PRELIMINARY STUDIES ON THE WINTER SEASON

ABUNDANCE AND FITNESS OF TEPHRITID FRUIT

FLIES IN THE HARARE AREA, ZIMBABWE

BY

GRACIAN TAKUDZWA BARA

A Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of Master

of Science in Tropical Entomology

University of Zimbabwe

Faculty of Science

Department of Biological Sciences

December 2013

ii

DECLARATION

I hereby declare that this thesis is my own original work and has not been submitted for a

degree in any other university.

Gracian Takudzwa Bara Date

I as the supervisor confirm that the work reported in this thesis was carried out by the

candidate under my supervision. The thesis was examined and approved for final submission.

Dr. P.Chinwada Date

iii

DEDICATION

This work is dedicated to people who believed and supported me when I was doing this

project- my parents, my wife Rujeko and finally, my daughter Tinashe. May God richly bless

you.

iv

ACKNOWLEDGEMENTS

I would like to express my appreciation and gratitude to Dr. P. Chinwada for his supervision

and guidance throughout the course of this study. I also extend my gratitude to Mr. G. Ashley,

Mr. S. Ndoma, Ms. B. Chikate and the entire staff at the University of Zimbabwe, Biological

Sciences Department, for their technical and administrative support. Above all, I am most

grateful to the Lord God Almighty who made this project possible.

v

ABSTRACT

Fruit flies (Diptera: Tephritidae) are among the major constraints in commercial fruit

production in many developing African countries. Due to their economic importance,

knowledge of the tephritid fruit fly spectrum in any given area is a prerequisite for the

development of an integrated pest management programme (IPM) to address the pest

problem. To determine the diversity and abundance of fruit fly species in Harare and its

environs during the winter season, assessments were conducted on avocado (Persea

americana), naartjie (Citrus reticulata), guava (Psidium guajava), lemon (Citrus limon) and

orange (Citrus sinensis) in the cold months of April to August 2013. Traps baited with methyl

eugenol and a 3-component lure (Biolure®) were used to trap adult fruit flies at different

locations. A total of 4,991 fruit flies were collected from the traps. In decreasing order of

abundance, the fruit flies recorded comprised the following: Ceratitis rosa (56.4%),

Bactrocera invadens (21.4%), Ceratitis cosyra (11.4%) and Ceratitis capitata (10.9%).

Overally, guava fruit trees recorded the highest number of fruit flies caught/trap/day. Traps set

up in avocado trees captured higher numbers of C. cosyra compared to those set up in guava

trees. Laboratory incubation of field-sampled fruits yielded C. capitata, C. rosa, C. cosyra and

B. invadens. Ceratitis capitata was observed to co-habitate with C. rosa and C. cosyra in

guava and naartjie fruits, whilst B. invadens co-habitated with C. rosa and C. cosyra in guava

fruits. The fruit infestation indices varied with fruit type with the highest infestation being

recorded in guava where C. rosa and B. invadens numbered 13 and 15 flies per kg of fruit,

respectively. Trirhithrum sp. was also observed to emerge from naartjie fruit at 0.53 flies per

kilogramme of fruit. Guava and naartjie were identified to be the main overwintering hosts for

C. cosyra whilst B. invadens utilized guava. The adult tephritid populations, in particular, B.

invadens, C. rosa, C. cosyra and C. capitata, were generally low during winter and this

vi

presents the most opportune time to suppress the fruit fly populations. The influence of host

fruit and temperature on the body size (and hence fitness) of field populations of C. cosyra

was also investigated. Ceratitis cosyra adults reared from guava fruits sampled at the end of

the summer season were generally larger than those reared from winter-sampled naartjie and

guava.

vii

TABLE OF CONTENTS

DECLARATION ........................................................................................................................ ii

DEDICATION ........................................................................................................................... iii

ACKNOWLEDGEMENTS ....................................................................................................... iv

ABSTRACT ................................................................................................................................ v

TABLE OF CONTENTS ......................................................................................................... vii

LIST OF TABLES ....................................................................................................................... x

LIST OF FIGURES ................................................................................................................... xi

LIST OF PLATES .................................................................................................................... xii

CHAPTER 1 ................................................................................................................................ 1

INTRODUCTION ....................................................................................................................... 1

1.1 Overview ....................................................................................................................... 1

1.2 Justification of the study ................................................................................................ 4

1.3 Statement of the problem ............................................................................................... 5

1.4 Objectives ...................................................................................................................... 5

1.5 Hypotheses .................................................................................................................... 6

CHAPTER 2 ................................................................................................................................ 7

LITERATURE REVIEW ............................................................................................................ 7

2.1 Tephritid fruit flies of economic importance in sub-Saharan Africa ............................ 7

2.1.1 Ceratitis capitata (Mediterranean fruit fly, Medfly) ..................................................... 7

2.1.2. Ceratitis cosyra (Mango fruit fly, Marula fruit fly, Marula fly) ................................... 9

viii

2.1.3 Ceratitis rosa (Natal fruit fly, Natal fly) ....................................................................... 9

2.1.4 Bactrocera invadens (African Invader fly, Asian fruit fly) ......................................... 10

2.2 Classification of the Tephritidae ................................................................................. 11

2.3 Tephritid biology ......................................................................................................... 12

2.3.1 Generalized fruit fly life cycle ..................................................................................... 13

2.4 Host selection .............................................................................................................. 14

2.5 Nature and extent of damage ....................................................................................... 14

2.6 Life history, environmental conditions and host availability as determinants of fruit

fly diversity ............................................................................................................................ 15

2.6.1 Means of movement/dispersal ..................................................................................... 16

2.6.2 Oviposition preference ................................................................................................ 16

2.7 Fruit fly monitoring ..................................................................................................... 17

2.8 Management of fruit flies ............................................................................................ 19

2.8.1 Chemical control ......................................................................................................... 19

2.8.2 Biological control ........................................................................................................ 21

2.8.3 Cultural control ............................................................................................................ 22

2.8.4 Mechanical and physical control ................................................................................. 22

2.9.5 Genetic control ............................................................................................................ 23

CHAPTER 3 .............................................................................................................................. 24

MATERIALS AND METHODS .............................................................................................. 24

3.1 Fruit fly trapping .......................................................................................................... 24

ix

3.2 Fruit sampling and ‘rearing’ ........................................................................................ 24

3.3 Fruit fly distribution data ............................................................................................. 27

3.4 Fruit fly identification .................................................................................................. 29

3.5 Flies per trap per day (FTD) ........................................................................................ 31

3.6 Ceratitis cosyra host suitability indicator studies ....................................................... 32

CHAPTER 4 .............................................................................................................................. 33

RESULTS .................................................................................................................................. 33

4.1 Fruit fly temporal dynamics ........................................................................................ 33

4.3 Fruit flies/ trap/ day (FTD) analysis ............................................................................ 38

4.4 Fruit infestation ........................................................................................................... 39

4.5 Wing length and hind tibial length as size parameters ................................................ 44

CHAPTER 5 .............................................................................................................................. 45

DISCUSSION ............................................................................................................................ 45

5.1 Fruit fly monitoring ..................................................................................................... 45

5.2 Fruit rearing ................................................................................................................. 49

5.3 Host suitability studies ................................................................................................ 52

CHAPTER 6 .............................................................................................................................. 54

CONCLUSIONS AND RECOMMENDATIONS .................................................................... 54

6.1 Conclusions ................................................................................................................. 54

6.2 Recommendations ....................................................................................................... 55

REFERENCES .......................................................................................................................... 57

x

LIST OF TABLES

Table 1. Locations of fruit fly traps ........................................................................................... 24

Table 2. Total number of trapped adult fruit flies captured ....................................................... 33

Table 3. Overall Biolure®-baited trap catches showing fruit fly species % composition during

the entire sampling period. ........................................................................................................ 34

Table 4. Number of adult fruit flies of each species caught per trap/day (mean ±SE) for all

traps throughout the monitoring season. .................................................................................... 39

Table 5. Baseline data on host fruits and % composition of fruit fly species emerging from

laboratory-“reared” fruits during the period January to March 2013. ....................................... 39

Table 6. Summary of fruit fly species abundance in different fruit types. ................................ 41

Table 7. Number (mean ± SE) of flies per fruit for all fruit samples collected (n =7). ............. 42

Table 8. The mean fruit infestation index (number of adults/kg of fruit) (n =7). ...................... 42

Table 9. Number (mean ± SE) of adult fruit flies emerging from guava fruit. ......................... 43

Table 10. Right wing and hind tibial lengths of adult male C. cosyra (means ± SE). .............. 44

xi

LIST OF FIGURES

Figure 1. Identification of Ceratitis adults (a); three conspicuous dark spots on thorax of C.

