New Bait-Based Techniques for the Control of the Peach Fruit Fly Bactrocera zonata (Saunders) and the Mediterranean Fruit Fly Ceratitis capitata (Wiedemann)

Master's Thesis, 2013

76 Pages, Grade: Cum Maxima Laude

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Table of Contents

Chapter 1 Introduction

Chapter 2 Literature Review
2.1. General Information and Statistics
2.1.1. Apricot
2.1.2. Mango
2.2. Use of Pheromones and Parapheromones in Pest Management
2.3. Mediterranean Fruit Fly, Ceratitis capitata (Wiedemann)
2.3.1. Taxonomic Hierarchy
2.3.2. Morphology
2.3.3. Biology
2.3.4. Damage
2.3.5. Integrated Management of C. capitata
2.4. Peach Fruit Fly, Bactrocera zonata (Saunders)
2.4.1. Taxonomic Hierarchy
2.4.2. Morphology
2.4.3. Biology
2.4.4. Damage
2.4.5. Integrated Management of B. zonata
2.4.6. B. zonata in Egypt
2.5. Background of the Study’s Control Strategies
2.6. Control Strategies of the Study
2.6.1. Principles of the A&K Technique
2.6.2. Examples of A&K Systems
2.6.3. Examples of Fruit Fly Attractants

Chapter 3 Materials & Methods
3.1. Zonatrac Male Annihilation Technique
3.2. Ceranock A&K Technique
3.3. Monitoring Traps
3.3.1. McPhail Trap Description
3.3.2. TML in McPhail trap
3.3.3. ME in McPhail trap
3.3.4. Femilure in McPhail trap
3.3.5. DDVP Trapping Strips
3.4. Data Collection
3.5. Biotopes
3.5.1. Apricot Trial
3.5.2. Mango Trial

Chapter 4 Results & Discussion
4.1. Apricot Trial
4.1.1. Trap Catches
4.1.2. Apricot Fruit Damage Assessment
4.2. Mango Trial
4.2.1. Trap Catches
4.2.2. Mango Fruit Damage Assessment
4.3. Statistical Analysis: “t”-test

Chapter 5 Conclusions

Chapter 6 References

List of Tables

Table 1. Principal countries producing apricots in 2011. All volumes are in metric tons. Source: Statistical Division of the Food and Agriculture Organization of the United Nations (FAOSTAT, 2013).

Table 2. Principal producers of mangoes, mangosteens, and guavas in 2011. All volumes are in metric tons. Source: Statistical Division of the Food and Agriculture Organization of the United Nations (FAOSTAT, 2013).

Table 3. GF-120, Magnet MED, and Ceranock A&K systems juxtaposed (Bouagga 2012).

Table 4. Weekly trap catches recorded in 8 TML-baited McPhail traps and 2 Femilure-baited McPhail traps distributed throughout the apricot treatment and control plots between mid-March and early June 2013 at El-Imam El-Ghazaly Village in Al-Beheira Governorate, Egypt.

Table 5. Infested and non-infested fruits (400 apricots) collected from the trees and orchard floor of Plots A, B, and C.

Table 6. Weekly trap catches recorded in 3 Femilure-baited McPhail traps, 6 ME-baited McPhail traps, and 6 TML-baited McPhail traps evenly distributed throughout the mango treatment and control plots at the Royal Property orchards in Al-Sharqiyah Governorate, Egypt, between mid-May and late August 2013.

Table 7. Infested and non-infested fruits (180 mangoes) collected from Plots A, B, and C.

Table 8. Results of the “t”-test on mean catches of different traps in treatment plots against those in control plots of the apricot and mango trials.

List of Figures

Figure 1. Apricots: Production quantities by country in tons (2011 averaged estimates)

Figure 2. Mangoes, mangosteens, and guavas: Production quantities by country in tons (2011 averaged estimates)

Figure 3. Worldwide distribution of the Mediterranean fruit fly Ceratitis capitata (Wiedemann)

Figure 4. Worldwide distribution of the peach fruit fly Bactrocera zonata (Saunders)

Figure 5. Egg, larva, pupae, and adult of the Mediterranean fruit fly Ceratitis capitata (Wiedemann)

Figure 6. Wing of adult Mediterranean fruit fly Ceratitis capitata (Wiedemann)

Figure 7. Life cycle of the Mediterranean fruit fly Ceratitis capitata (Wiedemann)

Figure 8. (a) Female Medfly ovipositing into a peach. (b) Larvae in the pulp of a citrus fruit. (c) Damage due to larval feeding in peaches. (d) Larvae in an apricot dissected during the present study

Figure 9. Dorsal view of a complete adult, head, thorax, and abdomen of the peach fruit fly Bactrocera zonata (Saunders)

Figure 10. Wing of the of the peach fruit fly Bactrocera zonata (Saunders)

Figure 11. Life cycle of the peach fruit fly Bactrocera zonata (Saunders)

Figure 12. Female B. zonata laying eggs into a mango fruit

Figure 13. Damage caused by the feeding of B. zonata larvae in a citrus fruit and a peach fruit

Figure 14. The flycatcher (or McPhail) trap and mothcatcher for pheromone- and parapheromone-mediated pest management

Figure 15. Mating disruption rings, delta trap (monitoring), and colored sticky traps (mass trapping) as pheromone- and parapheromone-mediated techniques for pest management

Figure 16. Components of the Ceranock bait station

Figure 17. Field application of Zonatrac paste using a caulking gun

Figure 18. Ceranock bait stations and their application in field

Figure 19. Trapping strips (DDVP) used in monitoring traps of the trials

Figure 20. McPhail trap installation

Figure 21. Apricot trial site in Al-Beheira, Egypt

Figure 22. Apricot trial: experimental area layout

Figure 23. Ceranock bait station, Zonatrac paste dollop, McPhail monitoring trap, and Trichogramma spp. biocontrol envelope applied in the apricot orchard trial

