Intensity of Infestation by Fruit on Traditionally Grown ("gerif") Snake melon (Cucumis melo var. flexuosus) and Squash (Cucurbita pepo) in Khartoum State

By Ekhlas Ahmed Fadelmola Mohammed B.Sc. (Agric) Honours University of Khartoum 2002

A thesis submitted in partial fulfillment of the requirements for the degree of M.Sc. Crop Protection

Supervisor Dr. Kamal Mowafi Abdel Fattah

Department of Crop Protection Faculty of Agriculture University of Khartoum

May 2008

Dedication

To my Mother

Ekhlas...

i

ACKNOWLEDGEMENT

Thanks firstly to the great Alla.

Sincere thanks to my supervisor Dr. Kamal

Mowafi Abdel Fattah for his help throughout this study.

Special thanks are due to Sharaf Eldeen Dawood,

Director General of Plant Protection Directorate, who gives me this chance.

Iam also greatful to Dr. Eltigani Eltahir,

Dr. Elwasila Gadura, Professor Saad Abbady and

Professor Abdalla Mohammed, Department of

Horticulture.

My deep thanks are to my husband, family, friends, colleagues, farmers and the many who helped me.

ii

LIST OF CONTENTS Title page Dedication...... i Acknowledgements...... ii List of Contents...... iii List of Tables...... v List of Figures...... vi List of Plates………………………………………………………… vii Abstract...... viii Arabic abstract...... ix CHAPTER ONE: INTRODUCTION...... 1 CHAPTER TWO: LITERATURE REVIEW...... 4 2.1. Introduction...... 4 2.2. Dacus ciliatus (Loew)...... 5 2.3. Description...... 6 2.3.1. Dacus ciliatus (Loew)...... 6 2.3.2. Dacus vertebratus (Bezzi)...... 6 2.4. Geographical distribution...... 7 2.5. Host range...... 8 2.6. Damage...... 10 2.7. Life history...... 10 2.8. Influence of biotic and abiotic factors on distribution of fruit flies 14 2.8.1. Temperature...... 14 2.8.2. Humidity...... 15 2.8.3. Host plants...... 15 2.8.4. Natural enemies...... 16 2.9. Strategies for integrated management of melon fruit ...... 17 2.9.1. Bagging of fruit...... 17 iii

2.9.2. Field sanitation...... 17 2.9.3. Monitoring and control with pheromone...... 18 2.9.4. Biological control...... 19 2.9.5. Host plant resistance...... 20 2.9.6. Chemical control...... 21 2.9.7. Male-sterile technique...... 21 2.9.8. Quarantine...... 22 CHAPTER THREE: MATERIALS AND METHODS...... 23 3.1. Fields surveyed...... 23 3.2. Intensity of infestation...... 23 3.3. Species identification...... 25 3.4. Effect of temperature and moiture on the development of the

cucurbit fly larvae (days)...... 25

3.5. Exposure of the cucurbit flies pupae to the sunlight...... 26

CHAPTER FOUR: RESULTS...... 30 4.1. Intensity of infestation...... 30

4.1.1. Intensity of infestation by fruit fly in snake melon...... 30

4.1.2. Intensity of infestation by fruit fly in squash ...... 30

4.2. Species identification ...... 30

4.3. Effect of temperature and moisture on the development of the

cucurbit fly larvae (days)...... 30

4.4. Effect of sunlight on the mortality of cucurbit flies pupae...... 31

CHAPTER FIVE: DISCUSSION...... 39 CONCLUSION AND RECOMMENDATIONS...... 43

REFERENCES……………...... 45 iv

LIST OF TABLES

Title Page

Table 1: Intensity of infestation by fruit fly in snake melon at Aburoof

and Eljumoeya area...... 32

Table 2: Intensity of infestation by fruit fly in squash at Aburoof and

Khartoum area...... 34

Table 3: Effect of temperature and moisture on the development of the

cucurbit fly larvae (days)...... 36

Table 4: Effect of sunlight on the mortality of cucurbit flies ...... 38

v

LIST OF FIGURES

Title Page

Figure 1: Intensity of infestation by fruit fly in snake melon at Aburoof and Eljumoeya area...... 33 Figure 2: Intensity of infestation by fruit fly in squash at Aburoof and Khartoum area...... 35 Figure 3: Effect of temperature and moisture on the development of the cucurbit fly larvae (days)...... 37

vi

LIST OF PLATES

Title Page

Plate 1: The cage...... 27

Plate 2: The pupae...... 28

Plate 3: The adult...... 29

vii

ABSTRACT

A survey was carried out in the traditional cultivation areas

("gerif") on banks of the Nile (Aljamoia), the Blue Nile (near the

University of Khartoum) and the White Nile (Aburoof) to study the infestation of the cucurbit fruit flies Dacus spp on snake melon and squash.

The infestation level on snake melon ranged 4.35-9.03% at

Aburoof area and 14.63-26.41% at Aljamoia area. The infestation level on squash crop ranged 0-1.17% at Aburoof area and 0-0.2 % at Khartoum area.

Collection of infestation samples of snake melon, squash and melon from Aburoof, Blue Nile, Eljumoeya, Sleit and Amdoum revealed that the infesting fruit flies is identification as Dacus ciliatus only, according to the Agricultural Research Corporation-Wad Madani.

The study of the effect of sunlight on the pupae of the fruit fly

Dacus ciliatus, mortality of the pupae the increased with the increase of exposure time.

It is found that high tempreture and moisture excaralated the larval development in the black plastick bages (2.67 days) compared with the rearing cages (6.67 days).

viii

ﻤﻠﺨﺹ ﺍﻷﻁﺭﻭﺤﺔ

ﺃﺠﺭﻱ ﻤﺴﺢ ﺤﻘﻠﻲ ﺒﻤﻨﺎﻁﻕ ﺍﻟﺯﺭﺍﻋﺔ ﺍﻟﺘﻘﻠﻴﺩﻴﺔ (ﺍﻟﺠﺭﻭﻑ) ﻋﻠﻰ ﻀﻔﺘﻲ ﺍﻟﻨﻴـل ﺍﻷﺒـﻴﺽ

(ﺍﻟﺠﻤﻭﻋﻴﺔ) ﻭﺍﻟﻨﻴل ﺍﻷﺯﺭﻕ (ﺒﺎﻟﻘﺭﺏ ﻤﻥ ﺠﺎﻤﻌﺔ ﺍﻟﺨﺭﻁﻭﻡ ) ﻭﻨﻬﺭ ﺍﻟﻨﻴل (ﺃﺒﻭﺭﻭﻑ) ﻟﺩﺭﺍﺴﺔ ﻜﺜﺎﻓﺔ

ﺁﻓﺔ ﺫﺒﺎﺒﺔ ﻓﺎﻜﻬﺔ ﺍﻟﻘﺭﻋﻴﺎﺕ .Dacus spp ﻋﻠﻲ ﻤﺤﺼﻭﻟﻲ ﺍﻟﻌﺠﻭﺭ ﻭﺍﻟﻜﻭﺴﺔ.