cosyra (b); black bristles on the legs of the male C. rosa (c); hairs with diamond-shaped points

on the head of the male C. capitata (White and Elson-Harris, 1992). ...................................... 30

Figure 2. Bactrocera invadens: (i) wing pattern- conspicuous continuous coastal band, (ii)

separated overlapping and abdominal 3-5 tergites with T-shaped mark (iii) lateral yellow

stripes on thorax. ........................................................................................................................ 30

Figure 3. Fluctuations in fruit fly catches in Biolure® traps set up in banana trees during the

period 27 May to 5 August 2013. .............................................................................................. 35

Figure 4. Fluctuations in fruit fly catches in Biolure® traps set up in guava trees during the

period 27 May to 5 August 2013. .............................................................................................. 36

Figure 5. Fluctuations in fruit fly catches in Biolure® traps set up in orange trees during the

period 27 May to 5 August 2013. .............................................................................................. 36

Figure 6. Fluctuations in fruit fly catches in Biolure® traps set up in avocado trees during the

period 27 May to 5 August 2013. .............................................................................................. 37

Figure 7. Fluctuations in B. invadens catches in methyl eugenol-baited traps set up in guava

trees during the period 4 April to 14 August 2013. ................................................................... 38

xii

LIST OF PLATES

Plate 1. Adult female fruit fly ovipositing on fruit (A); third instar larva emerging from peach

(B) and (C) inside view of a damaged fruit. .............................................................................. 15

Plate 2. Biolure®-baited fruit fly trap in a guava tree at the University of Zimbabwe. ............ 27

Plate 3. Methyl eugenol-baited Lynfield-trap® on a guava tree at the University of Zimbabwe.

................................................................................................................................................... 28

Plate 4. Methyl eugenol plug and fruit flies in Lynfield-trap®. ................................................ 28

1

CHAPTER 1

INTRODUCTION

1.1 Overview

Fruit and vegetable production is one of the fastest-growing agricultural sectors in Africa,

providing both income and employment to growers and exporters alike. The development of

horticultural industries to meet the demands of both the domestic and external markets is an

important component of the economic development of African countries. However, tephritid

fruit flies constitute a major constraint to increased production of fruits and vegetables on the

continent. They cause enormous losses through direct feeding damage and loss of market

opportunities through imposition of strict quarantine by importing countries to prevent entry

and establishment of fruit flies (Ekesi and Billah, 2006).

Fruit flies are a large group of tropical or subtropical phytophagous insects in the order Diptera

and family Tephritidae (Ebeling, 1959). In the family Tephritidae, more than 4,000 species in

about 500 genera have been described (Foote et al., 1993). These include species of economic

importance as well as numerous others and entire subfamilies that are harmless to crops and in

some cases beneficial (as weed biological control agents). Members of this family can be

found in every zoogeographic region of the globe, inhabiting a vast diversity of habitats

(Grimaldi and Engel, 2005).

The African fruit fly fauna comprises almost 1,000 described species of which more than 50

are of economic importance. Most of the tephritid fruit flies known in Africa attack both wild

fruits and flowers. Most species which attack commercially grown fruit crops belong to just

two genera, Ceratitis (95 species) and Dacus (195 species) (White and Goodger, 2009).

However, the four species which are the most economically important in sub-Saharan Africa

2

are the African Invader Fly, Bactrocera invadens Drew, Tsuruta & White, the Mediterranean

Fruit Fly, Ceratitis capitata (Wiedemann); the Mango Fruit Fly, Ceratitis cosyra (Walker), and

the Natal Fruit Fly Ceratitis rosa Karsch.

Ceratitis capitata is indigenous to Africa but has spread to almost every other continent to

become the single most important pest species in the family. Both C. capitata and C. rosa are

highly polyphagous and cause damage to a very wide range of unrelated fruit crops, with C.

rosa tending to displace C. capitata in some areas where both species occur (Hancock, 1989).

Conversely, C. cosyra is recorded from a limited range of plants, although it is the major fruit

fly pest of mangoes in Kenya and Zambia (Malio, 1979; Javaid, 1986).

The Ceratitis flies are all native to the Afrotropical region (De Meyer, 2001) whilst B.

invadens is thought to have originated from the Oriental and Australian regions (White and

Elson-Harris, 1992). The first record of B. invadens in Africa was in the coastal parts of Kenya

in 2003 (Ekesi et al., 2004; Drew et al., 2005). Barely three years after B. invadens was

reported in Kenya, the pest had spread to 22 African countries attacking more than 30 plant

species (Ekesi et al., 2004; Ekesi and Billah, 2006; Mwatawala et al., 2006). Yield losses

averaging 15-50% due to B. invadens have been reported in some African countries

(Vayssières et al., 2005).

Of the 900 plus tephritid species known from the Afrotropical region, approximately one-fifth

occurs in Zimbabwe (Hancock, 1986). Many of the species, both frugivorous and non-

frugivorous, are widespread throughout the country while others have a more restricted range

conforming to the distribution of host plants (Hancock, 1986). Until the introduction of B.

invadens, the species that were known to be of economic importance in subtropical fruit

production in Zimbabwe were C. rosa, C. cosyra, and C. capitata. The presence of B. invadens

3

in Zimbabwe was only confirmed towards the end of 2012 by the government’s Plant

Quarantine Services Institute (Chinwada, P., personal communication).

Fruit flies cause direct damage by puncturing the fruit skin to lay eggs. During egg-laying,

bacteria from the intestinal flora of the fly are introduced into the fruit. These bacteria cause

rotting of the tissues surrounding the egg. When the eggs hatch, the maggots feed on the fruit

flesh making galleries. These provide entry points for pathogens and increase fruit decay,

making fruits unsuitable for human consumption.

The effect on exports is both inter‐regional as well as international. Adult flight and transport

of infested fruit are the major means of movement and dispersal to previously un-infested areas

(Grove et al., 1998). The Herald (5 Feb 2010) reported that the Zimbabwean government had

suspended the importation of fruits from Mozambique following the detection of B. invadens

in that country. Zimbabwe mainly buys mangoes, bananas, pawpaws, guavas, pineapple,

litches, tomatoes and strawberries from Mozambique.

Several fruit fly species interact with each other at various levels. These interactions include

intraspecies and interspecies competition. The outcomes of species invasions on local species

diversity can be visualised along a continuum with impacts ranging from a neutral effect on the

whole system to exclusion by the more highly adapted native species (Hadven et al., 1998) and

can also be very negative through displacement or depression of populations of native species.

For example, the ability of B. zonata to replace C. capitata was noted in Egypt where annual

damage and fruit losses were estimated at $US 177 million (Elnagar et al., 2008; NERC,

2010).

4

In holometabolous insects, oviposition behaviour is critical for larvae survival, since they have

relatively little mobility and depend on the nutritive resources of the host plant selected by

adult females (Singer, 1986; Renwick, 1989). The existence of a possible positive correlation

between the choice of a host for oviposition and offspring performance has been extensively

studied over the last few years and has been demonstrated in some species (Barros and

Zucoloto, 1999; Gu and Walter, 1999; Huk and Kuhne, 1999).

1.2 Justification of the study

Fruit and vegetable production is one of the fastest-growing agricultural sectors in Africa,

providing both income and employment to growers and exporters alike. The range of fruits and

vegetables grown is diverse and commonly includes apples, pumpkin, watermelon, avocado ,

papaya, guava, avocado, cucumber, mangoes, pumpkin and citrus for domestic urban markets

and for export to major outlets in Europe and the Middle East (Ekesi and Billah, 2006).

However, different types of insect pests afflict production in Africa, and perhaps none have

gained greater notoriety than tephritid fruit flies. The enormous losses they cause through

direct damage to fruits and vegetables and loss of market opportunities through imposition of

strict quarantine regulations by importing countries to prevent their entry and establishment

demand urgent need for implementation of sustainable fruit fly management practices. The

introduction of uniform and strict quarantine restrictions and the maximum residue level

(MRL) regulations in the European Union compound the existing fruit fly problem and

jeopardise the lucrative export of fresh fruits and vegetables from Africa (Ekesi and Billah,

2006). In addition, the lack of local expertise in fruit fly management makes it difficult to

respond in a timely and efficient manner to the challenges imposed by fruit flies. The correct

identification of fruit flies occurring in a particular area and their damage symptoms is

therefore the first step towards developing appropriate management strategies. While Africa

5

has a number of native fruit flies of its own, invasion by some exotic species has raised some

serious biosecurity concerns among local experts (Abdullahi et al., 2011). Bactrocera invadens

is one such exotic fruit fly that recently invaded Africa and poses a major threat to the fruit

industry by displacing indigenous fruit flies (Mwatawala et al., 2009).