Figure 24. Mango trial site in Al-Sharqiyah, Egypt

Figure 25. Mango trial: experimental area layout

Figure 26. Sampling data: emergence and accumulation of Medfly trap catches relative to weekly mean temperatures

Figure 27. Comparison between averaged catches of Medfly males in TML traps in Plots A, B, and C

Figure 28. Catches of Femilure-baited traps (2 traps) in treatment plots and the control plot

Figure 29. Incubation and rearing of apricot-infesting larvae for species confirmation

Figure 30. Flies of Genus Muscina attracted by Femilure

Figure 31. (a) Infested and non-infested on-tree and fallen apricots for each plot. (b) Total infested vs. non-infested fruits per plot

Figure 32. (a) Daily mean temperatures of the 101 days of the mango trial. (b) Sampling data: emergence and accumulation of PFF and Medfly trap catches relative to weekly mean temperatures

Figure 33. (a) Male PFF trap catches in Plots A, B, and C over the trial’s period of 13 weeks. (b) Total male PFF catches in each plot at the end of the trial

Figure 34. Total infested vs. non-infested mangoes in each plot

Chapter 1 Introduction

Apricot, Prunus armeniaca (L.) is native of Asia. The tree is small (6–10 m tall), and it has long been cultivated in China, India, Egypt, and Iran. It is now grown in Europe, parts of Africa, and the warmer parts of the New World. This tree is susceptible to frost, so it is grown in warm temperate regions and subtropical regions (Hill, 2008).

According to FAO estimates, the world production of apricots mounted to 3,834,474.7 tons in 2011. In Egypt, the production of apricots was estimated at 96,643 tons in the same year, which constitutes about 2.5 percent of world production (FAOSTAT 2011 estimates). While Egypt is not one of the world's top producers of apricots, the country ranks third globally in terms of highest yields, with a yield of 154,703.06 hectograms per hectare (FAOSTAT 2011 estimates).

The San José scale Quadraspidiotus perniciosus (Comst.), peach twig borer Anarsia lineatella (Zell.), peach fruit fly Bactrocera zonata (Saunders), and Mediterranean fruit fly Ceratitis capitata (Wiedemann) are major insect pests infesting apricot in Egypt. The last two insect pests cause significant economic damage on a number of crops in Egypt, including apricots.

A number of aphids (e.g., the mealy plum aphid Hyalopterus pruni), mealybugs (e.g., the mango giant mealybug Drosicha mangiferae), and scale insects (e.g., the plum scale Parthenolecanium corni) are known to be minor pests infesting apricots (Hill, 2008).

Another important fruit crop that this research is focusing on is mango, Mangifera indica. The center of origin of mangoes is the Indo-Burma region, and the tree grows wild in the forests of Northeast India. Mango is now widely grown throughout the tropical regions for fruit. It is also grown in the subtropical regions as an ornamental or shade tree. The main production areas are India, US State of Florida, Egypt, Brazilian State of Rio Grande do Norte, West Indies, the Philippines, and the eastern coast of Africa. The tree is grown from sea-level to 1500 meters, but grows best below 1000 meters in climates with strongly marked seasons. Dry weather is required for flowering. The tree is susceptible to frost, and the preferred temperature is 25–30°C.

According to FAOSTAT, the world production of mangoes, mangosteens, and guavas was estimated at 38,899,593.02 tons in 2011. In Egypt, the production was estimated at 598,084 tons in the same year, which constitutes about 1.5 percent of world production (FAOSTAT 2011 estimates). Egypt is the world's 14th largest producer of mangoes and the top producing country in the Mediterranean Basin.

In addition to B. zonata and C. capitata, which are major pests on mango in Egypt, other major pests include the coconut scale Aspidiotus destructor (Sign) and the pink hibiscus mealybug Maconellicoccus hirsutus (Green). Minor pests of mango in Egypt include, among others, the long-tailed mealybug Pseudococcus longispinus (Targioni-Tozzetti) and the mango soft scale Kilifia acuminate (Signoret).

Fruit flies are insect pests of great economic importance. There are approximately 4,000 fruit fly species, out of which around 1,200 are members of Family Tephritidae. About 40 percent of the tephritid fruit flies are polyphagous, and the remaining 60 percent attack flowers, stems, leaves, and roots of the host plant. Most of the described fruit flies belong to 5 tephritid genera: Anastrepha, Bactrocera, Ceratitis, Dacus, and Rhagoletis. Genus Bactrocera is the largest and contains about 500 described species—(Frey et al., 2013; El-Heneidy, 2012).

This research is focusing on two tephritid fruit flies of major economic importance on both apricot and mango in Egypt: the peach fruit fly Bactrocera zonata (PFF) and the Mediterranean fruit fly Ceratitis capitata (Medfly).

In 1924, in his work A Monograph of Egyptian Diptera. (Part II. Fam. Trypaneidae), H.C. Efflatoun reported that B. zonata was first detected in Egypt in 1914 in Port Said, but the quarantine interception from an Indian shipment was not confirmed by further records.

According to De Meyer et al. (2007), the first record of B. zonata as an established insect pest in Egypt was in Al-Qalyubia Governorate to the east of Cairo in 1993 on samples of guava, Psidium guajava, and later in the same year in Al-Fayoum Governorate to the southwest of Cairo. The pest was later found to be present in most of Egypt’s governorates.

As the PFF is widely spread in Egypt, it has restricted the presence of the Medfly in horticultural areas (Hashem et al., 2001). It also turns out that a mixed infestation by both fruit flies would actually mostly produce PFFs regardless of which insect infested the fruit first (Mohamed, 2004). This note on mixed infestation by the two fruit flies in Egypt is of particular importance for the interpretation of the results of this study.