ﻭﺠﺩ ﺃﻥ ﻤﺴﺘﻭﻯ ﺍﻹﺼﺎﺒﺔ ﻋﻠﻰ ﻤﺤﺼﻭل ﺍﻟﻌﺠﻭﺭ ﻴﺘﺭﺍﻭﺡ ﺒـﻴﻥ 4.35-9.03 % ﻓـﻲ

ﻤﻨﻁﻘﺔ ﺃﺒﻭ ﺭﻭﻑ ﻭ 14.63-26.63% ﻓﻲ ﻤﻨﻁﻘﺔ ﺍﻟﺠﻤﻭﻋﻴﺔ . ﻭﻤﺴﺘﻭﻯ ﺍﻹﺼﺎﺒﺔ ﻓﻲ ﻤﺤـﺼﻭل

ﺍﻟﻜﻭﺴﺔ ﻴﺘﺭﺍﻭﺡ ﺒﻴﻥ 0-1.17% ﺒﻤﻨﻁﻘﺔ ﺃﺒﻭﺭﻭﻑ ﻭ 0-0.2 % ﺒﻤﻨﻁﻘﺔ ﺍﻟﺨﺭﻁﻭﻡ.

ﺘﻡ ﺠ ﻤﻊ ﻋﻴﻨﺎﺕ ﻤﻥ ﺍﻟﺜﻤﺎﺭ ﺍﻟﻤﺼﺎﺒﺔ ﻟﻤﺤﺼﻭل ﺍﻟﻌﺠﻭﺭ ، ﺍﻟﻜﻭﺴﺔ ﻭﺍﻟﺸﻤﺎﻡ ﻤـﻥ ﻤﻨـﺎﻁﻕ

ﺃﺒﻭﺭﻭﻑ،ﺍﻟﻨﻴل ﺍﻷﺯﺭﻕ (ﺒﺎﻟﻘﺭﺏ ﻤﻥ ﺠﺎﻤﻌﺔ ﺍﻟﺨﺭﻁﻭﻡ )، ﺍﻟﺠﻤﻭﻋﻴﺔ، ﺍﻟـﺴﻠﻴﺕ ﻭﺃﻡ ﺩﻭﻡ ﻟﻴﻭﻀـﺢ

ﺘﺼﻨﻴﻑ ﺍﻵﻓﺔ Dacus ciliatus . ﻜﻤﺎ ﺘﻡ ﺘﺼﻨﻴﻔﻬﺎ ﻓﻲ ﻫﻴﺌﺔ ﺍﻟﺒﺤﻭﺙ ﺍﻟﺯﺭﺍﻋﻴﺔ ﺒﻤﺩﻨﻲ.

ﻭﺠﺩ ﺘﺄﺜﺭ ﺃﺸﻌﺔ ﺍﻟﺸﻤﺱ ﻋﻠﻰ ﻋﺫﺍﺭﻯ ﺫﺒﺎﺒﺔ ﺍﻟﻔﺎﻜﻬﺔ Dacus ciliatus , ﻤﻭﺕ ﺍﻟﻌﺫﺍﺭﻯ

ﻴﺯﺩﺍﺩ ﺒﺯﻴﺎﺩﺓ ﻓﺘﺭﺓ ﺍﻟﺘﻌﺭﺽ.

ﻭﺠﺩ ﺃﻥ ﺍﺭﺘﻔﺎﻉ ﺩﺭﺠﺔ ﺍﻟﺤﺭﺍﺭﺓ ﻭﺍﻟﺭﻁﻭﺒﺔ ﻴﺴﺭﻉ ﻓﻲ ﻨﻤﻭ ﻴﺭﻗﺎﺕ ﺍﻟﺤﺸﺭﺓ ﻓﻲ ﺍﻷﻜﻴـﺎﺱ

ﺍﻟﺒﻼﺴﺘﻴﻜﻴﺔ ﺍﻟﺴﻭﺩﺍﺀ (2.67 ﻴﻭﻡ) ﻤﻘﺎﺭﻨﺔ ﺒﺄﻗﻔﺎﺹ ﺍﻟﺘﺭﺒﻴﺔ (6.67 ﻴﻭﻡ).

ix

i ii iii iv v vi vii viii ix

CHAPTER ONE

INTRODUCTION

Fresh vegetables could contribute greatly to the economy of the

Sudan. Sudan can produce and export a number of fresh vegetables to the

European and other markets, which will provide a good source of foreign currency. This is because of the availability of vast arable land, reasonable supply of irrigation water and a varied suitable climatic condition.

Around Khartoum there are two major vegetable production units

The Arab development company (3.000 feddans in Oumdum) and the

Seleit Scheme (27.000 feddans in Khartoum North area).

Traditionally the production of vegetables in Khartoum State was by "gerif" cultivation on the banks of the Nile and its tributaries. The increase of the population of the urban areas in Sudan increased the demand for the vegetables.

Cucurbitaceae is among the most important plant families that supply man with edible products. It has characteristic chemistry which makes it an important family that could supply useful medicines for different diseases. The main cucurbits productes are melons, cucumber, and squash for both local markets and export.

The fruit flies (family ) are of a major economic importance because they attack important fruit crops in tropical and

1 subtropical regions of the world. A number of recent invasions by tephritids have been observed, despite quarantine procedures (White et al ., 2000 ; Allwood et al ., 2002 and Duyck et al ., 2004).

The genus Bactrocera is the most economically important one gnificant genus, with about 40 species considered to be important pests

(White and Elson-Harris, 1992); many of them are highly polyphagous.

The females ovipuntures cause deformation and rotting of fruits due to the entry of microorganisms which affect both yield and quality.