1.3 Statement of the problem

Information relating to the composition of tephritid fruit fly species in Zimbabwe is outdated

and due for revision now that we have B. invadens in the country. One of the major fruit crops

which underpins the livelihoods of many communal farmers and urban vendors is mango.

Although the fruit is attacked by many fruit fly species, C. cosyra has been the most damaging

prior to the advent of B. invadens. As part of an integrated management strategy targeting C.

cosyra, an understanding of its overwintering host range and population dynamics when

mangoes are out of season in Zimbabwe is therefore of utmost importance. Whilst some

invaluable information on host preference and suitability of selected fruits for C. cosyra

development has been documented in other countries, this is not the case in Zimbabwe.

1.4 Objectives

The specific objectives were:

1) to determine the alternate fruit hosts of C. cosyra when mango fruits are out of season

during the winter months in Harare, Zimbabwe;

2) to determine the incidence and relative abundance of C. cosyra, C. capitata,C. rosa and

B. invadens on alternate winter hosts;

3) to determine the population dynamics of C. cosyra, C. capitata,C. rosa and B. invadens

in the Harare area during the winter season; and

6

4) to determine relative fitness of C. cosyra emerging from different non-mango fruit

hosts.

1.5 Hypotheses

1) Ceratitis cosyra has more than one alternate fruit host when mango is off-season during

winter.

2) Ceratitis cosyra is the dominant species on its alternate winter season hosts.

3) Ceratitis cosyra occurs at every trap location and its populations are maintained at the

same level throughout the winter season.

4) Adult C. cosyra are of the same size irrespective of the host they develop on.

7

CHAPTER 2

LITERATURE REVIEW

2.1 Tephritid fruit flies of economic importance in sub-Saharan Africa

Over the last two decades, diversification into high value horticultural crops has been pushed

as an economic development strategy for sub-Saharan Africa (Delgado and Siamwalla, 1997;

ODI/DFID, 2004; Weinberger and Lumpkin, 2007; World Bank, 2008). Horticulture offers one

of the most important opportunities for employment creation, affording access to education and

health care and providing women with economic opportunities in rural economies where the

highest production of fruits and vegetables takes place (Weinberger and Lumpkin, 2007).

Africa is the aboriginal home of several species of highly damaging fruit flies. For example, on

mango, the results of several surveys across Eastern and Southern Africa show that the crop is

attacked by native fruit fly species such as C. cosyra, C. quinaria, C. fasciventris, C. rosa, C.

anonae and C. capitata. Traditionally, yield losses on this crop due to native fruit flies can

range between 30 and 70% depending on the locality, season and variety (Lux et al., 2003).

Other important native Ceratitis species in the region include C. rubivora, C. puntata, C.

discussa, C. ditissima and C. pedestris that attack a variety of important fruits and vegetables.

On cucurbits, several native Dacus species (e.g. D. bivittatus, D. lounsburyi, D. ciliatus, D.

puntatifrons, D. frontalis and D. vertebratus) also inflict considerable losses on crops (White

and Elson-Harris, 1992; De Meyer et al., 2002; Ekesi and Billah, 2006).

2.1.1 Ceratitis capitata (Mediterranean fruit fly, Medfly)

The Medfly is by far the most polyphagous and widely distributed species in the Ceratitis

genus (Wharton et al., 2000). Ceratitis capitata is a highly polyphagous species whose larvae

8

develop in a very wide range of unrelated fruits. It has been reared from over 300 commercial

and wild host plants (White and Elson-Harris, 1992; De Meyer et al., 2002). Important hosts

include fruit tree crops such as apples, avocados, citrus, figs, mangoes, medlars, pears and

Prunus spp. Ceratitis capitata has also been recorded from wild hosts belonging to a large

number of families (Ekesi and Billah, 2006).

Ceratitis capitata has a blackish thorax marked with silver and a tan abdomen with darker

stripes extending across the abdomen and clear wings with two light brown bands across the

wing, another along the distal front edge and grey flecks scattered near the base (USDA NASS,

2006). The Medfly holds its wings in a drooping position when at rest. Most importantly, the

black spots of the thorax, the two white bands on the yellowish abdomen and the black and

yellow markings on the wings are distinguishing characteristics of this species (Ebeling, 1959;

USDA NASS, 2006). Ceratitis capitata is native to Africa and has spread to other parts of the

world where it was previously unknown (White and Elson-Harris, 1992).

In Africa, C. capitata is recorded from Algeria, Angola, Benin, Burkina Faso, Burundi,

Cameron, Congo, Democratic Republic of Congo, Egypt, Ethiopia, Gabon, Ghana, Guinea,

Cote d'Ivoire, Kenya, Liberia, Libya, Malawi, Morocco, Mozambique, Niger, Nigeria, Senegal,

South Africa, Sudan, Tanzania, Togo, Tunisia, Uganda and Zimbabwe (White and Elson-

Harris, 1992). Outside its aboriginal home of Africa, it has also been reported in Australia,

several European countries, Central, North and South America, the Middle East, Oriental Asia,

the Atlantic Islands, Indian Ocean Islands, Pacific Ocean Islands, the West Indies and nearby

islands (White and Elson-Harris, 1992).

9

2.1.2. Ceratitis cosyra (Mango fruit fly, Marula fruit fly, Marula fly)

Ceratitis cosyra is the most serious pest of mango (Mangifera indica) in Africa. This fly is

a serious pest in smallholder and commercial mango where it is more destructive than either

the Mediterranean fruit fly or the Natal fruit fly (Javaid and De Lima, 1979; Malio, 1979;

Rendell et al., 1995; Labuschagne et al., 1996; Lux et al., 1998). Along with B. invadens, C.

cosyra is one of the most commonly intercepted fruit flies on mango in Europe (Steck, 2000).

The fly also attacks guava (Psidium guajava), sour orange (Citrus aurantium), avocado

(Persea americana), marula plum (Sclerocarya birrea), peach (Prunus persica) and wild

custard-apple (Annona senegalensis) (White and Elson-Harris, 1992).

Adults of C. cosyra have a yellowish body and wing colour with sides and posterior of thorax

prominently ringed with black spots (Rendell et al., 1995). The dorsum is yellowish except for

two tiny black spots centrally and two larger black spots near the scutellum. The scutellum has

two wide black stripes and wing length is about 4-6 mm. The coastal band and discal cross

band are joined together.

Ceratitis cosyra is widespread in Africa and has been reported from Benin, Democratic

Republic of Congo, Cote d'Ivoire, Kenya, Madagascar, Malawi, Mali, Mozambique, Namibia,

Nigeria, Sierra Leone, South Africa, Sudan, Tanzania, Uganda, Zambia and Zimbabwe (White

and Elson-Harris, 1992; Ekesi and Billah, 2006).

2.1.3 Ceratitis rosa (Natal fruit fly, Natal fly)

The Natal fruit fly, C. Rosa (= Pterandrus) rosa Karsh [also known as Pterandrus flavotibialis

Herring] is a polyphagous species with a host range exceeding 100 fruits (White and Elson-

Harris, 1992). It is known to attack apples, apricots, avocados, citrus, guavas, figs, mangoes,

10

pawpaws, peaches, pears, plums, quinces, tomatoes and grapes (Weems and Fasulo, 2002). It

is also a common pest of coffee (Coffea arabica) in Eastern Africa (Ekesi and Billah, 2006).

Ceratitis rosa is known from Angola, Ethiopia, Democratic Republic of Congo, Kenya,

Malawi, Mali, Mauritius, Mozambique, Nigeria, Reunion, Rwanda, Seychelles, South Africa,

Swaziland, Tanzania, Uganda, Zambia and Zimbabwe (White and Elson-Harris, 1992). In

Zimbabwe, this species occurs widely in both Harare and Bulawayo but is still to be recorded

west of the central watershed (Hancock, 1986).

2.1.4 Bactrocera invadens (African Invader fly, Asian fruit fly)

The Bactrocera genus is the most economically significant group with more than 40

polyphagous species considered important pests (White and Elson-Harris, 1992). Bactrocera is

native to the Old World tropics and most of the major pests are from the Oriental and

Australian regions (White and Elson-Harris, 1992). Bactrocera invadens belongs to the

Bactrocera dorsalis complex of tropical fruit flies (French, 2005). This complex comprises

more than 75 species largely endemic to South-East Asia (Drew and Hancock, 1994), with

several undescribed species remaining in collections (Lawson et al., 2003). The group is

arguably one of the most important pest species complexes in world agriculture (Clarke et al.,

2005; Drew et al., 2005).