Control strategies for B. zonata in Egypt are mainly based on the use of conventional chemical pesticides. Tree trunks are either partially sprayed or baited. Killing bags are used in semi-isolated orchards and in areas with moderate population densities. A number of cultural control methods (e.g., pruning, weeding, and collection of fallen fruits) are relatively considered by farmers for population reduction. Pheromone-mediated control measures are not a common practice (El-Heneidy, 2012).

In a related effort, a PFF eradication program in cooperation with the International Atomic Energy Agency (IAEA) and the FAO is under way in Egypt. The program utilizes the Male Annihilation Technique (MAT) as a method for eradication, and was made available to Egypt in 2000 by an IAEA-funded FAO technical cooperation project (Aleryan, 2006). It might be of relevance to mention that MAT has been found to be more effective than baiting techniques against the PFF in Pakistan (Ali et al., 2010).

Fruit bagging to prevent female oviposition and quarantine measures to prevent the importation of infested fruits are recommended control measures suggested by the procedure for official control followed by the European Plant Protection Organization (EPPO, 2010).

As for the Medfly, control strategies in Egypt are mainly based on sprays of conventional synthetic pesticides (Hashem and El-Halawany, 1996). Broad-spectrum insecticides are generally used. However, it has also been observed during the field visits of this study that an extensive number of homemade traps containing a product called Buminal are used for control. Buminal is a mixture of protein hydrolysate and a generic salt, and the product is used for mass trapping purposes in traps made of plastic bottles.

Fruit stripping is a cultural control measure in which fruits are stripped from host trees, placed in plastic bags, and then buried. Another technique that proved to be successful, though it is not applied in Egypt yet, is the Sterile Fruit Fly Release, in which the orchard is flooded with sterile flies produced in rearing cages. When the sterile flies mate with the fertile population, no offspring are produced. Gradually, the wild flies can find only sterile flies to mate with, and eventually the wild population is eradicated from the agro-ecosystem (Thomas et al., 2001).

In Egypt, the most commonly used control measure against the Medfly and the peach fruit fly in apricot and mango orchards is chemical sprays. Although some unconventional control measures can be found in the large areas owned by some fruit processing firms, other areas of the fragmented agricultural lands owned by "small" farmers have almost exclusively chemical sprays as a control measure. However, as mentioned earlier, it was noted during the field trials conducted for this study that some small farm owners tend to use a primitive type of traps (empty coke plastic bottles with small amounts of a local attractant) as a cheap complementary control measure besides spraying.

Egyptian exporters of agricultural crops, however, often find it difficult to strike a balance between efficient pest management requirements and export market requirements, particularly when it comes to the European export market. This is due to the restrictions imposed by importing countries on the maximum residue limits (MRLs) of pesticides.

This explains the need for applying unconventional controls against agricultural pests, with a total or near total annulment of pesticide application. Nowadays, such a need has utmost priority due to the growing concerns for public health.

Pesticide residues on harvested agricultural goods increasingly put the health of consumers and farmworkers at risk. Between October 1996 and May 1997, a market basket survey for pesticides was conducted in a Caribbean country, and the results showed that 10 percent of the surveyed produce exceeded the internationally acceptable MRLs for the respective pesticides (El-Saeid, 2003).

Also, according to estimates of the World Health Organization and United Nations Environmental Program, each year there are 1 to 5 million cases of pesticide poisoning among agricultural workers, with about 20,000 fatalities mostly reported from developing countries (El-Wakeil et al., 2013).

In a recent experiment conducted in Egypt, 132 samples of fruits, vegetables, herbs, and spices collected from local markets were analyzed for pesticide residues, and contamination with pesticide residues reached 54.55 percent of the samples (72 samples), with one sample violating Codex MRLs. It is worth noting here that 6.06 percent of the contaminated samples had 2 pesticide residues, and 5.3 percent had more than 2 residues. Furthermore, 2 caraway and 1 fennel samples contained 4 pesticide residues; 1 marjoram sample contained 5 pesticide residues; and 1 mint sample contained 6 pesticide residues! Six of the pesticides detected as residues in the analyzed food items were considered to be carcinogenic (Farag et al., 2011).

On the other hand, insecticide resistance (a sort of genetic changes caused by human activity) is another setback of insecticide-based controls. Excessive use of insecticides in pest control activities over the years has contributed to genetically induced resistance in many insect species, a matter which renders pest control efforts less effective.

Insecticides have been extensively used for the control of tephritid flies, which attack a large variety of fruits representing highly-priced commodities in many countries. Due to the nature of fruit flies as highly mobile insect pests with tendency for wide spatial dispersal, their insecticide resistance has been considered to be less evolving than the insecticide resistance of other insects. However, recent studies indicate that selection pressure has already reached the point where insecticide resistance is obviously detectable in fruit flies in the field, which renders control efforts problematic (Vontas et al., 2011).

Such evolving fruit fly insecticide resistance has become a problem in field situations, and a relevant example is the case of Medfly’s resistance to malathion in Spain in such a way that resistance levels have overcome the insecticide concentration used in field treatments (Magaña et al., 2007).

Another relevant example is a study conducted at the Faislabad-based University of Agriculture in Pakistan on PFF resistance to a number of insecticides, where the study results showed that the fly was resistant (3 to 19 fold) to trichlorfon, malathion, lambda-cyhalothrin, and bifenthrin (Ahmad et al., 2010).

From the above, it becomes obvious that there is an urgent need for an alternative approach to the strategy followed for the control of the two fruit flies. One possible solution is the use of the Attract & Kill (A&K) technique and a bait-based Male Annihilation Technique (MAT) as sustainable, eco-friendly, and effective control measures.

Therefore, the objectives of this study are laid out as follows:

- Monitoring and studying the population densities of the PFF and Medfly in apricot and mango orchards in Egypt.
- Evaluating the impact of using the A&K technique Ceranock against both fruit flies on apricot and mango orchards in Egypt.
- Evaluating the impact of using the bait-based MAT Zonatrac against the PFF on apricot and mango orchards in Egypt.