It is a major pest in Sudan affecting cucurbits (mostly melon), particularly in Kassala and Gash Delta , Khartoum area and Northern

Sudan (Guddoura et al., 1984; Siddig, 1984 and Ahmed, 1994).

Bezzi (1916) believed that this species is primarily of Ethiopian origin and that it might have spread to other African and Asian countries.

Schmutterer (1969) reported that, the family Tephritidae was considered the fourth ranking group of pests causing serious damage to fruit crops in Sudan. Four species, of Tephritid fruit flies: the oriental fruit fly, Dacus dorsalis (Hendle), the melon fruit fly, Dacus cucurbitae (Coquillett), Malaysian fruit fly Dacus latifrons (Hendel) and the mediteranean fruit fly Ceratitis capitata (Weid.) were found to be the most destructive flies in Hawaii (Nishida et al., 1985).

This work is infended to survey some of the main production areas of vegetables, for both local consumption and exportation, in Khartoum

2 State to determine the incidence, intensity of infestation, and the occurrence of the infesting species of fruit flies in each area.

The work is designed to aid the management of these pests.

3 CHAPTER TWO

LITERATURE REVIEW

2.1. Introduction

The family Tephritidae of the order Diptera contains over 4000 species, of which nearly 700 species belong to Dacine fruit flies (Fletcher,

1987). Nearly 250 species are of economic importance, and are distributed widely in temperate, subtropical, and tropical regions of the world (Christenson and Foote, 1960). The first report on melon fruit flies was published by Bezzi (1913), who listed 39 species from India.

Forty three species have been described under the genus

Bactrocera including cucurbitae, drosalis, zonatus, diversus, tau, oleae, opiliae, kraussi, ferrugineus, caudatus, ciliatus, umbrosus, frauenfeldi, occipitalis, tryoni, neohumeralis, opiliae, jarvisi, expandens, tenuifascia, tsuneonsis, latifrons, cucumis, halfordiae, cucuminatus, vertebrates, frontalis, bivittatus, amphoratus, binotatus, umbeluzinus, brevis, serratus, butianus, binotatus, umbeluzinus, brevis, serratus, butianus, hageni, scutellaris, aglaia, visendus, musae, newmani, savastanoi, diversus, and minax, from Asia, Africa, and Australia (Syed, 1969; Cavalloro, 1983;

Drew and Hooper,1983 ; Munro, 1984 and Fletcher ,1987). Among these,

Bactrocera cucurbitae (Coquillett) is a major threat to cucurbits (Shah et al., 1948). Senior-White (1924) listed 87 species of Tephritids in India.

4 Among these, the genus, Bactrocera (Dacus) caused heavy damage to fruits and vegetables in Asia (Nagappan, et al; 1971).

It is a serious pest in Sudan, throughout the country especially in

Khartoum State threatening the production and export of the sweet melon

(PPD, 2007).

2.2. Dacus ciliatus (Loew)

Dacus ciliatus (Loew) belongs to the family Tephritidae

(Trypetidae) is highly destructive to commercially grown fruits and vegetable crops throughout the world. Common names, Ethiopian fruit fly, lesser pumpkin fly, Cucurbit fly.

Synonyms are Dacus appoxanthus var. decolor (Bezzi), Dacus brevistylus (Bezzi), Dacus insisten (Curran), Dacus sigmoides

(Coquillett), Didacus ciliatus (Loew), Leptoxyda ciliate (Loew) and

Tridacus mallyi (Munro).

Dacus ciliatus was generally found in association with Dacus vertebratus, there is a very close similarity between Dacus brevistylus and Dacus ciliatus. They were thought to be the same species (Bezzi,

1924).

Later the taxonomic studies of Munro (1932) confirmed that Dacus brevistylus and Dacus sigmoids (Coquillett), were actually synonyms of

Dacus ciliatus.

5 Notes on and nomenclature for phytosanitry purposes, non European Tephritidae collectively have long been considered as quarantine pests for EPPO and the EU. This category included a large group of Dacus spp. According to a recent taxonomic revision, most of these Dacus spp. are now renamed Bactrocera and are covered in a separate data sheet (EPPO/CABI, 1996). Dacus ciliatus is the only important species which remains in Dacus.

2.3. Description

2.3.1. Dacus ciliatus (Loew)

Dacus ciliatus has been described under two different names,

Dacus ciliatus and Dacus brevistylus by many workers (Bezzi, 1916 and

1924 and Silvestri, 1914).

A predominantly orange species with facial spots, 2 scuttles setae, a yellow spot covering most of the katatergite, anatergite orange, mid femur yellow or orange yellow and wing with a costal band that is expanded apically to form an apical spot. Male with a pecten. Scutum without yellow stripes, anterior supra-alar setae and prescutellar acrostichal setae (White and Harris, 1994).

2.3.2. Dacus vertebratus (Bezzi)

It is commonly known as the cucumber or the vegetable marrow fly, is quite similar to Dacus ciliatus (Loew) in morphological characters, and for sometime these two were considered to be the same species

6 (Bezzi, 1916). It was also found, commonly feeding in close association with Dacus ciliatus and causing the same type of damage on cucurbit fruits (Bishop, 1934 and Hargreaves, 1927). According to Bezzi, 1915,

1916 and 1924; Hargreaves, 1927; Bishop, 1934 and Strofberg, 1946),

Dacus vertebratus has been known to occur in Ethiopia, South Africa,

Zanzibar, Uganda, and Transvaal as a serious pest of cucurbits, both cultivated and wild.

A predominantly orange species, with facial spots, 2 scutellar setae, a yellow stripe covering most of anatergite and katatergite, all fermora darkened in apical half, and wing with a costal band that is expanded apical spot. Male with a pecten. Scutum without yellow stripes, anterior supra-alar setae and prescutellar acrostichal setae (White and Harris,

1994).

2.4. Geographical distribution

Dacus ciliatus (Loew) is presumably confined mainly to African continent and to a lesser extent present in Asia.

Bezzi (1915) had reported the receipt of specimens of the insect from Africa. It was originally described from Eritrea and probably later got introduced into South India. The reporting of Dacus species in the

Sudan by Theobaled (1906) is probably refering to Dacus ciliatus, as the characters mentioned agree with that of ciliatus. It was found in Africa

7 (White and Harris, 1994) and Asia (Fletcher, 1987 and Waterhouse,

1993).

2.5. Host range

Dacus ciliatus is primarily a pest of the members of the family

Cucurbitaceae, both cultivated and wild, but host plants belonging to families like, Rutaceae, Solanaceae are also reported (Ali, 1967).