Bactrocera invadens has high mobility and dispersive powers, high reproductive rates and

extreme polyphagy and in Africa, was first reported in Kenya (Ekesi et al., 2004; Drew et al.,

2005). The species attacks several host plants but primarily prefers mango (Ekesi and Billah,

2006). It has been reared from many fruits including mango, lemon, orange, tomato, banana,

11

guava, marula, custard apple, Indian almond (Terminalia catappa), Sorindea sp. and avocado

(Ekesi et al., 2006; Mwatawala et al., 2006, 2009; Rwomushana et al., 2008).

Bactrocera invadens is a recently described invasive fruit fly species of Asian origin (Drew et

al., 2005). It was discovered in Sri Lanka soon after it had been reported from Africa (Drew et

al., 2005). In Africa, it has been recorded in Benin, Cameroon, Democratic Republic of Congo,

Ethiopia, Gabon, Ghana, Guinea, Kenya, Mali, Nigeria, Senegal, Sudan, Tanzania, Togo and

Uganda (Drew et al., 2005; Ekesi and Billah, 2006).

2.2 Classification of the Tephritidae

Tephritidae workers worldwide have recognised that there is no current classification available

that is suitable for use on a world-wide basis (Hancock, 1986). Most classifications in use

today were designed for use on a regional basis and break down when used in other regions.

Hancock (1986) proposed a provisional classification that recognised eight tephritid

subfamilies: Toxotrypaninae, Trypetinae, Dacinae, Ceratitinae, Myopitinae,

Craspedoxanthinae, Aciunaria and Tephritinae. Although there may be disagreements with this

classification, the suggested scheme closely approximates to a robust classification for the

Zimbabwean fauna, as most of the work leading to the above was carried out in Zimbabwe.

There have been numerous changes in tephritid classification in the past two decades and

several competing classifications have been proposed (Norrbom et al., 1999). Hancock’s

classification recognises eight subfamilies and 24 tribes of the Tephritidae. The subfamily

Ceratitinae has two tribes, Gastrozonini and Ceratitini. The Ceratitis genera belongs to the

Ceratitini tribe. The same classification recognises the subfamily Dacinae with the tribes

Ichneumonopsidini, Monacrostinichini and Dacini. Two genera of the tribe Dacini are

12

recognized ─ Bactrocera and Dacus. The distinguishing feature between these two genera is

the presence of free abdominal tergites in Bactrocera and fused tergites in the latter.

2.3 Tephritid biology

The tephritid life cycle includes the stages of egg, three larval instars, pupa (formed inside the

hardened third stage larval cuticle, or puparium), and adult. Larvae feed on different parts of

the plant. Zwölfer (1983) divided the family into three groups based on resource exploitation

strategies: (i) generalist frugivorous species, (ii) specialist frugivorous species, and (iii) non-

frugivorous species.

In the generalist frugivorous species (e.g. Dacus, Ceratitis and Anastrepha spp.), larvae feed

and develop in the pulp of fleshy fruits. In specialist frugivorous species (e.g. Rhagoletis spp.),

larvae are monophagous or narrowly oligophagous feeders of fleshy fruit. For non-

frugivorous species (e.g. Procecidochares spp.), larvae feed on vegetative structures such as

leaves, shoots or roots and the inflorescences of Asteraceae, Lamiaceae and Capparidaceae.

Adult fruit flies feed on different substrates like fruit juices, honeydew (sugar-rich sticky liquid

secreted by aphids and some scale insects as they feed on plant sap), extra floral glandular

exudates, nectar from flowers, pollen, grains, bird faeces, yeast and bacteria (Hagen, 1958;

Bateman, 1972; Prokopy, 1976; Nishida, 1980; Fitt and O’Brien, 1985; Hendrichs and

Hendrichs, 1990; Hendrichs et al., 1991, 1993; Hendrichs and Prokopy, 1994; Aluja, 1994;

Warburg and Yuval, 1997).

13

2.3.1 Generalized fruit fly life cycle

The life history of the various fruit fly species is similar. Female fruit flies lay their eggs in

batches of 3–8 into healthy, ripening fruit on the tree. The white banana shaped eggs (close to

1mm long) are deposited just beneath the skin (Ekesi, 2006). Eggs are often laid up to eight

weeks before the fruit is mature. The sting sites show as discoloured, often blackish spots,

which may exude distinctive blobs. Depending on the temperature, the eggs hatch within 3-12

days into tiny white maggots. The larvae tunnel and feed within the fruit, passing through three

instars before they reach maturity. This usually takes between seven and ten days, by which

time the larvae are about 7-8 mm long (Ekesi, 2006). The larvae are creamy white, legless and

taper towards the front end. They have paired fine black mouth hooks for tearing at the fruit

tissue. As the larva tunnels and feeds, a localized rot develops. Developmental times are

somewhat similar for many fruit fly species (Paull and Armstron, 1994). At 25°C, egg hatch

occurs after 1-3 days, larval development to pupation about 7-9 days and adult emergence

occurs after 10-11 days (Fletcher, 1987).

Infested fruit will usually drop to the ground, and very heavy losses can be incurred if control

measures are not taken. Each fully fed larva leaves the fruit with a characteristic jumping

motion and burrows into the soil, where it pupates in a brown barrel‐like shell made out of its

own skin. The puparia (white, brown or black) are found buried in the soil 2-5 cm beneath the

host plant. The larval and pupal stages can take 10-20 days depending on climatic conditions.

When pupation is complete, a winged fly emerges and crawls to the soil surface. Adult fruit

flies are sexually mature between four to ten days after emergence (Ekesi, 2006). Soon after

mating, the female uses her sharp ovipositor to lay her eggs into the fruit to a depth of 2–5 mm.

Provided host fruits are available, she will then continue to lay eggs throughout her life, which

14

may last two or three months. Depending on the availability of hosts, there can be 10-16

generations per year in the warmest regions (Ebeling, 1959).

2.4 Host selection

Agricultural crops are attacked by different pests at variable levels based on the prevailing

climatic and ecological conditions. The ecological constraints of host acceptance or host-range

changes were divided into extrinsic and intrinsic factors by Zwölfer (1979, 1983). Extrinsic

factors involve the adult stage, and they include dispersal to and behavioural acceptance of

new hosts, timing the life cycle to include new hosts, and overcoming ovipositional constraints

in new hosts. Intrinsic factors involve the immature stages and include enemy-free space,

intraspecific and interspecific competition, nutritional suitability, and timing of diapause.

2.5 Nature and extent of damage

Attacked fruit will often have puncture marks made by the female’s ovipositor around which

necrosis may occur. Occasionally there may be some tissue decay around these marks or

secondary rot and some fruits with very high sugar content exude globules of sugar which are

usually visible surrounding the oviposition puncture (White and Elson-Harris, 1992). Rotting

of the underlying tissue causes a depression on the surface.

After egg hatching, the maggots bore into the pulp tissue and make feeding galleries. Maggots

feed inside the fruits. The fruit subsequently rots or becomes distorted (Plate 1). Young larvae

leave the necrotic region and move to healthy tissue, where they often introduce various

pathogens and hasten fruit decomposition (Dhillon et al., 2005). This usually makes the fruits

unsuitable for human consumption. Generally the fruit falls to the ground as, or just before the

maggots pupate. In fruits for export, fruit flies cause indirect losses resulting from quarantine

15

restrictions that are imposed by importing countries to prevent entry of fruit flies. Nearly all

fruit fly species are quarantine pests.

Plate 1. Adult female fruit fly ovipositing on fruit (A); third instar larva emerging from peach (B) and (C) inside view of a damaged fruit.

2.6 Life history, environmental conditions and host availability as determinants of

fruit fly diversity

The fluctuation in the population abundance of a fruit fly species is intimately connected with

the climatic conditions and with the diversity, phenology, abundance and degree of preference

of the host (Aluja, 1984). All these factors will determine the movement of the flies in their

search for food, water, shelter and breeding places.

The time required to complete the entire life cycle under field conditions is determined

primarily by temperature, but may also be affected by fruit ripeness, moisture content and

degree of larval crowding (Ebeling, 1959). Apart from temperature, the sequence of hosts is

important in determining the diversity and success of fruit flies (Ebeling, 1959). The

abundance of larval hosts is one of the major factors regulating fruit fly populations (Paull and

Armstron, 1994). Adult fruit flies require about 6-10 days to become sexually mature and

fecundity is usually high. After emergence, females need a protein source for egg development

and subsequent maturation (Pena et al., 1998). Major environmental mortality factors include

16

high and low temperatures, wet or arid conditions, parasitism (Bodenheimer, 1951; Huffacker

and Rabb, 1984) and frugivorous birds (Paull and Armstron, 1994). Good adult mobility,

relatively long life spans (50-93 days), high fecundity (800-1,600 eggs per female) and

multivoltine reproduction (10-12 generations per year, 15-16 in warmest regions) (Ebeling,

1959), explain the diversity and threat posed by fruit flies (Paull andArmstron, 1994; Grove et

al., 1998).