Chapter 2 Literature Review

2.1. General Information and Statistics

2.1.1. Apricot

Apricot, Prunus armeniaca (L.), is a stone fruit that belongs to family Rosaceae. Cultivated throughout the world's temperate regions, apricots are eaten fresh or cooked. While it is originally native to China, apricot is now cultivated in all countries of Central and Southeast Asia. It is also cultivated in parts of South Europe and North Africa (Fig. 1).

Turkey is the leading country in apricot production. Other important producers include Iran, Uzbekistan, Italy, Algeria, the United States, and France (see Table 1 and Fig. 1).

Table 1. Principal countries producing apricots in 2011. All volumes are in metric tons. Source: Statistical Division of the Food and Agriculture Organization of the United Nations (FAOSTAT, 2013)

Abbildung in dieser Leseprobe nicht enthalten

Although apricot trees are susceptible to late spring frosts, they perform best in climates with dry spring weather (Fig. 1). The trees are best planted at about 10 to 20 foot spacing. In Egypt, apricots, which are mostly self-fruitful trees, ripen between mid-June and late June within 100 to 120 days from full bloom (Pittenger, 2002).

Good sanitation practices are normally necessary to control the pests of apricots: all dead or diseased wood should be cut; dried apricots should be removed from the trees; and leaves and fallen debris should be cleared away from the orchard. Before and after use, pruning tools should be disinfected with a 10-percent solution of household bleach, and the areas between trees should also be disinfected with a similar solution. In spring, a horticultural oil should be sprayed on apricot trees at the first sign of green growth for the control of scale insects and a reduction of overwintering mites and aphid eggs (University of Illinois Extension, 2013).

2.1.2. Mango

A tropical fruit belonging to the Anacardiaceae family, mango is native to eastern India and Burma. While several hundred varieties of mango exist, only a few are commercialized. Apart from bananas, the mango is the most consumed tropical fruit worldwide. More than 90 countries grow it (UNCTAD, 2012)—see Fig. 2.

Global production of mangoes has doubled in 30 years to around 35 million metric tons in 2009. Asia, which is the origin of mango, is the largest producer, with 77 percent of world production. Asia is followed by the Americas and Africa with 13 and 10 percent of world production, respectively. India, where the mango is regarded as the “king of fruits,” is the main producer worldwide, with 13 to 17 metric tons annually. China ranks second worldwide with more than 4 metric tons, followed by Thailand (2.5 metric tons) and Pakistan (1.7 metric tons). In the Americas, Mexico (1.5 metric tons) and Brazil (1.2 metric tons) rank 5th and 7th, respectively. The main African mango-producing country is Nigeria followed by Egypt, whose production is estimated at 598,084 metric tons according to FAOSTAT 2011 estimates (UNCTAD, 2012).

Mango is basically a fruit that is consumed locally. Although international trade in mangoes is constantly increasing, it still represents only 3 percent of the volumes produced. This is due to the fact that mangoes, which are delicate and easily perishable fruits, are difficult to sell (UNCTAD, 2012). Another reason is obviously the infestation of mango by fruit flies, a matter which is becoming a major problem facing mango producers, particularly in countries where the PFF is present besides the Medfly.

Table 2. Principal producers of mangoes, mangosteens, and guavas in 2011. All volumes are in metric tons. Source: Statistical Division of the Food and Agriculture Organization of the United Nations (FAOSTAT, 2013)

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2.1.3. Mediterranean Fruit Fly (Medfly)

A major insect pest on apricot and mango in Egypt is the Medfly. The Medfly, which originated in sub-Saharan Africa, is considered the most important fruit fly species worldwide. This is due to its worldwide distribution (a metropolitan pest), its wide range of hosts (400 hosts), and its high tolerance to cool, subtropical, and tropical climates (USDA, 2013)—see Fig. 3. Other reasons behind the massive spread worldwide include the fly’s rapid dispersion mediated by the expansion of world trade, the cultivation of host plants in areas close to human habitats, and the smuggling of prohibited fruits and vegetables in violation of quarantine regulations (Bergsten et al., 1999).

Abbildung in dieser Leseprobe nicht enthalten The fly is recorded in 132 countries and groups of islands in different areas in Africa, Asia, Central America, Europe, North America, Oceania, and South America (Commonwealth Institute of Entomology, 1984).

While the fly has a wide range of hosts including fruit and vegetable hosts, the adults can actually feed on all sorts of protein sources, including animal excreta, in order to develop eggs (Sela et al., 2005).

In the Mediterranean Basin, the Medfly was detected for the first time in 1829 in the Atlantic islands Azores, Madeira, and Cape Verde. It was later reported in Spain (1842), Algeria (1859), Italy (1863), Tunisia (1885), and France (1900) (Mediouni-Ben Jemâa and Boushih, 2010). In 1904, it was reported as a pest in Egypt (Headrick and Goeden, 1996).

Fruit loss due to damage caused by the Medfly is estimated at US$365 million in Mediterranean countries (Lysandrou, 2009). Also, in the Mediterranean Basin, it was noted that the fly causes damage particularly to citrus and peach (Cayol et al., 1994). In Turkey, yield losses due to Medfly infestation are estimated to levels up to 80 percent, if no proper control measures are applied (Elekçioğlu, 2013). In Egypt, fruit damage due to Medfly infestation can be severe in some hosts more than others. A study in a reclaimed desert area in Egypt showed that Medfly infestation can reach levels up to 74 percent on apricot as opposed to only 5.7 percent on Valencia orange (Saleh and El-Hamalawii, 2004).