Schmutterer (1969) reported Dacus ciliatus and Dacus vertebratus from cucurbits mainly, and Sarcophaga destructor on cucurbits, tomato and egg plant. A list of known host plants of Dacus ciliatus are tabulated below.

8 Common Name Scientific name Reference

Musk Cucumis melo Narayanan, 1953; Narayanan and Batra, 1960; melon Cucumis melo var. conomon Wen, 1985; Pareek and Kavadia, 1994; Allwood et al., 2002; Weems and Heppner, 2001.

Pumpkin Cucurbita maxima Back and Pemberton, 1917; Narayanan, 1953; Cucurbita pepo Narayanan and Batra, 1960; Wen, 1985; Pareek Cucurbita moschata and Kavadia, 1994; Hollingsworth et al., 1997; Allwood et al., 2002; Weems and Heppner, 2001. Narayanan, 1953; Cucumber Cucumis sativus Narayanan, 1953; Narayanan and Batra, 1960; Pareek and Kavadia, 1994; Allwood et al., 2002; Weems and Heppner, 2001. Water melon Citrulus vulgaris Narayanan, 1953; Narayanan and Batra, 1960; Citrulus lanatus Pareek and Kavadia, 1994; Allwood et al., 2002; Weems and Heppner, 2001. Squash melon Benincasa hispida Narayanan and Batra, 1960; Back and Cucumis vulgaris. pemberton, 1917; Narayanan, 1953; Allwood et Fistulosus al., 2002; Weems and Heppner, 2001. Wild cucurbits Cucumis melon Narayanan, 1953; Narayanan and Batra, 1960; Cucumis melon var conomon Uchida et al., 1990; White and Elson- Harris, 1994; Weems and Heppner, 2001; Dhillon et al., 2005b. Wild snake gourd Cucurbita maxima Narayanan, 1953; Narayanan and Batra, 1960. Cucurbita pepo Cucurbita moschata Tomato Lycopersicon esculentum Narayanan, 1953; Narayanan and Batra, 1960; Ranganath and Veenakumari, 1997; Weems and Heppner, 2001; Fontem et al., 1999. Sunflower Helianthus annus White and Elson- Harris, 1994. Sweet corn Zea mays White and Elson- Harris, 1994. Guava Psidium guajava Narayanan, 1953; Narayanan and Batra, 1960; Wen, 1985. Date palm Phoenix dactylifera Narayanan, 1953; Narayanan and Batra, 1960. Mango Mangifera indica Narayanan and Batra, 1960; Weems and Heppner, 2001. Orange Citrus sinensis Narayanan and Batra, 1960; Weems and Heppner, 2001.

9 2.6. Damage

The melon fruit fly damage is the major limiting factor in obtaining good quality fruit and high yield (Srinivasan,1959; Lall and Singh, 1969;

Mote, 1975; Rabindranath and Pillia,1986). It prefers young, green, and tender fruits for egg laying by piercing them with ovipositor. After eggs hatching, the maggots feed inside the fruits. The fruit rots and contamination was spread. Secondary like Musca domestica and

Drosophilla were found to entre fruits for egg laying. The larvae of these secondary flies, further contribute to the rotting. Later the epidermal layers of the rind, dry up and attain brownish colour, which appear as a healed up wound. At this stage the fruits curl, twist and attain yellow in colour. The damaged fruits, when left in the field attracted termites (Ali,

1967).

Dhillon et al (2005) reported that the extent of losses vary between

30 to 100% depending on the cucurbit species and the season.

2.7. Life history

Mating of the flies under captivity was seldomly noticed during the day. It generally took place soon after sunset. The process of copulation lasted for about 20 minutes in the laboratory.

The egg is shiny, whitish, elongated, narrower at one end and slightly curved. It measures 1-2 mm in length. In the case of cucurbit fruits, the eggs were laid to depth varying from 2 to 4 mm. Egg laying

10 process was found to continue for nearly 30 minutes. The incubation period was 1-2 days in the laboratory. The viability (hatching %) under the laboratory condition was 70%.

The larva was found to undergo three moults. The first instar invariably fed on the tender soft seeds. The 2nd larval instar resembles the first, in general morphological characters, but bigger in size and darker in colour and also more active. The 2nd instar is creamy yellow in colour, and has the peculiar habit of curling and jumping when placed on a smooth surface. This habit helps in the dispersal of the larvae far away from the infested fruits for pupation. The 3rd moult was a concealed one within the puparium giving rise to the 4th larva larva instar, which is described by some workers as the prepupal stage. It measures about 9 mm in length. The anterior end is tapering and provided with a heavily sclerotized pair of mouth parts or hooks. The larvae generally preferred the damp soil under infested fruits for pupation (Ali, 1967).

Foote and Blank (1963), mentioned that the insects of the family,

Tephritidae, undergo 3 moults. The duration of larval period, reared on cucurbit fruit, was 3-4 days, under laboratory conditions in Sudan (Ali,

1967), and 4-6 days in October under laboratory conditions in India

(Cherian and Sundaram, 1939) . Mason (1916) recorded the larval period as 22 days.

11 The 3rd larva instar turned into a pupa passing through a very short larval stage with in the puparium. Pupation occurred inside the fruits, but emergence of the flies was hampered due to the wet conditions in the rotting fruit, and also sometimes due to the absence of an exit hole. In the laboratory, pupation took place under the filter papers.

The adult on emergence from the puparium pushed its away out through the soil particles or through cracks in the soil. The adult emerged by pushing through the cap of the puparium. The head appeared first.

When the front and middle legs were out they further assisted in pushing back the puparium. The depth of pupation was found to vary from 1-3.3 cm depending upon the soil type and structure. The puparium is oval, vary in colour from cream yellow to pale brown, and about 6 mm in length. The pupal period was 12 days under laboratory conditions (Ali,

1967). Mason (1916) recorded the pupal period as 9-11 days.

A detail description was given ealier of the adult. Newly emerging flies were pale yellow in colour, and the wings appeared short and remained folded. The brownish hues appeared over the body in a few minutes after emergence, and the wings quickly unfolded, and they immediately started feeding.

Emergence of flies took place in the early hours of the day. In nature, the flies were active during the day. In captivity, flies preferred mostly to remain at the top of the rearing cage, alighting for feeding and

12 oviposition only. In captivity, males were always found restlessly moving about in the cage. The females lived longer than the males (Ali, 1967).

