traps mid-canopy, in the shade (north side of the tree), and in an open area to avoid leaves blocking the trap.  Record numbers of flies trapped weekly. The number of flies in the traps likely will decline during the course of a hot summer and increase as the weather cools in late summer. Although traps reduce damage, they are more useful as monitoring devices. Traps should not be used as a stand-alone treatment, in part because of their inconsistent ability to attract and trap adult flies and because traps can not compete with olive fruit as the fruit becomes more attractive. McPhail traps McPhail traps are plastic or glass containers with a reservoir for liquid baits. Yellow McPhail traps appear to be superior to red or clear traps.

Flies enter from the bottom of the trap through an opening and drown in the solution. Recommended baits to use in these traps are yeast or NuLure bait. The addition of pheromones in liquid traps does not increase trap catches. Torula yeast catches more flies earlier than ammonia-based lures.

 Place 2 traps for each 20 to 40 Dunums (5 to 10 acre) block of trees to evaluate treatment efficacy.

 More traps per block are necessary to evaluate fly activity or density.

 For mass trapping, place one trap in each tree.

 Use 3 to 4 yeast tablets per trap and change monthly.

 In hot weather add water to the trap to replace what evaporates, maintaining correct bait concentrations. However, weekly maintenance may be necessary during hot and dry weather.  McPhail-type Ball traps are larger than standard McPhail traps and therefore do not dry out as fast, making maintenance more time efficient. They may also trap more flies.

  Bactrocera oleae (olive fruit fly); McPhail trap loaded with protein attractant for monitoring olive fruit fly populations. Chania, Kolymvari, Crete, Greece. October, 2014. ©Kiki Varikou-2014

 To count trapped flies, empty the trap contents into a sieve so that the liquid drains out and the flies can be identified and counted.

 It is easiest to empty the trap contents (including the liquid) into a labeled plastic container with a snap lid while in the field. The sieving, counting, and disposal of the liquid can be done away from the orchard. Do not leave the used liquid in the orchard. Olipe trap Olipe traps are made with 1.5 to 2 liter plastic non-food bottles, with several 4 to 5 mm sized holes drilled or melted at the top, and baited with 3 to 4 torula yeast tablets per liter of water. Pheromones may or may not increase trap catches.

 Place 2 traps for each 20 to 40 Dunums (5 to 10 acre) block for monitoring and one trap per tree for mass trapping control.  Mass trapping usually does not work as a stand-alone treatment, but can supplement the efficacy of other treatments or reduce the number of treatments by reducing the overall number of flies in the orchard. Flies attracted to the bait, crawl into the bottle through the holes at top, and drown.

 Change the bait solution monthly. Use the same method to count trapped flies as with McPhail traps. Yellow sticky traps Yellow sticky traps are baited with a sex pheromone (spiroketal), an ammonium bicarbonate attractant, or both. The sex pheromone attracts the males. Ammonium bicarbonate attracts both males and females. Both lures can be combined in one trap, but pheromones may not increase trap catches.  Place 2 traps for each 20 to 40 Dunums block for monitoring and one trap per tree for mass trapping control..

 Replace the yellow sticky traps once a month or more often if they get wet, contaminated with non-target insects, or dusty such that they are no longer sticky.

o Replace spiroketal lures every 4 months and ammonium bicarbonate packets every 2 weeks.

o The spiroketal lure must be pierced with a pin (e.g., a small map pin or insect pin) before using.

o Some types of ammonium bicarbonate packets must be pierced with something larger than a pin to produce an opening of at least 1 mm so that sufficient vapors will escape.

o Ammonium bicarbonate packets made by PaCoast have a peel- off cover that exposes a release area on one side.

 Sticky traps may be more difficult to use than McPhail traps. Attract and kill traps The Magnet OL trap attracts flies with a food lure on every trap and sex pheromone on every fourth trap. The traps contain a pyrethroid insecticide, which kills the flies when they land. The traps are designed to be effective for about five months (usually May through September for table olives and July through November for oil).

For mass trapping, large numbers of traps are needed (up to one trap per tree). They are most effective when fly numbers are very low in oil olives and where orchards are isolated from nearby untreated trees. Bait and deterrent sprays Research indicates that bait and deterrent sprays are very effective in managing olive fruit fly. Both spray treatments provide consistent damage reduction and can be used as a sole management tool. If used in conjunction with a mass-trapping device they can provide exceptional control of the olive fruit fly. Bait and insecticidal sprays Applications of bait sprays (GF-120 Naturalyte) are very effective and should begin when trap captures begin to increase in early summer. If flies are captured in spring and the orchard has a history of damage, begin spinosad bait treatments at pit hardening or when fruit reach about 10 mm in length (the point when flies begin to sting fruit and larvae can develop). Once initiated, continue to apply bait sprays according to label directions to protect the crop until harvest. Apply at least to every other tree row at biweekly intervals. If fly captures begin to increase in late summer but few fly stings on fruit are found, continue treatments with spinosad, kaolin clay, or both. However, if the number of stung fruit is increasing or if greater than normal numbers of flies are being captured in traps, treat with fenpropathrin (Danitol). Fenpropathrin is a relatively inexpensive pyrethroid, which may tempt a grower to use it early and often, but early season or excessive use of fenpropathrin can lead to a treadmill effect that can increase mite or scale numbers. Therefore, the routine use of fenpropathrin as a cover spray should be avoided unless significant damage is anticipated.

Kaolin clay sprays Apply kaolin clay sprays (Surround WP) when olives become attractive to the fly, which is usually in early June or when the fruit reaches pea size.

Host camouflaging of Surround WP. After M.ANTONAKOU, TH. ARAPOGIANNIS and P. ROUSSOS. Completely coat leaves and fruit. After the spray dries it turns into a white powdery coat, which acts as a repellant to olive flies. Repeat every 5 to 6 weeks, which is approximately three times during the season. It can be used successfully in orchards with high fly numbers. Because of the need to completely cover fruits and leaves, which makes this treatment expensive, one application just before most olive fruit fly damage occurs (late in season) is probably most practical, most economical, and may be sufficient for oil olives, especially if the fruit is harvested early. The clay will need to be rinsed from the fruit before processing.

Sterile Insect Technique (SIT)

SIT is an environmentally-friendly and species-specific method of pest control based on the release of large numbers of sterilised insects (Dyck et al., 2005). Competition for mating between wild and sterile males results in a decrease in the number of fertile matings and a decline in the overall population size. SIT has been successfully implemented against various pest insect species including several Tephritidae. However, despite decades of research aimed at developing an olive fly SIT programme using radiation-sterilised flies (Economopoulos et al., 1977), consistently poor results led to the eventual abandonment of trials. Key issues included: low quality of the radiation-sterilised mass-reared flies Eeconomical production of sufficient numbers of sterilised flies, Assortative mating of released and wild populations because of different preferred mating times. Laboratory-reared wild-type flies were found to mate several hours earlier than wild flies.

Data in this lecture from H.V. Weems Florida Department of Agriculture and Consumer Services

UC IPM Pest Management Guidelines: Olive, UC ANR Publication 3452 and Eppo data sheet 2015 and other internet photos.