Another form of damage caused by the Medfly is the fact that it can transmit fungi causing fruit rot (Cayol et al., 1994). A more recent study showed that the fly can even be a potential vector of human pathogens transmitted to fruits. In a lab experiment, Medflies exposed to fecal material enriched with green-fluorescent-protein-tagged Escherichia coli were contaminated with E. coli and were capable of transmitting the bacteria to intact apples placed in a cage. Wild flies were also found to carry coliforms (Sela et al., 2005).

2.1.4. Peach Fruit Fly (PFF)

Another serious insect pest of apricot and mango in Egypt is the PFF. It causes severe damage also to peach and guava. Many other fruits and vegetables are infested by this fly. In certain areas of North India and Pakistan (the region where the pest originally comes from), the PFF has been more notorious than the Oriental fruit fly Bactrocera dorsalis (CAB International, 2011).

A polyphagous insect pest, the PFF has more than 50 hosts (EPPO, 2005). While its origin is South and Southeast Asia, it is now found in more than 20 countries, mostly in Asia. In the Mediterranean Basin, it is found only in Egypt and quite recently in Libya. Only very recently in July 2011, not very far from the Mediterranean Basin, the pest was found to be present in Sudan in three locations in Wad Medan of Al-Gezira State (Salah et al., 2012).

Other Mediterranean/Mid-Eastern countries where the fly is present include Palestine, Saudi Arabia, Yemen, UAE, Oman, Iran (CAB International, 2011), and Lebanon (EPPO, 2010). In Saudi Arabia, the fly was introduced in 1982, and is known to be present as an invasive species in Jazan, Najran, and the southeast region of the kingdom (CAB International, 2011)—see Fig. 4.

Abbildung in dieser Leseprobe nicht enthalten

Because of its wide range of hosts, the PFF can easily adapt and spread after being introduced into a new territory. Its establishment in a newly invaded area is also much helped by its high reproductive potential (up to 564 eggs in a lifetime), high biotic potential (several generations annually), rapid dispersal, and strong flying ability (CAB International, 2011).

The economic impact of the PFF primarily results from the loss of export markets due to quarantine measures imposed by the importing countries. In countries where the pest is present, costly quarantine restrictions and eradication measures are required by local authorities. Furthermore, the establishment of the PFF in an area can seriously impact the environment due to the initiation of chemical and biological control programs (CAB International, 2012).

Crop loss due to PFF infestation also adds to the severity of economic impact, due to the high percentage of fruit damage in infested areas. A striking example is the case in Egypt where crop loss due to the PFF is estimated at 190 million Euros a year, almost 60 percent of the annual costs of damage by the same pest in the entire Near East (320 million Euros)—(EPPO, 2005).

2.2. Use of Pheromones and Parapheromones in Pest Management

There are many chemical and visual lures that can attract insects. They are used to monitor or directly reduce insect populations either by mass trapping or through the A&K technique. Such attractants are used in ways that do not pose a threat to animals or humans as in the case of pesticides, which leave residues on foods and feeds. They are thus used in an environmentally sound manner in integrated pest management (IPM) programs (Weinzierl et al., 1995).

Pheromones are semiochemicals produced and received by individuals of the same species. They influence a range of behaviors and biological processes. However, IPM programs often use compounds that attract a mate (sex pheromones) or call other individuals to a suitable food or nesting site (aggregation pheromones). Other pheromones are used to regulate the caste or reproductive development in social insects (e.g., honey bees and termites), to signal alarm (honey bees, ants, and aphids), to mark trails (ants), and to serve other functions (Weinzierl et al., 1995).

Pheromone traps can be so effective for catching certain insect pests. That is why the use of a sufficient number of traps throughout a pest's environment can substantially reduce the pest’s local population and limit the damage it causes. The process of placing such traps with the aim of reducing an insect pest’s population is termed “Mass Trapping” or “Attract & Kill” (Weinzierl et al., 1995).

The practice of combining insect attractants with insecticides has been used in IPM programs for many years. For example, poisoned bran baits were used for the control of grasshoppers in the early 1900s. The grasshoppers attracted by the treated bran were killed by an insecticide that could not be applied safely, economically, or effectively in any other way.

The process of using a high density of bait stations consisting of an insecticide combined with a lure attracting only male individuals of an insect species is termed a “bait-based Male Annihilation Technique” (MAT). The process aims at reducing the male population of an insect pest to such a low level that mating does not occur.

There are several examples of the successful use of methyl eugenol (ME) in that technique. In the 1960s, the oriental fruit fly Bactrocera dorsalis was eradicated using such a technique from Guam and the Commonwealth of the Northern Mariana Islands. Outstanding successes using this technique have also been achieved for the eradication of the same fruit fly from California and from the Amami Islands of Japan (Secretariat of the Pacific Community, 2002).

2.3. Mediterranean Fruit Fly, Ceratitis capitata(Wiedemann)

2.3.1. Taxonomic Hierarchy

Kingdom: Animalia

Phylum: Arthropoda

Subphylum: Hexapoda

Class: Insecta

Subclass: Pterygota

Infraclass: Neoptera

Order: Diptera

Suborder: Brachycera

Infraorder: Muscomorpha

Family: Tephritidae (Newman, 1834)

Genus: Ceratitis (Macleay, 1829)

Subgenus: Ceratitis (Ceratitis) Macleay, 1829

Species: Ceratitis capitata (Wiedemann, 1824)

Integrated Taxonomic Information System (ITIS, 2013)

2.3.2. Morphology

Egg. Smooth, shiny white, very slender, curved, 1 mm long. The micropylar region is distinctly tubercular (Fig. 5).

Larva. White; cylindrical shape typical of fruit fly larvae; elongate; anterior end narrowed, somewhat recurved ventrally; anterior mouth hooks; flattened caudal end. The last instar is usually 7 to 9 mm in length, with 8 ventral fusiform areas. The anterior buccal carinae are usually 9 to 10 in number. The anterior spiracles are usually nearly straight on dorsal edge of tubule row (often more straight than illustrated in Fig. 5). There are usually 9 to 10 tubules, although there may be 7 to 11.