The melon fruit fly remains active throughout the year on one or more hosts. The lower developmental threshold for melon fruit fly was recorded as 8.1°C (Keck, 1951). The lower and upper developmental thresholds for eggs were 11.4 and 36.4 °C (Messenger and Flitters, 1958).

The accumulative day degrees required for egg, larvae and pre egg laying adults were recorded as 21.2, 101.7 and 274.7 day degrees, respectively

(Keck, 1951). This species actively breeds when the temperature falls bellow 32 °C and the relative humidity ranges between 60 to 70 %. Fukai

(1938) reported the survival of adults for a year at room temperature, if fed on fruit juices. In general, the life cycle lasts from 21 to 179 days

(Fukai, 1938 and Narayanan and Batra, 1960).

Development from egg to adult takes 13 days at 29 °C in Solomon

Islands (Hollingsworth et al., 1997). High temperature, long period of sunshine, and plantation activity influence the Bactrocera cucurbitae abundance in the North east Taiwan (Lee et al., 1992). Bhatia and Matho

(1969) reported that the life cycle is completed in 36.3, 23.6, 11.2 and

12.5 days at 15, 20, 27.5 and 30 °C respectively. There are 8 to 10 generations in a year (White and Elson, 1994 and Weems and Heppner,

2001). Munro (1925) under South Africa conditions estimated a period of one month for the whole life cycle.

13 2.8. Influence of biotic and abiotic factors on distribution of fruit flies

Tephritids distribution and abundance are markedly structured by various abiotic and biotic factors which have a direct effect on species distribution, but also an indirect effect, by modulating interspecific competition.

Several factors might affect fruit fly distribution and competition including:

2.8.1. Temperature

Temperature has a marked influence on tephritid development and survival. Many comparative studies have been conducted to determine threshold and thermal constants for different species (Messenger and

Flitters, 1958; Crovetti et al., 1986; Delrio et al., 1986, Kasana and

Aliniazee,1994.; Yang et al., 1994; Vargas et al., 1996, 1997, 2000;

Brevault and Quilici, 2000 and Duyck and Quilici, 2002). These studies showed that the dominant species may differ depending on temperature, particularly as a function of latitude or altitude. For instance, in Reunion island, Ceratitis capitata dominates Ceratitis rosa in the low land areas of the west, where temperature are highest, while C rosa is dominant in the uplands (Etienne, 1972), which tallies with the minimum development thresholds for the species (Duyck and Quilici, 2002 and Duyck et al.,

2004). Similarly, in Hawaii, Bactrocera drosalis is dominant almost throughout the island, Ceratitis capitata subsists in the uplands. It is to be

14 noted that, in this latter case, old records exist that mention the abundance of C.capitata in the low lands before the establishment of Bactrocera drosalis (DeBach, 1966), which supports the hypothesis of modulation as a result of interspecific competition by temperatures.

2.8.2. Humidity

The optimum relative humidity for development ranges from 60 to

70% then tend to decline very much in number to the dry season (dead), when partically no cultivated cucurbits are available. Also in the rainy months (July- August), the population remained nearly the same as in dry season (Ali, 1967). Only a few studies have looked at the impact of relative humidity on pupal development, despite the fact that it may be a major factor in species distribution. For example, in Reunion island,

Ceratitis catoirii is dominanted by other species but subsists in narrow costal strip in the east and south of the island where there is more rainfall.

2.8.3. Host plant

Host fruit species and quality both affect immature larval development and adult behavior. In a study of five species of Dacini fruit flies, Fitt (1986) showed that the abundance of species on different host fruits was due more to the choices made by females than to larval specialization. However, while many host plants can sustain the full development of different tephritid species, host quality governs major differences in survival rate, larval development and adult fecundity.

15 The nutritive value of the fruit has a major impact on larval development

(Fernandes. Da-Silva and Zucoloto, 1993).

Carey (1984) showed that the larval development time of Ceratitis capitata at 25 °C could increase from around a week on a favourable host such as mango (Mangifera indica L.) to over 3 weeks on quince (Cydonia oblonga (Miller)).

In Hawaii, the greater competitiveness of larvae on certain host fruits was shown at least partly to account for the competitive displacement of Ceratitis capitata by Bactrocera drosalis (Keiser et al.,

1974).

A field experiment was designed to study host plants preferred by

Dacus ciliatus by Ali (1967). The result showed that Cucumis sativus,

Cucumis melon var fllexusus and Cucurbita pepo, were preferred, respectively.

2.8.4. Natural enemies

In a few cases, natural enemies have been shown to play a key role in the population dynamics of some tephritid species, such as Rhagoletis cerasi (Boller and Remund, 1989). In this species a high mortality of pupae in the soil caused by predators was demonstrated. It is, however, probable that the impact of generalist predators such as ants would affect more or less equally different tephritid species in a given biotope.

16 Several natural enemies have been reported from different parts of

Africa and India on the various stages of Dacus ciliatus, but no study was made to evaluate the role of these natural enemies.

2.9. Strategies for integrated management of melon fruit fly

The fruits of cucurbits, for which the melon fly is serious pest, are picked up at short intervals for marketing and self consumption.

Therefore, it is difficult to rely on insecticides as a means of controlling this pest. In situations where chemical control of melon fruit fly becomes necessary, one has to rely on soft insecticides with low residual toxicity and short waiting periods. Therefore, keeping in view importance of the pest and crop, the melon fruit fly management could be done using local management or wide area management.

2.9.1. Bagging of fruits

Akhtaruzzaman et al., (1999) suggested bagging of cucumber fruits at 3 days after anthesis, and the bags should be retained for 5 days for effective control. It is an environmental safe method for the management of this pest.

2.9.2. Field sanitation

The most effective method in melon fruit fly management use the primary component, field sanitation. To break the reproduction cycle and population increase, growers need to remove all unharvested fruits or vegetables from a field and completely burying them deep into the soil.

17 Burying damaged fruits 0.46 m deep in the soil prevents adult fly eclosion and reduces population increase (Klungnes et al., 2005).