2.6.1 Means of movement/dispersal

Adult flight and the transport of infected fruit are the major means of movement and dispersal

to previously uninfested areas. Work carried out by Navarro-Llopis et al., (2012) suggests that

C. capitata is able to move more than 1 km seeking hosts and upto 20 km (Fletcher, 1989).

2.6.2 Oviposition preference

In holometabolous insects, oviposition behaviour is critical for larvae survival, since they have

relatively little mobility and depend on the nutritive resources of the host plant selected by

adult females (Singer, 1986; Renwick, 1989). The existence of a possible positive correlation

between the choice of a host for oviposition and offspring performance has been extensively

studied over the last few years and has been demonstrated in some species (Barros and

Zucoloto, 1999; Gu and Walter, 1999; Huk and Kuhne, 1999).

Several studies have demonstrated the existence of inter- or intrapopulational variability of

host recognition and selection, as well as an inter- or intrapopulational variability of correlation

between oviposition preference and larval performance (Ng, 1988; Courtney et al., 1989;

Sadeghi and Gilbert, 1999). This behavioural variability may be due to genetic variation

among individuals in terms of the possibility of finding or choosing different hosts

17

(Wasserman and Futuyma, 1981; Jaenike, 1990), or it may also be the result of experiencing

different environments as adults and/or as immatures. These experiences may include different

types of learning as well as the effects of the physical environment (Rausher, 1985).

2.7 Fruit fly monitoring

Accurate methods for fruit fly population surveys are a prerequisite for effective decision

making in area-wide control programmes aimed at pest suppression, as well as those

attempting to establish fruit fly-free or low prevalence areas. Knowledge of the tephritid

spectrum in any given area is thus necessary for the development of an integrated pest

management (IPM) programme to alleviate the pest problem. Fruit fly monitoring helps to (i)

identify fruit fly pests in an area, (ii) determine distribution of pest species, (iii) identify local

hot spots with high populations of the pest, (iv) track changes in population levels, (v)

determine efficacy of control measures, and (vi) facilitate early detection of new fruit fly pests

in a particular area (Manrakhan, 2006).

FAO (1999) defined a trapping survey as an official procedure conducted over a defined period

of time to determine the characteristics of a pest population, or to determine which species

occur in an area. The three objectives of a trapping survey are: (i) to determine if a given

species is present in an area (i.e., a detection survey), (ii) to determine the boundaries of an

area considered to be infested or free from a pest (i.e. a delimiting survey), and (iii) to verify

the characteristics of a pest population including seasonal population fluctuation, relative

abundance, host sequence, etc. (i.e. a monitoring survey) (IAEA, 2003).

Traps used for fruit flies are dependent on the nature of the attractant (IAEA, 2003). Several

traps exist such as the Lynfield trap®, Jackson trap®, Multilure trap®, Tephri trap® and

18

Chempac bucket trap®. The two main types of attractants used in fruit fly monitoring include

para-pheromones or male lures and food baits (Cunningham, 1989; Heath et al., 1997; Lux et

al., 2003). Para-pheromones attract only male fruit flies. They are highly species specific and

are known to have a high efficacy in attracting flies from long distances (Cunningham, 1989;

Economopoulos and Haniotakis, 1994; White and Elson-Harris, 1992).

The para-pheromone trimedlure (TML) (t-butyl-4 (or 5)-chloro-2 methyl cyclohexane

carboxylate) captures Medfly and Natal fruit fly. The para-pheromone methyl eugenol (ME)

(Benzene, 1,2-dimethoxy-4-(2-propenyl)) and cure-lure (4 (p-acetoxyphenyl)-2-butanone)

capture a large number of Bactrocera species including the Oriental fruit fly (B. dorsalis),

Peach fruit fly (B.zonata), Carambola fruit fly (B. carambolae), Philippine fruit fly (B.

philippinensis), and Banana fruit fly (B. musae). The para-pheromone cuelure (CUE) also

captures a large number of Bactrocera including melon fly (B. cucurbitae) and Queensland

fruit fly (B. tryoni) (IAEA, 2003).

TML, ME and CUE have controlled release formulations providing a long lasting attractant for

field use. Attracted flies are retained in panel and delta traps using a sticky material. Para-

pheromones may also be mixed with a sticky material and applied to the surface of the panels.

The male-specific lures used are known to have a different level of attractiveness for their

particular target species. Generally methyl eugenol has the longest range of attraction, cue-lure

less so, and trimedlure has the least range of attraction (Jang and Light, 1996).

Another attractant used in traps are food baits. Food baits attract both male and female fruit

flies. They are not species-specific and are known to have a lower efficiency compared to male

lures (White and Elson-Harris, 1992). Food baits can also attract a number of non-target

insects, including beneficial ones. They are available in both liquid and dry synthetic forms.

19

Ammonia is the principal attractant emanating from food baits (Manrankan, 2006). However,

protein bait traps generally have a more consistent level of attractiveness over C. capitata, C.

rosa and C. cosyra, although there are some species differences (Heath et al., 1994; Barry et

al., 2006; Vargas and Prokopy, 2006). Protein bait traps also have a short range of attraction,

and thus are a better measure of the population of flies in the trapping site (McQuate and

Vargas, 2007). They also capture females, which is the important sex to monitor, because they

oviposit in the fruit.

Biolure®is a commercially available dry attractant consisting of three components: putrescine,

ammonium acetate and trimethylamine. These components are available as membrane-based

dispensers (Manrankan, 2006). It is known to attract males and females of C. cosyra, C.

capitata, C. rosa and B. invadens.

2.8 Management of fruit flies

In Zimbabwe, no particular control methods have been used in the control of fruit flies. Trials

using combined trimedlure and methyl eugenol traps were once set up in Eastern Zimbabwe

and results were promising (Hancock, 1986). However, several methods have been used in

Africa and the world in general with varying levels of success. Fruit fly management strategies

include chemical, mechanical and physical, cultural, biological, and genetic manipulation.

2.8.1 Chemical control

Chemical control has been the most widely used control strategy but recent heightened public

and political concerns have led to the implementation of other pest management approaches

that reduce or eliminate pesticide applications (Daly et al., 1998). Chemical control methods

are effective against all life stages of the fruit flies. Fruit fly suppression is mainly based on use

20

of food baits (hydrolysed proteins or their ammonium mimics) combined with a killing agent

such as pesticide and applied in localized spots. This method targets adult flies, mainly

females, and aims at attracting (and killing) them before they oviposit into the fruits. The bait

attracts the fruit flies from a distance to the spot of application, where the flies feed on the bait,

ingest the pesticide and die (Ekesi and Lux, 2006).

Malathion bait sprays consist of malathion mixed with protein hydrolysate which acts as an

attractant and feeding stimulant. Protein baits are mostly attractive to sexually immature

female flies in need of a protein meal to produce viable eggs although some mature females as

well as males are also attracted (Allwood and Drew, 1997). Aerial malathion bait sprays are

used either to suppress or eradicate fruit flies or as regulatory treatments when commodities

are shipped from regulated areas (Smith, 1999). Malathion protein hydrolysate bait sprays have

been used successfully for area-wide control and eradication of the Mediterranean fruit fly

(Rhode et al., 1972). Methyl bromide and ethylene dibromide fumigation have also been

widely used as a regulatory control technique to kill fruit flies and allow movement of produce

from within quarantine areas to locations outside the quarantine boundaries.

During development, mature fruit fly maggots drop from the fruits to the ground, burrow into

the soil and form a resting stage called the puparia (White and Elson-Harris, 1992). Soil

drenches with diazinon, chlopyrifos or fenthion target the larval and emerging adult stages

(Allwood and Drew, 1997).

Though chemical application has brought about spectacular results on control, undesirable

effects such as insecticide resistance, destruction of non target organisms, pest resurgence,

secondary pest outbreaks, adverse environmental effects and dangers to human health have

also been widely reported (Gullan and Cranston, 1996). For example, the use of chemicals in

21

Pakistan’s mango plantations resulted not only in the desired effect of fruit fly infestation

reduction but also caused an upsurge of scale insects due to the indiscriminant effect on natural

enemies (Mohyuddin and Mahmood, 1993). Thus recent research has turned to the

development of other biorational management strategies, e.g. the use of natural microbial

control agents including entomopathogenic fungi as alternatives to chemical control and as

integral components of an IPM strategy (Dimbi et al., 2004). The fungus Metarhizium

anisopliae, a naturally-occurring fungus isolated from the soil, is being used worldwide as a

biological pesticide for controlling different kinds of insect pests (Ekesi and Lux, 2006).