Pupa. Cylindrical; 4 to 4.3 mm long; dark reddish brown; resembles a swollen grain of wheat (Fig. 5).

Adult. Slightly smaller than a house fly; picture wings typical of fruit flies. The adult fly is 3.5 to 5 mm in length. The color is yellowish with brown tinge, especially on abdomen, legs, and some markings on wings. The lower corners of the face have white setae. Eyes are reddish purple (fluoresce green, turning blackish within 24 hours after death). Ocellar bristles are present (Fig. 5).

The male has a pair of bristles with enlarged spatulate tips next to the inner margins of the eyes. The thorax is creamy white to yellow with a characteristic pattern of black blotches. Light areas have very fine white bristles. Humeral bristles are present. Dorsocentral bristles are anterior of the halfway point between supraalar and acrostichal bristles. The scutellum is inflated and shiny black. The abdomen is oval with fine black bristles scattered on dorsal surface and two narrow transverse light bands on basal half (Thomas et al., 2001).

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Wing. Wings are usually held in a drooping position on live flies. They are broad and hyaline with black, brown, and brownish yellow markings. There is a wide brownish yellow band across the middle of the wing. The apex of the wing's anal cell is elongate. There are dark streaks and spots in the middle of wing cells in and anterior to anal cell (Fig. 6).

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The males are easily separated from all other members of this family by the black pointed expansion at the apex of the anterior pair of orbital setae. The females can be separated from most other species by the characteristic yellow wing pattern and the apical half of the scutellum being entirely black. The female's extended ovipositor is 1.2 mm long.

2.3.3. Biology

Medflies undergo a complete metamorphosis: the flies begin their life as larvae and then transform into completely different-looking adults. Mated females lay their eggs in host fruits approximately 1 mm beneath the pericarp. A female lays only 2 to 10 eggs in the one fruit. However, more than one female can lay eggs in the same location, so that the slim eggs may be clustered together in a single spot of 75 eggs or more (Allen, 2010).

Eggs hatch after 1.5 to 3 days (longer if the temperature is lower). The larvae then carve tunnels, eating their way through the host fruit. Larval life may last only 6 to 10 days (when temperature is around 25ºC). Besides temperature, the type of host fruit affects the length of the larval stage. In citrus fruits, 14 to 26 days may be required for the larvae to reach pupation. Development in a green peach is completed within 10 to 15 days (Thomas et al., 2001).

There are three larval stages or instars. In the first stage, larvae are slender, cream colored, translucent, and about 0.1 cm long. In the second stage, larvae are partly transparent, revealing the fruit in the gut. By the third stage, larvae are opaque white and 0.6 to 0.8 cm long. Medfly larvae can be distinguished from other fruit fly larvae by their thoracic spiracles, with 7 to 11 small protruding tubules (Allen, 2010).

Most larvae begin to pupate at sunrise, an inch or two into the soil. The pupal stage lasts from 6 to 13 days at around 24.4ºC. This range significantly increases (possibly to about 19 days) when the temperature drops to around 20.5ºC. The pupal stage is resistant to temperature extremes and desiccation, so it may last much longer if conditions are not right for emergence.

It is typical for the new adult Medflies to surface on warm mornings. At this early adult stage, they are capable of flying short distances, and may disperse further distances via the wind. (Mau and Kessing, 2007; Thomas et al., 2001)—see Fig. 7.

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2.3.4. Damage

C. capitata is a serious pest to many crops. Damage results from:

1. Oviposition in fruits and soft tissues of vegetative parts of certain plants;
2. Larval feeding;
3. Plant tissue decomposition by secondary microorganisms.

Larval feeding inside fruits is the most severe type of damage. Attacked ripened fruits may develop a water soaked appearance. Young fruits, however, become distorted and usually drop on the ground. The tunnels resulting from larval feeding serve as entry points for bacteria and fungi, which cause fruit rotting (Fig. 8). Medfly larvae also attack the host plant’s young seedlings, succulent taproots, stems, and buds.

Trapping for population detection and population exclusion (using foliage baits), as well as chemical sprays and releases of sterile male Medflies to reduce populations, all require a wide range of resources and can have significant economic implications. Medflies are serious quarantine pests that also affect world trade. The presence of Medflies often calls for quarantine treatments or disinfestation measures for areas of host crops to be certified as fly-free in certification programs. The costs of such phytosanitary regulatory measures can be significant (Global Invasive Species Database, 2010).

As C. capitata is polyphagous, it takes advantage of the various hosts in its surrounding environment and uses them as stepping stones to move on from one fruit tree species to another as fruits mature throughout the season. This eventually gives the flies the ability to destroy an area's entire production of many fruits. Also, such ability to infest multiple fruit species provides Medflies with refuges from control measures, as different fruit species serve as a source of re-infestation to surrounding plots (ibid).

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2.3.5. Integrated Management of C. capitata

Mechanical Control. One of the most effective mechanical control methods is bagging the fruits to exclude egg laying. Trapping is an alternative method that is yet to be proved completely effective.

Cultural Control. The principal cultural control method used for controlling this pest is field sanitation directed toward the destruction of all unmarketable and infested fruits. Infested fruits should be buried 3 feet under soil surface with an addition of sufficient lime to kill larvae. Weekly harvesting keeps the quantity of ripe fruits on the trees to a minimum, thus reducing food sources from which large populations may develop. Other practices that reduce the amount of in-field breeding of Medflies should be used.

Biological Control. According to Mau and Kessing, between 1947 and 1952, 32 entomopathogenic species and varieties of natural enemies to fruit flies were introduced to Hawaii. These parasites lay their eggs in the eggs or maggots of fruit flies and emerge in the pupal stage. Only three— Opius longicaudatus var. malaiaensis (Fullaway), O. vandenboschi (Fullaway), and O. oophilus (Fullaway)— have become abundantly established. These parasites are primarily effective on the oriental and Mediterranean fruit flies in cultivated crops.