2.9.3. Monitoring and control with pheromone

The principal of this particular technique is the denial of resources needed for laying by female flies such as protein food (protein bait control) or para pheromone lures that eliminate males. There is a positive correlation between cure lure trap catches and weather conditions such as low temperature, rain fall, and low humidity. The set attractant cure lure traps are more effective than food attractant tephrit lure traps for monitoring the Bactrocera cucurbitae in bitter gourd. Methyl eugenol and cue lure traps have been reported to attract Bactrocera cucurbitae males from mid-July to mid-November (Ramsamy et al ., 1987; Zaman, 1995;

Liu and Lin, 1993).

A leaf extract of Ocimum sanctum, which contains eugenol (53.4%), beta caryophyllene (31.7%) and beta elemene (6.2%) as the major volatiles, when placed on cotton pads (0.3mg) attract flies from a distance of 0.8 km (Roomi et al.,1993). Thus, melon fruit fly can also be controlled through the use of Ocimum sanctum as the border crop sprayed with protein bait (protein derived from corn, wheat or other sources) containing spinosad; (is a metabolite from the soil actinomycete

Saccharopolyspora spinosa).

18 It is a mixture of the two most active naturally occurring secondary metabolites from aerobice fermentation of S. spinosa: spinosyns A and D

(Sparks et al., 2001) as a toxicant. Cure lure traps have been used for monitoring and mass trapping of the melon fruit flies in bitter gourd

(Pawar et al.,1991; Permalloo, et al ., 1998 and Seewooruthun, et al .,

1998). Maize can also be used as a border crop for melon fruit fly attraction through application of bait (Dhillon et al., 2005).

2.9.4. Biological control

There are no reports on the successful use of bio-control agents against the melon fruit fly. Srinivasan (1994) reported Opius fletcheri silv to be a dominant parasitoid of B. cucurbitae, but efficacy of this parasitoid has not been tested under field conditions in India. The parasitization of B. cucurbitae by Opius fletcheri has been reported to vary from 0.2 to 1.9% in Mcharantia fields in Honolulu at Hawaii (Wong et al., 1989). Similar level of parasitization (3%) was also reported from northen India by Nishida (1963). However, Willard (1920), Newell et al.,

(1952) and Nishida (1955) have reported parasitization at level of 80.44 and 37%, respectively, from Hawaii. Thus, there is a need to reevaluate the parasitization potential of Opius fletcheri berore its exploitation as biological agent for the management of Bactrocera cucurbitae.

A Mexican strain of the nematode, Steinernema carpocapscae

Weiser (Neoaplectana carpocapsae), has been reported to cause 0 to 86%

19 mortality to melon fruit fly after an exposure of 6 days to 5000 to

5,000,000 nematodes/cup in the laboratory, and an average of 87.1% mortality under field conditions when applied at 500 infective juveniles/ cm2 soil (Lindegren, 1990). Sinha (1997) reported that culture filtrate of the fungus, Rhizoctonia solani (Kuhn), to be an effective bio agent against B. cucurbitae larvae. While, the fungues, Gliocladium virens oeigen, has been reported to be an effective against Bactrocera cucurbitae (Sinha and Singh, 1998). Culture filtrates of the fungi

Rhizoctonia solani, Trichoderma viridae (Pers), and Gliocladium virens adversely affected the oviposition and development of Bactrocera cucurbitae (Sinha and Saxena, 1999).

The efficacy of most of these bio agents is under field conditions.

Therefore, there is a need to evaluate the efficacy of these bio control agents against B. cucurbitae for practical use in integrated pest management programes (Sinha and Saxena, 1999).

2.9.5. Host plant resistance

Host plant resistance is an important component in integrated pest management programes. It does not cause any adverse effects to the environment, and no extra cost is incurred to the farmers. Unfortunately success in developing high yielding fruit fly-resistant varieties has been limited. There is a distinct possibility of transferring resistance genes in the cultivated genotypes from the relatives of cucurbits for developing

20 varieties resistant to melon fruit fly through wide hybridization. The soureses of resistance are Bitter gourd, resistance, Pal et al., 1984.

Pumpkin, High resistance, Nath, 1966 Nath. Wild melon, High resistance,

Chelliah, 1970.

2.9.6. Chemical control

Chemical control of the melon fruit fly is relatively ineffective.

However, insecticides such as malthion, dichlorvos, phosphamidon, and endosulfan are moderately effective against the melon fly (Agarwal et al.,

1987). The application of molassest malthion (Limithion 50 EC) and water in the ratio of 1: 0.1:100 provides good control of melon fly

(Akhtaruzzaman et al., 2000).

2.9.7. Male sterile technique

In this technique, sterile males are released in the field for mating with the wild females. Sterilization is accomplished through irradiation, chemicals, or genetic manipulation. In sterile insect programme the terms

"sterility" or sterile insect refer to the transmission of dominant lethal mutations that kill the progeny.

A sterile insect programme is specific, and is considered an ecologically safe procedure and has been successfully used in area-wide approaches to suppress or eradicate insect pests in entire regions such as the pink bollworm, Pectinophora gossypiella in California (Walters et al.,

2000). Although the sterile insect technique can be used successfully to

21 suppress economically important pest species, conventional sterilization by ionizingradiation reduces insect fitness, which can result in reduced competition of the sterilized insect (Horn and Wimmer, 2003).

2.9.8. Quarantine

The import and export of infested plant material from one area or country to an other non infested places is a major mode of spread of insect pests. Import controls carried out in airports in France since 1993 on tropical fruits have revealed the presence of 12 non-European and one

European species of Tephritidae (Bayart et al., (1997).

The control in Sudan depend on local efforts, In Sinar State, they used pheromone traps contain malthion 57% and methyl eugeinol 9:1.

They used 20 traps, and randomly took 6 traps after 24 hours. The average number of insects about 300 males in traps, against Ceratitis capitata in guava, and Ceratitis cosyra in mango (PPD, 2006).

At Alfky Hashim, the plant protection diroctory of Khartoum State used diazinon 60% ml, sugar mg, yeast ml and water ml in the ratio of 20:

100:10:100 against Bactrocera invidance in mango. The experment is still under evaluation (PPD, 2008).

22 CHAPTER THREE

MATERIALS AND METHODS

3.1. Fields surveyed

This survey was carried out at many fields selected randomly on the banks of rivers "gerif", namely Aburoof, Eljumoeya (west Omdrman), and Blue Nile bank at Khartoum near University of Khartoum, where cucurbits were grown. The soils of these areas are classified as silty clay loam.