2.8.2 Biological control

Although successes have been generally limited, the use of natural enemies (parasitoids and

predators) for the suppression of fruit flies has always had a wide appeal because it is relatively

safe, permanent and economical. Several species of parasitoids and predators which can

contribute to the suppression of fruit flies abound in fruits and vegetable agro-ecosystems have

been recorded (Ekesi and Lux, 2006).

Hymenopterous parasitoids are known to attack a wide range of insect groups (Bodenheimer,

1951). In fruit flies, these wasps enter the infested fruit through the oviposition hole or other

injured spots of the rind and deposit their eggs in groups in the posterior part of the host

maggot (Bodenheimer, 1951). Hymenopterous parasitoids were once introduced into Hawaii

from various areas of the Orient in which the Oriental fruit fly, B. dorsalis was known to occur

(Ebeling, 1959). Three species (Opius longicaudata, O. vandenboschi and O. oophilus) were

found to be most effective against the Oriental fruit fly. Another success was recorded in Fiji

where Dacus passiflorae was successfully controlled by O. oophilus (Huffacker and Rabb,

1984).

22

Ceratitis spp. are known to be attacked by the small chalcidid, Pachyneuron vindemniae

Rondani (Bodenheimer, 1951). However, parasitism has been observed to be much higher in

smaller fruits than in bigger ones, which are not easily accessible to most parasitoids

(Bodenheimer, 1951).

2.8.3 Cultural control

Cultural control involves the manipulation of the environment to make it less favourable to

pest populations (Elzinga, 2004). Poorly managed or abandoned orchards and a variety of wild

hosts can result in high fruit fly population build up. Orchard sanitation, which entails the

collection and destruction of all infested fruits found on the tree and fallen fruits containing

fruit fly maggots on the ground, and destruction of wild hosts around orchards can contribute

significantly to reduction of fruit fly populations in the orchard. Benefits of cultural control are

not immediate and cultural practices must be applied long before economic damage is evident

if their impact is to be maximized. However, cultural control methods are of limited

effectiveness if employed on their own but most useful when used in conjunction with other

compatible pest management strategies (Smith, 1999).

2.8.4 Mechanical and physical control

Mechanical and physical techniques have been used for thousands of years to control insect

pests (Elzinga, 2004). Physical control of fruit flies involves providing a physical barrier

between the host fruits and the egg-laying female flies (Allwood and Drew, 1997). The most

common method involves wrapping developing fruits with a protective covering. Fruits are

bagged or wrapped before they reach the stage of maturity at which they are susceptible to

infestation. The technique is, however, applicable where relatively small areas of production

23

are involved, or where the cost of labour is cheap and high quality and value-unblemished

produce is necessary.

2.9.5 Genetic control

The ultimate goal of genetic control is to convert a pest insect to the non-pest status (Elzinga,

2004). Avenues of accomplishing this include sterilizing native pest populations through

chemosterilants (Fletcher and Giannakakis, 1973), mass-sterilizing males and then releasing

them or conferring beneficial advantages such as insecticidal resistance on natural predators or

parasites that utilize certain pests (Elzinga, 2004). Mass releases of insects that can mate

normally but do not reproduce have been used increasingly to eliminate certain pests from

entire regions. Pests such as the cotton boll weevil, the codling moth and tephritid fruit flies

have been eradicated from prescribed regions by means of the sterile insect technique (White

and Elson-Harris, 1994; Daly et al., 1998). For sterile release to succeed, the number of

offspring produced from matings after each release must drop enough to ensure that the

ensuing adult generation decreases in size with each release. Lowering the target pest

population before release increases the sterile to fertile ratio after release. For this reason,

sterile insects are released when the normal insect populations are just recovering from normal

seasonal lows or just after insecticide application. Because a complex of fruit fly species

commonly co-exist in the fragmented production systems in Africa, the approach that is being

promoted on the continent is a combination of methods, i.e. integrated pest management (Ekesi

and Lux, 2006).

24

CHAPTER 3

MATERIALS AND METHODS

3.1 Fruit fly trapping

Fruit fly traps baited with Biolure® (synthetic food lure) and methyl eugenol (para-

pheromone) were set up on banana, guava, orange and avocado fruit trees. The main study

sites were in and around Harare (Mount Pleasant, Mabelreign, Marlborough, Zimre Park).

Another Biolure®-baited fruit fly trap was set up to monitor fruit fly population in an orange

orchard on a farm near the town of Chivhu, 141 km south of Harare. Methyl eugenol-baited

traps were also set up on guava trees at the University of Zimbabwe, Biological Sciences

Department, and in the suburb of Mabelreign, Harare (Table 1).

Table 1. Locations of fruit fly traps

Fruit tree on which trap was placed

Site Coordinates

Banana Mabelreign -17.792696, 31.014948 UZ‡ -17.781492, 31.062885

Orange Mabelreign -17.791476, 31.015804

Marlborough -17.745173, 30.993357 Chivhu farm -18.808785, 30.907541

Avocado Zimre Park -17.858213, 31.217086

Guava Mabelreign -17.791135, 31.015773

Marlborough -17.745116, 30.993010 UZ -17.781660, 31.062551

‡ University of Zimbabwe

3.2 Fruit sampling and ‘rearing’

25

Fruits were collected from Mbare Musika from April to mid-July 2013 and brought to the

laboratory for incubation or ‘rearing’. Other fruits were also collected from fruit trees were

traps had been set up. Mbare Musika is Harare’s major fruit and vegetable market, where

several fruits and vegetables originating from all over Zimbabwe are on sale daily. This makes

it an ideal sampling study site as it gives a quick insight into the fruit fly species spectrum in

the country.

Convenience sampling was used to select the type of fruit to be sampled for the experiment.

Convenience sampling is a non-probability sampling design where sampling units are

conveniently selected. In this case, the fruits selected were those that were in season and on

sale at Mbare Musika or were easily accessible to the researcher. The actual sampling of fruits

was done using purposive sampling (non-probability sampling design) where the basis of fruit

selection was the presence of visual fruit fly oviposition marks on the fruit surface. Selection

of the 'infested' fruit was aided by the fruit vendors themselves who were selling off apparently

decaying fruits at discounted prices. Fruits were acquired for ‘fruit rearing’ experiments every

two weeks, with the target sample size for each sampling occasion being 20- 30 fruits for each

type of fruit.

In the laboratory, individual fruits were first washed in 0.035% sodium hypochlorite solution

and rinsed several times with tap water before they were air-dried, weighed and placed in

clearly labeled incubation units (one fruit/ unit) following the method described by Ekesi and

Billah (2006). An incubation unit consisted of a 1 litre transparent plastic lunch box containing

steam-sterilized sand (1-3 cm deep). In order to allow for aeration, a circular hole was cut into

the lid and closed off with a piece of nylon netting. The lunch boxes were then transferred to

26

an insectary and held at 26 - 28°C, 75 ± 5 % relative humidity and 12:12 light: dark

photoperiod (Ekesi and Billah, 2006).

The sand in each incubation unit was sifted thoroughly after the first 10 days to check for fruit

fly puparia. Thereafter, the sand layer was inspected daily. Puparia collected from the

incubation units were taken out, counted and placed individually in Petri dishes. The pupa was

then covered with a thin layer of steam-sterilized sand and monitored daily for adult

emergence (Ekesi and Billah, 2006). All the larva and pupa recovered were held for three

weeks to ensure maximum adult eclosure. After three weeks of incubation, fruits were

dissected to check for any larvae/ pupae still inside and the fruit discarded.

Emerging adult fruit flies were aspirated out and transferred to new Petri dishes where each

was supplied with sugar in the form of sugar solution on a cotton ball as well as distilled water

on a cotton ball. The adults were kept alive for at least four days after emergence to enable

them to develop their full body colour and normal shape as morphological features were the

main identification tools. White and Elson-Harris (1992) noted that failure to feed the flies

results in specimens that have shrivelled abdomens and dull colours.

After five days, when adult body colour had fully developed, the adults were euthanized and

identified as described in section 3.4. Adults were identified to species and the male and

female numbers produced per fruit and per kilogramme of fruit were recorded. The flies were

then preserved in 70% alcohol. Fruit infestation index was calculated as the ratio of number of

adults per kilogramme of fruit collected (Cowley et al., 1992).

Analysis of variance (ANOVA) was used to compare the number of flies produced per fruit for

the different fruit types as well as the number of flies emerging per kilogramme of the different

27

fruit types. A square root transformation was used to address the assumptions underlying the

ANOVA and where a significant difference (P < 0.05) was found, the 95% Fisher’s Least

Significant Difference (LSD) was used to make pair-wise comparisons.