A number of other parasites have also been introduced into Hawaii specifically for Medfly control. The most important were the braconid wasps Opius humilis and Diachasma tryoni. Later, parasites of the Oriental fruit fly were found to be destroying the Medfly. They are Biosteres oophilus, B. vandenboschi, and B. longicaudatalisted in order of their effectiveness.

Chemical Control. Chemical sprays have not been completely effective in protecting fruit crops from Medflies. Egg laying requires only a few minutes and chemical residues do not kill adults within this time frame.

The use of proteinaceous liquid attractants in insecticide sprays is a recommended method for controlling adult Medfly populations in the vicinity of crops. Insecticide-bait sprays are applied to broad leaf plants that serve as a refuge for adult Medflies. Baits serve to encourage the adults (especially females) to feed on the spray residue, and can provide good rates of killing. To be effective, insecticide-bait sprays must be used in combination with good sanitation practices (Mau and Kessing, 2007).

2.4. Peach Fruit Fly, Bactrocera zonata (Saunders)

2.4.1. Taxonomic Hierarchy

Kingdom: Animalia

Phylum: Arthropoda Subphylum: Hexapoda

Class: Insecta Subclass: Pterygota Infraclass: Neoptera

Order: Diptera Suborder: Brachycera Infraorder: Muscomorpha Family: Tephritidae (Newman, 1834)

Genus: Bactrocera (Macquart, 1835)

Subgenus: Bactrocera (Bactrocera) Macquart, 1835

Species: Bactrocera zonata (Saunders, 1842)

Integrated Taxonomic Information System (ITIS, 2013)

2.4.2. Morphology

Color. Face with a spot in each antennal furrow; scutum with lateral yellow or orange vittae; scutellum entirely pale colored, except sometimes for a narrow black line across the base; costal margin of wing without a colored band along whole length of cell r1; cell sc usually yellow, and apex of vein R4 + 5 often with a brown spot; crossveins R-M and Dm-Cu not covered by any markings (Fig. 9).

Head . With reduced chaetotaxy, lacking ocellar and post-ocellar setae; first flagellomere at least three times as long as broad (Fig. 9).

Thorax. With reduced chaetotaxy, lacking dorsocentral and katepisternal setae. Post-pronotal lobes without any setae (sometimes with some small setulae or hairs); scutum with anterior supraalar setae and prescutellar acrostichal setae; scutellum not bilobed, with only two marginal setae (the apical pair)—see Fig. 9.

Abdomen. All tergites are separate (view from side to see overlapping sclerites); tergite five with a pair of slightly depressed areas (ceromata); male with a row of setae (the pecten) on each side of tergite three (Fig. 9)— (EPPO, 2005).

Abbildung in dieser Leseprobe nicht enthalten

Wing . Vein sc is abruptly bent forward at nearly 90°, weakened beyond this bend, and ending at subcostal break. Vein R1 with dorsal setulae; cell bcu (= cup) is very narrow, about half depth of cell bm; bcu (= cup) extension is very long, equal to or longer than the length of vein A1 + CuA2; 4–6 mm long. Raised narrow subbasal section of cell br lacking microtrichiae (Fig. 10).

Abbildung in dieser Leseprobe nicht enthalten

2.4.3. Biology

The flies overwinter in the pupal stage, and then adults emerge with the increase of ambient temperature and start mating. After selecting a suitable site for oviposition, a mated female inserts her ovipositor into the host fruit beneath the pericarp and deposits 3 to 9 eggs at one time.

Eggs then hatch within 1 to 3 days, and the larvae feed on the fruit tissue and grow for another 4 to 5 days inside the host fruit. The duration of various immature stages normally varies at different temperatures. No stages develop at 15°C or less, and the optimum temperature is 25 to 30°C (Qureshi et al., 1993).

Full-grown larvae enter the soil under the host plant for pupation, and then adults emerge after 1 to 2 weeks (longer in cool conditions). Adults occur throughout the year. The eclosion of adults from pupae mainly occurs in the early hours of the morning (CAB International, 2011; Rahman et al., 1993)—see Fig. 11.

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For most Bactrocera spp., adults are the only life stage that can best survive low temperatures, with a normal torpor threshold of 7°C. Temperatures survived can even drop as low as 2°C in winter, which explains why the fly is now established in Egypt after it had been originally considered an exclusively tropical fruit fly. This raises questions about the fly’s possible survival during cold winters (EPPO, 2005).

2.4.4. Damage

Signs of oviposition punctures usually appear on attacked fruits. Fruits with high sugar content, such as peaches, exude a sugary liquid droplet that usually solidifies adjacent to the oviposition puncture. The dry droplet appears in the form of a brown, resinous deposit (EPPO, 2005).

On hatching, larvae eat their way into the interior of the host fruit. The activity of first-instar larvae is restricted to the area below the oviposition puncture. However, second- and third-instar larvae are voracious feeders: they go deeper in the host fruit tissue and are responsible for the complete deterioration of host crops (CAB International, 2011)—Fig. 12 and Fig. 13.

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2.4.5. Integrated Management of B. zonata

Sanitary Measures. Proper field sanitation is essential. Infested host fruits are plucked and those on the ground are collected and buried deep in the soil. After harvest, if some fruits are left unpicked on the trees they become the source of later infestation, so all fruits should be picked (Plantwise, 2013).

Physical Control. This type of control is mainly based on the wrapping or bagging of individual fruits to prevent female oviposition. It has proved to be effective (CAB International, 2011).

Chemical Control. Chemical controls based on bait sprays and on relatively less hazardous insecticides like malathion seem to be the most efficient control methods available (Roessler, 1989).