3.2. Intensity of infestation

To estimate the infestation by fruit fly in snake melon (Agor) at

Aburoof, five harvest pickings were inspected in an area of 1960 m2 previously selected. The harvest picks interval was 5 days and the first harvest pick was on 12/11/2006. The infested fruits were separated by hand and counted as well as the non infested. The sowing date of snake melon was 2/10/2006.

Twenty to thirty infested fruits of the same size were randomly collected from each field, kept in plastic bags and brought to the laboratory for identification of the infesting fruit fly species.

Also to estimate the infestation by fruit fly in snake melon

(Abu selka) at Eljumoeya, five harvest picks were inspected in 2500 m2 area selected previously. The harvest picks interval was 5 days and the first harvest pick was on 10/12/2006. The infested fruits were separated

23 by hand and counted as well as the non infested. The sowing date of snake melon was 28/10/2006.

Twenty to thirty infested fruits of the same size were randomly collected from each field, kept in plastic bags and brought to the laboratory for identification of the infesting fruit fly species.

To estimate the infestation by fruit fly in squash (Almani) at

Aburoof, five harvest picks were inspected in a previously selected area of 2600 m2. The harvest interval was 3 days and the first harvest pick was on 10/12/2006. The infested fruits were separated by hand, then infested and non infested fruits were counted. The sowing date of squash was

2/10/2006.

Five to ten infested fruits of the same size were collected randomly from each field, kept in plastic bags and brought to the laboratory for identification of the infesting fruit fly species.

To estimate the infestation by fruit fly in squash at Blue Nile bank, five harvest picks were inspected in an area 2340 m2 selected previously.

The harvest interval was 3 days and the first harvest pick was on

22/11/2006. The infested fruits and non infested fruits were separated by hand and counted. The sowing date of squash was 7/10/2006.

Five to ten infested fruits of the same size were randomly collected from each field, kept in plastic bags and brought to the laboratory for identification of the infesting fruit fly species.

24 3.3. Species identification

The collected infested fruits (melon, squash and snake melon) from

(Aburoof, Eljumoeya, Blue Nile bank near University of Khartoum, Sleit and Amdoum) were transferred in the black plastic bags to the laboratory and kept in rearing cages at 25-27 °C.

The cages are made of wood (30*30*39 cm), the top and the three sides were made of wire mesh, the front side covered with thin muslin cloth, the bottom was made of soft wood and sandy layer was placed for pupation (Plate 1).

The pupae were transferred to Petri-dishes, provided with moistened filter papers in empty rearing cages, and then observed daily for adult emergence (Plate 2).

The emerged insects were fed in laboratory with diet made of yeast and sugar 1:4 dissolved in 500 ml of distilled water. The emerged adults were sent for identification to the Agriculture Research Corporation in

Wad Madni (Plate 3).

3.4. Effect of temperature and moiture on the development of

the cucurbit fly larvae (days)

It had been observed that when infested fruits of snake melon are left in the bags, the larvae die or pupate early. Four infested fruits of snake melon were kept in black plastic bags in the laboratory and other

25 four in bages until the pupation. Three replicates were used for each treatment.

3.5. Exposure of the cucurbit flies pupae to the sunlight

To study the effect of the sunlight exposure on pupae, five pupae were chosen from the rearing cages and transferred to Petri-dishes half filled with sand. The exposure period was 1, 3 and 5 days respectively.

Three replicates were used for each treatment with control. After the exposure period the treated pupae were transferred to other Petri dishies provided with wet filter papers and kept in the laboratory. The death of pupae was considered after 4-11 days.

26

Plate 1: The cage

27

Plate 2: The pupae

28

Plate 3: The adult

29 CHAPTER FOUR

RESULTS

4.1. Intensity of infestation

4.1.1. Intensity of infestation by fruit fly in snake melon The infestation percentage of snake melon variety at Aburoof area ranged between 4.35 and 9.03%, and at Eljumoeya area ranged between

14.63 and 26.41%. These values indicate that the infestation level at

Eljumoeya was greater than that at Aburoof (Table 1 and Figure 1).

4.1.2. Intensity of infestation by fruit fly in squash

The infestation percentage of squash variety at Aburoof locality rrange between 0 and 1.17%, and at Khartoum area ranged between 0 and

0.15%. These values indicate that the infestation level at Aburoof was greater than that at Khartoum (Table 2 and Figure 2).

Generally the infestation level was very low in squash variety.

4.2. Species identification

Dacus ciliatus was the only species of fruit flies on cucurbits in

Khartoum State.

4.3. Effect of temperature and moisture on the development of

the cucurbit fly larvae (days)

The development period of larvae of Dacus ciliatus was less in the black plastic bags 2.67 days with more mortailty, compared with that in

30 the rearing cages 6.67 days. This may be due to high tempreture and moisture in the black plastic bags (Table 3 and Figure 3).

4.4. Effect of sunlight on the mortality of cucurbit flies pupae

The exposure of pupae to the sunlight had shown a good effect.

The five day exposure was found to be the most effective with mortality mean 4.33, compared with the one and three day exposure which gave 2 and 2.67. The control was 0.0 (Table 4).

31 Table 1: Intensity of infestation by fruit fly in snake melon

at Aburoof and Eljumoeya area

Harvest Sample of fruits Infested fruits Infestation level%

examined

Aburoof Eljumoeya Aburoof Eljumoeya Aburoof Aljamuia

First pick 113 130 10 30 8.85 23.07

Second pick 400 560 30 120 7.5 21.43

Third pick 1609 2801 70 453 4.35 16.17

Four pick 1132 2050 92 300 8.13 14.63

Five pick 1550 1511 140 399 9.03 26.41

32

30

25

20

15

10 Infestation (%) Infestation

5

0 12345Harvest

Aburoof Eljmoaia

Figure 1: Intensity of infestation by fruit fly in snake melon at Aburoof and Eljumoeya area

33 Table 2: Intensity of infestation by fruit fly in squash

at Aburoof and Khartoum area

Harvest Sample of fruits Infested fruits Infestation level%

examined

Aburoof Khartoum Aburoof Khartoum Aburoof Khartoum

First pick 220 300 0 0 0 0

Second pick 495 670 0 1 0 0.15

Third pick 900 1000 2 2 0.22 0.2

Four pick 1050 403 3 0 0.29 0

Five pick 428 465 5 0 1.17 0

34

1.2

1

0.8

0.6

Infestion (%) 0.4

0.2

0 12345 Harvest Aburoof Khartoum

Figure 2: Intensity of infestation by fruit fly in squash at Aburoof and Khartoum area