3.3 Fruit fly distribution data

Trapping surveys were used to generate data to complement results from fruit “rearing”

outlined in 3.2. The surveys were carried out from April to August 2013 using the fixed sites

described in 3.1 for continuous trapping. Continuous trapping at fixed sites enables the

seasonal dynamics of fruit flies to be determined. In this survey, two types of traps and lures

were employed: a) Biolure® fruit fly trap (a modified Chempac® bucket with synthetic food

lures) (Plate 2), and b) Methyl eugenol-baited Lynfield-trap® (Plates 3 and 4).

Plate 2. Biolure®-baited fruit fly trap in a guava tree at the University of Zimbabwe.

28

Plate 3. Methyl eugenol-baited Lynfield-trap® on a guava tree at the University of Zimbabwe.

Plate 4. Methyl eugenol plug and fruit flies in Lynfield-trap®.

29

Biolure® was placed in a modified Chempac® bucket trap. The trap used was a locally made 1

litre transparent plastic container (11.5 cm diameter by 10 cm height) with a yellow lid. Four 3

cm holes were drilled in the upper third of the container for fruit fly entry. A DDVP (2,2

Dichlorovinyl dimethyl phosphate) insecticide block was placed on the base of the trap so as to

kill trapped flies.

The methyl eugenol lure was placed in a Lynfield trap® and catches a large number of male

Bactrocera species. The Lynfield trap® was standard issue obtained from the International

Centre of Insect Physiology and Ecology’s (ICIPE) fruit fly programme. Traps were placed in

fruit trees at a height of 2-4 metres from the ground and oriented towards the upwind side to

allow for proper air flow and easy access for the fruit flies. The traps were not exposed to

direct sunlight, strong winds or dust.

Using the International Atomic Energy Agency’s guidelines, the traps were serviced every 14

days and re-baited every 4–6 weeks depending on environmental conditions. The release rate

of the attractants is high in hot and dry areas, and low in cool and humid areas. Service interval

was therefore dependant on the prevailing environmental conditions. In cool and dry climates,

traps have to be re-baited twice per week, whereas, under hot and humid/dry conditions, the re-

bait interval is once per week (IAEA, 2003). Insect catches from the traps were collected at 14

day intervals and preserved in 70% alcohol for later identification and counting.

3.4 Fruit fly identification

Fruit flies were mounted on a stereomicroscope and identified at X10 magnification.

Taxonomic keys outlined by Ekesi and Billah (2006) were the main tools used for species

30

identification. Figures 1 and 2 shows some of the adult fruit fly morphological features that

were used in identification.

Figure 1. Identification of Ceratitis adults (a); three conspicuous dark spots on thorax of C. cosyra (b); black bristles on the legs of the male C. rosa (c); hairs with diamond-shaped points on the head of the male C. capitata (White and Elson-Harris, 1992).

Figure 2. Bactrocera invadens: (i) wing pattern- conspicuous continuous coastal band, (ii) separated overlapping and abdominal 3-5 tergites with T-shaped mark (iii) lateral yellow stripes on thorax.

31

Ceratitis capitata is the smallest of the three Ceratitis species. It has a dark thorax, while the

other two species are lighter in colour. Typical of C. cosyra are three conspicuous dark spots

on each side of the thorax. Adult fruit fly females have an ovipositor at the tip of the abdomen,

which is absent in the males. Males of the three species are easily distinguished from one

another. The males of C. rosa have clearly visible black bristles on the middle pair of legs.

Ceratitis capitata males can be distinguished from the other two species by two hairs with

diamond-shaped points on its head (Figure 1).

3.5 Flies per trap per day (FTD)

The number of flies caught per trap per day (FTD) is a population index that estimates the

average number of flies captured in one trap in one day that the trap is exposed in the field.

The function of this population index is to have a relative measure of the size of the adult pest

population in a given space and time. It is used as base-line information to compare the size of

the population during the survey. The FTD is the result of dividing the total number of

captured flies by the product obtained from multiplying the total number of serviced traps by

the average number of days the traps were exposed (IAEA, 2003).

The formula is as follows:

��� =�

� ∗ �

where:

� = Total number of flies �= Number of serviced traps

� = Average number of days traps were exposed in the field

32

3.6 Ceratitis cosyra host suitability indicator studies

Host suitability indicator studies were conducted using field-infested guava and naartjie fruits

collected in May and July 2013. In total, eight fruits of each type were selected based on

visible signs of fruit fly infestation, implying advanced larval development. To increase the

likelihood of getting larvae at advanced stages of development, decaying fruits were collected

from the ground. These were taken to the laboratory for “rearing”.

Freshly-emerged adults (1-3 day old) were killed by deep-freezing. Adults were then

preserved in 70% alcohol for later wing and hind tibia measurements. Wing size reflects body

size, which is related to survival and reproductive success (Nasci, 1986; Clements, 1992). For

purposes of this study, the longest segments of the limbs of male C. cosyra were chosen, i.e.

the tibia of the metathoracic (= 3rd or hind) limb as well as the wing length (R4+5 – m).

The wing and right hind tibial lengths were measured by detaching the respective limbs using

forceps. The detached wings and hind tibiae from the specimens were then mounted on a

stereomicroscope fitted with an ocular micrometer. The ocular micrometer was calibrated

using a stage micrometer and measurements of the wing and hind tibia lengths were taken.

Only adults that emerged from pupa whose larvae had pupated within three days of collection

from the field were considered. This was done to ensure that maximum larval development had

taken place in the field under ambient temperature (Navarro-Campos et al., 2011).

One way analysis of variance was used to analyze the variation in the size of C. cosyra adults

emerging from guava and naartjie as well as the variation in the size of the flies that emerged

from guava. Means were compared using Fisher’s Least Significant Difference (LSD) (P <

0.05).

33

CHAPTER 4

RESULTS

4.1 Fruit fly temporal dynamics

The total number of adult fruit flies captured over the entire monitoring period for all the traps

was 4991. Of all the catches collected from the Biolure®-baited traps, females constituted 74.7

% compared to 25.3 % of male catches. Methyl eugenol-baited traps recorded 3012 male B.

invadens (Table 2).

Table 2. Total number of trapped adult fruit flies captured

Type of trap Fruit tree on which trap was placed

Total no. of adult fruit flies

% Fruit fly composition by sex

Male Female

Biolure Banana 346 52.3 47.7

Biolure Orange 186 29.0 71.0

Biolure Avocado 278 29.9 70.1

Biolure Guava 1169 15.6 84.4

Methyl eugenol Guava 3012 100.0 0.0

Total 4991 70.4 29.6

Ceratitis rosa, C. capitata, C. cosyra and B. invadens were the only fruit flies that were

captured. The majority were C. rosa (62.4%) while B. invadens, C. capitata and C. cosyra

constituted 25.7, 10.4 and 1.6%, respectively. Non-target Drosophilidae, Neeridae,

Hymenoptera and Dacinae flies were also caught in the Biolure® traps. On banana, 65.9 % of

the captured adult fruit flies were C. rosa. Bactrocera invadens and C. capitata accounted for

33.8 and 0.3 %, respectively. No C. cosyra was caught in all the banana fruit fly traps. In

guava, fruit fly catches followed a similar trend with C. rosa, B. invadens, C. capitata

34

constituting 59.4, 28.0, 11.9 and 0.7 % of the captured flies, respectively. Only in avocado fruit

fly traps did C. cosyra populations exceed B. invadens and C. capitata (Table 3).

Table 3. Overall Biolure®-baited trap catches showing fruit fly species % composition during the entire sampling period.

Fruit tree on which trap was placed

No. of fruit flies

Species composition (%) C. rosa C. capitata B. invadens C. cosyra

Banana 346 65.9 0.3 33.8 0

Guava 1169 55.9 12.1 31.4 0.7

Avocado 278 90.3 1.4 0.7 7.6

Orange 186 55.4 31.7 11.8 1.1

Total 1979 62.4 10.4 25.7 1.6

The highest mean number of fruit flies caught per trap recorded for Banana for C. rosa was

42.0 at the very beginning of the survey. Bactrocera invadens also recorded its highest mean

number of fruit flies caught per trap of 22.5 recorded over the same period (13 to 27 May

2013). Thereafter, the fruit fly population began to drop reaching a low of 5.0 and 6.0 mean

number of fruit flies caught per trap for C. rosa and B. invadens, respectively, on the 24th of

June 2013. No C. cosyra was captured in all the banana traps throughout the survey period

whilst a high of 0.5 fruit flies per trap was recorded for C. capitata on the 10th of June 2013.

Thereafter no further C. capitata captures were made.

From the 22nd of July, the B.invadens and C. rosa populations began to increase gradually. No

captures of C. cosyra and C. capitata were made from the 10th of June 2013 (Figure 3).

35

Figure 3. Fluctuations in fruit fly catches in Biolure® traps set up in banana trees during the period 27 May to 5 August 2013.