Bait-Based Male Annihilation Technique (MAT). Methyl eugenol is an effective attractant to PFF males. It is mixed with an insecticide and protein bait and used in traps. Attractant-based male annihilation can be effective in substantially reducing an insect’s population area-wide if it is carried out on a large scale. It is also worth mentioning that MAT is officially considered as part of the eradication treatments recommended by the European and Mediterranean Plant Protection Organization (EPPO).

A treatment used by the EPPO procedure for official control of B. zonata is aerial proteinaceous bait sprays. Supplemental eradication methods include ground-applied proteinaceous bait sprays, soil treatment with diazinon, and stripping and disposal of ripe fruits within 200 meters of a confirmed larval site (EPPO, 2010).

Plant Quarantine. Prevention of the PFF from establishing in areas free from the pest is achieved through strict quarantine regulations. Imports of host fruits and vegetables from infested areas without post-harvest disinfestation measures should be prohibited. Thorough checking of travelers’ baggage for infested hosts at entry ports is also essential.

Post-harvest Treatment. Many countries forbid the import of host fruits without a strict post-harvest treatment applied by the exporter in advance. Such treatments include fumigation, heat treatment (hot vapor or hot water), cold treatments, insecticidal dipping or irradiation (Armstrong and Couey, 1989; Armstrong, 1997). Many countries now do not accept both irradiation and methyl bromide fumigation. Heat treatment can reduce the shelf-life of most fruits, and therefore the most effective method of regulatory control is the restriction of imports of a given fruit to areas free from the fly (CAB International, 2011).

2.4.6. B. zonata in Egypt

In 1924, B. zonata was declared present in Egypt. The declaration was based on a detection of the fly in an intercepted consignment in Port Said in 1912. The pest was no longer mentioned for a long period of time, until an intensive tephritid fruit fly survey was initiated by the FAO in the 1980s, but the PFF was not found then. In 1998, the pest was identified for the first time on infested guavas collected in Al-Agamy and Al-Sabahia districts near Alexandria (EPPO, 2013).

In 1999, the first traps that were set up for the fly showed high capture rates in Alexandria and Cairo. In October 2000, the PFF was detected in Al-Arish in North Sinai. A monitoring scheme set up in the North Sinai Governorate involved the installation of 45,000 A&K blocks.

At present, the PFF is considered present and widespread in Egypt, and the situation can be detailed as follows. Mainland : whole Nile Delta region, Nile Valley, and Al-Kharga and Al-Dakhla oases. There are extremely high populations in Cairo (>30 flies per trap per hour in downtown Cairo). Sinai peninsula : Ras Sidr, Al-Tur, and Nuweiba in the South Sinai Governorate. Captures all along the North Sinai Governorate (130 km2 of potential hosts) from Al-Qantara in the northwest to Rafah in the northeast. High populations are found in gardens in Al-Arish city of the North Sinai Governorate (EPPO, 2013).

The pest is also present on the Egypt-Palestine border south of Rafah City. No efficient control action has yet been taken. It is stressed that the pest is present even in very dry areas with few host plants, and even on isolated trees. While the fly is found in peach, apricot, and mango orchards, larger populations occur in gardens with several different fruit trees in a relatively limited area. Although eradication seems to be difficult to achieve nationwide, it appears to be achievable in the Sinai Peninsula (EPPO, 2013).

2.5. Background of the Study’s Control Strategies

Over the twentieth century, different traps and attractants have been developed and applied for the purpose of surveying fruit fly populations. Historically, methyl eugenol (ME) was the first attractant to be used exclusively for male fruit flies in what is referred to now as a bait-based MAT. ME was then followed by kerosene as an attractant to Medflies. In 1956, Angelica seed oil was also utilized as an attractant to Medflies (IAEA, 2003).

Trimedlure (TML) was later found to be an effective attractant to Medfly males (Beroza et al., 1961). Two years later, Beroza and Green (1963) demonstrated that cuelure is an effective attractant to Bactrocera cucurbitae.

Other food baits based on protein solutions, fermenting sugar solutions, fruit juices, and vinegar have been in use since 1918 as attractants for the females of a number of fruit fly species (IAEA, 2003).

Different types of traps are currently used worldwide (see examples in Fig. 14 and Fig. 15). For fruit fly surveys, such traps complement fruit fly control activities and eradication campaigns.

The first trap to be used with protein baits was the McPhail trap. It was later followed by the development of Steiner traps in 1957 and Jackson traps in 1971. While McPhail traps are often used with protein attractants, Jackson traps are used with TML and Steiner traps with ME or cuelure (IAEA, 2003).

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Traps used for fruit flies depend on the nature of the attractant. The most widely used traps contain parapheromone or pheromone attractants that are male specific. The parapheromone TML captures the Medfly and Natal fruit fly. The parapheromone ME captures a large number of Bactrocera species, including the PFF . The parapheromone cuelure also captures a large number of Bactrocera species including B. cucurbitae. The pheromone Spiroketal (SK) captures B. oleae.


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New Bait-Based Techniques for the Control of the Peach Fruit Fly Bactrocera zonata (Saunders) and the Mediterranean Fruit Fly Ceratitis capitata (Wiedemann)
Integrated Pest Management of Mediterranean Fruit and Vegetable Crops
Cum Maxima Laude
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bait-based, techniques, control, peach, fruit, bactrocera, saunders, mediterranean, ceratitis, wiedemann
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Ramy Aljazzar (Author), 2013, New Bait-Based Techniques for the Control of the Peach Fruit Fly Bactrocera zonata (Saunders) and the Mediterranean Fruit Fly Ceratitis capitata (Wiedemann), Munich, GRIN Verlag,


  • guest on 12/5/2014

    thanks Ramy for sharing the knowledge.. wish you the best of luck

  • Ramy Aljazzar on 12/8/2014

    Thanks Amani. I wish you all the best in your endeavors.

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