35 Table 3: Effect of temperature and moisture on the

development of the cucurbit fly larvae (days)

Period

Infested fruits Infested fruits

Replication put in cages put in black

plastic bags

R1 7 3

R2 6 2

R3 7 3

Mean 6.67 2.67

S D+ 0.47 0.47

36

8 7 6 5 4

Days 3 2 1 0 Infested fruits put in a cage Infested fruits put in plastic bags Container

Figure 3: Effect of temperature and moisture on The development of the cucurbit fly larvae (days)

37 Table 4: Effect of sunlight on the mortality of cucurbit flies

pupae

Mortality

Replication Zero day One Three Five

day days days

R1 0 1 3 5

R2 0 3 1 4

R3 0 2 4 4

Mean 0 2 2.67 4.33

S D+ 0 0.82 1.25 0.47

38 CHAPTER FIVE

DISCUSSION

The melon fruit fly Dacus ciliatus remains active throughout the year on one or more hosts, and it is considered the dominant pest of cucurbits, as it causes considerable losses.

The survey in this study in the traditional production areas of vegetables in Khartoum State was conducted to assess the intensity of infestation and to identify the species of fruit flies attracking cucurbits in different areas.

The results showed that, the damage at Eljumoeya area showed high degree in Snake melon variety, compared with that at Aburoof. This due to abundance of the crops cultivations at wide areas, low temperature conditions and wild host, such as Zyziphus sp. and Procesa ageratum.

Jannone (1946) estimated the damage caused by Dacus ciliatus to be 50% in sweet and mandarin oranges in Eritrea. Dhillon, et al (2005) reported that, the percentage of losses varied between 30 to 100% depending on the cucurbit species and season.

Fruit infestation by melon fruit fly in bitter gourd has been reported to vary between 41 to 89% (Lall and Sinha, 1959; Narayanan and Batra,

1960; Kushwaha et al., 1973; Gupta and Verma, 1978; Rabindranath and

Pillia, 1986).

39 Hollingswoth et al., (1997) reported that the melon fruit fly infested 95% of bitter gourd fruits in Papua (New Guinea), and 90% of snake gourd and 60 to 87% of Pumpkin fruits in Solomon Islands. Singh et al., (2000) reported that, the damage is 31.27% in bitter gourd and

28.55% in water melon in India caused by Dacus ciliatus. Pruthi

(1939/40) reported that the extent of damage due to Dacus ciliatus and

Dacus vertebratus has been estimated as ranging from 40-80%.

The results showed that Dacus ciliatus was the only species of fruit flies on cucurbits in Khartoum State. These results agree with the report of Christenson and Foote (1960) who stated that Dacus ciliatus was a dominant species which had eliminated Dacus vertebratus apparently in competition, as attained by Dacus dorsalis over Ceratitis capitata in

Hawaii.

Ali (1967) reported that Dacus ciliatus was the main species during the two seasons of his study, while Dacus vertebratus had practically disappeared from the field, for some unknown reasons. In 1965/66 season

Dacus vertebratus had completely disappeared from fields in Shambat, but in the following season (1966/67) it reappeared, and constituted hardly 1% of the total population.

The results showed the damage in squash was less than in snake melon, probably the snake melon is a preferred host plant.

40 Ali (1967) studied the host plants preference of Dacus ciliatus and reported that Cucumis sativus was the preffered host followed by

Cucumis melon var. flexusus and then Cucurbita pepo.

The exposure of pupae to the sunlight had shown a good effect.

The five day exposure was found to be the most effective with mortality mean 4.33, compared with the one and three day exposure which gave 2 and 2.67. The control was 0.0.

These results agree with that reported by Abbass (1998), who showed that when pupae of med fly Ceratitis capitata in guava were exposed for more than 2 days, all ages were completely dead except the 7 day old pupae which showed a very low survival percentage.

Tisitsips (1969) reported young pupae were sensitive to desiccation and puparia were not enough to protect the pupae.

The results show that the development period of larvae of Dacus ciliatus was less in the black plastic bags 2.67 days with more mortailty, compared with that in the rearing cages 6.67 days. This may be due to high tempreture and moisture content in the bags. These results agree with that reported by Akhtaruzzaman et al., (1999), who suggested that cucumber fruits should be bagged at 3 days after anthesis, and the bags should be retained for 5 days for effective control. It is an environmental safe method for the management of this pest.

41 During the course of this study some difficulties were encountature. The remotenss of some of the areas and the lack of transportation made the visits time consuming and difficult. The lack of security was also a problem, where there were drunkard, druggist and thieves around the production areas which hinder the visits. Being a girl without a private car and without safe company prented difficulties. Also the period of harvesting was short in cucurbits. In addition to that the illetracy of the farmers themselves and lack of knowlege to estimate the infestation and losses. Also they do not allow others to visit their farms and do not tell the truth if they used chemical pesticides or not.

42 CONCLUSION AND RECOMMENDATIONS

CONCLUSION

1. This study revealed that Dacus ciliatus showed preferred snake

melon to squash.

2. This study was show that cucurbit flies exhibited regular adult

emergence throughout the year, with low extent during the

summer.

3. The study indicated that, Dacus ciliatus was the only species

of fruit flies on cucurbits in Khartoum State.

4. The black plastic bags permit fast development and high

mortality of cucurbit fly larvae compared to the cages.

5. Direct exposure of pupae of the cucurbit flies to sunlight stopped

their development to adults.

RECOMMENDATIONS

From the survey and observations in Aburoof, Eljumoeya, Blue

Nile bank near University of Khartoum, Sleit and Amdoum areas, cucurbit fly infestation could be reduced the following suggestions are implemented.

1. Regular survey for collection and rearing of flies from infested

areas, to map the distribution of infestation and identify the

species in Khartoum State.

43 2. Sanitation of cucurbit fields by removal and bagging of infested

fruits or burning them deep in the soil.

3. Ploughing and any other cultural practices.

4. Quarantine measures, to prevent the further spread of fruit flies.

5. Use of soft insecticides to control adult flies when their

population is at its peak.

6. Trapping of adult flies by using natural attractants.

7. Collection and identification of the natural enemies (predators,

parasitoids and pathogens).

8. Mass rearing and release of potential natural enemies.

9. Use of the sterile insect techniques (SIT).

10. Training of national scientists in the field of biological control.

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