Ceratitis capitata mean flies/trap/2 week period populations were highest in guava and oranges

with peaks of 34.5 and 16, respectively, at the beginning of winter. The populations thereafter

began to drop till the beginning of August. Banana and avocado recorded few or no C. capitata

(Figure 4).

In the Biolure-baited traps set up on orange trees, mean fruit fly highs of 26; 16, 3.5 were

recorded for C. rosa, C. capitata and B. invadens, respectively, at the beginning of the survey.

Thereafter the catches declined gradually to below 4.0 fruit flies caught per trap for all species

after the 22nd of July 2014 (Figure 5).

0

5

10

15

20

25

30

35

40

45

Mea

n nu

mbe

r of

frui

t flie

s/ tr

ap

C. rosa

C. capitata

B. invadens

C. cosyra

36

Figure 4. Fluctuations in fruit fly catches in Biolure® traps set up in guava trees during the period 27 May to 5 August 2013.

Figure 5. Fluctuations in fruit fly catches in Biolure® traps set up in orange trees during the period 27 May to 5 August 2013.

0

20

40

60

80

100

120

140M

ean

num

ber

of fr

uit f

lies/

trap

C. rosa

C. capitata

B. invadens

C. cosyra

0

5

10

15

20

25

30

35

40

45

Mea

n N

o. o

f fru

it fli

es /

trap

C. rosa

C. capitata

B. invadens

C. cosyra

37

In Biolure-baited traps set up on avocado trees, fruit fly populations were highest at the

beginning of the survey and thereafter declined gradually for all the fruit fly species. The most

prevalent fruit fly species was C. rosa and the least was B. invadens. As with all the other fruit

types surveyed during the winter period, the fruit fly populations were greatly depressed

(Figure 6).

Figure 6. Fluctuations in fruit fly catches in Biolure® traps set up in avocado trees during the period 27 May to 5 August 2013.

Bactrocera invadens catches in methyl eugenol-baited traps placed on guava trees displayed a

pattern similar to that of the other fruit flies ─ high initially (peaking at 675 flies in mid April)

and declining gradually till the end of July (54 flies/trap). Thereafter, B. invadens catches

began to increase steadily and had risen to 373 adult flies/trap by mid-August (Figure 7).

0

10

20

30

40

50

60

70

Mea

n nu

mbe

r of

frui

t flie

s/ tr

ap

C. rosa

C. capitata

B. invadens

C. cosyra

38

Figure 7. Fluctuations in B. invadens catches in methyl eugenol-baited traps set up in guava trees during the period 4 April to 14 August 2013.

4.3 Fruit flies/ trap/ day (FTD) analysis

An analysis of the data on numbers of fruit flies/trap/day revealed that C. rosa was the

dominant fruit fly across all fruit trees while B. invadens was the second most predominant

species in banana and guava (Table 4). Ceratitis capitata was the second most dominant

species in oranges with a mean of 0.6 flies/trap/day. No C. cosyra was captured in all the

banana fruit fly traps throughout the monitoring season; however, it was the second most

abundant fruit fly after C. rosa in avocado with a mean 0.13 flies/trap/day.

0

100

200

300

400

500

600

700

800

4-A

pr

11-

Ap

r

18-

Ap

r

25-

Ap

r

2-M

ay

9-M

ay

16-

May

23-

May

30-

May

6-Ju

n

13-

Jun

20-

Jun

27-

Jun

4-Ju

l

11-

Jul

18-

Jul

25-

Jul

1-A

ug

8-A

ug

Mea

n nu

mbe

r of

frui

t flie

s / t

rap

2013

39

Table 4. Number of adult fruit flies of each species caught per trap/day (mean ±SE) for all traps throughout the monitoring season.

Fruit tree on which trap was placed

C. rosa C. capitata B. invadens C. cosyra

Banana 1.4 ± 0.5 0.006 ± 0.006 0.7 ± 0.3 0.0

Guava 5.2 ±1.7 1.0 ± 0.4 2.5 ± 1.2 0.06 ± 0.03

Orange 0.6 ±0.3 0.6 ± 0.3 0.1 ± 0.07 0.03 ± 0.03

Avocado 1.5 ± 0.6 0.02 ± 0.01 0.01 ± 0.008 0.13 ± 0.05

Guava‡ 0.0 0.0 16.8 ± 4.1 0.0

‡ Methyl eugenol lure

4.4 Fruit infestation

In a baseline study conducted during the late part of the 2012/2013 summer season, C. cosyra

had been found to outnumber both C. rosa and B. invadens, accounting for 54.8% of all the

fruit flies that emerged from avocado, naartjies, mango, Mexican apple and guava fruits.

Bactrocera invadens and C. rosa accounted for 38.9 and 6.3%, respectively. No C. capitata

emerged from all the fruits sampled during this period (Table 5).

Table 5. Baseline data on host fruits and % composition of fruit fly species emerging from laboratory-“reared” fruits during the period January to March 2013.

Date Fruit Site N C. cosyra B. invadens C. rosa

30 January Avocado Marlborough 158 75.3 24.7 0.0

30 January Mango Zimre Park 154 85.7 7.8 6.5

30 January Mango UZ 36 11.1 86.1 2.8

30 January Mexican apple

Marlborough 9 0.0 11.1 88.9

30 January Mango Marlborough 112 4.5 92 3.6

4 March Naartjie Zimre Park 2 100k 0.0 0.0

4 March Guava Chivhu 7 0.0 0.0 100

Totals 478 54.8 38.9 6.3

40

A total five fruit fly species emerged from fruit rearing experiments carried out from 3 May to

18 August 2013: C. cosyra, C. capitata, C. rosa, B. invadens and Trirhithrum sp. No

parasitoids emerged from all the incubated fruit samples. Ceratitis capitata was observed to co-

habitate with C. rosa and C. cosyra in guava and naartjie fruits whilst B. invadens co-habitated

with C. rosa and C. cosyra in guava fruits. No fruit flies emerged from 143 bananas weighing a

total of 10.1 kg and 96 oranges weighing 13.0 kg. A single B. invadens fly emerged from 124

lemons weighing 15.0 kg. In avocadoes, only 2 C. rosa flies emerged from 144 fruits with a

total weight of 27.8 kg.

In naartjies, C. capitata was the most abundant fruit fly (51.5%) followed by Trirhithrum sp.

(24.2%)(Table 7). No B. invadens emerged from naartjie fruits. Ceratitis cosyra and C.rosa

were equally abundant (12.1%). Bactrocera invadens and C. rosa were the most abundant fruit

flies in guava (45.7 and 45.5%, respectively) while C. cosyra was the least abundant (3.9%).

Trirhithrum sp. only emerged from naartjie fruit.

41

Table 6. Summary of fruit fly species abundance in different fruit types.

Fruit type Weight (kg)

No. of fruits

No. of pupae

No. of adults

% Adult emergence

% Species abundance

C. cosyra C. capitata C. rosa B. invadens Trirhithrum sp.

Banana 10.144 143 0 0 0.0 0.0 0.0 0.0 0.0 0.0

Orange 12.977 96 0 0 0.0 0.0 0.0 0.0 0.0 0.0

Lemon 15.024 124 0 0 0.0 0.0 0.0 0.0 0.0 0.0

Avocado 27.763 144 2 2 100 0.0 0.0 100 0.0 0.0

Naartjie 15.190 179 84 33 39.3 12.1 51.5 12.1 0.0 24.2

Guava 19.693 331 1062 613 57.7 3.9 4.9 45.5 45.7 0.0

42

Table 7. Number (mean ± SE) of flies per fruit for all fruit samples collected (n =7).

Fruit C. cosyra C. capitata C. rosa B. invadens Trirhithrum sp.

Naartjie 0.02± 0.02 0.05±0.02 0.05±0.03 0.0 0.06±0.05

Guava 0.1±0.04 0.1±0.06 0.8±0.3 0.8±0.3 0.0

Lemon 0.0 0.0 0.0 0.005±0.005 0.0

Banana 0.0 0.0 0.0 0.0 0.0

Avocado 0.0 0.0 0.01±0.01 0.0 0.0

Orange 0.0 0.0 0.0 0.0 0.0

An assessment of the mean number of fruit flies/fruit showed that Trirhrithrum sp., C.

capitata and C. rosa were the most abundant fruit flies in naartjies whilst in guava, B.

invadens and C. rosa predominated. Lemon, banana, avocado and orange recorded few or no

fruit flies (Tables 7 and 8). No fruit flies emerged from banana and orange. Bactrocera

invadens and C. rosa had the highest mean infestation indices in guava, whilst C. capitata and

Trirhithrum were the most dominant in naartjie. Ceratitis cosyra was absent in all the fruits

save for naartjie and guava.

Table 8. The mean fruit infestation index (number of adults/kg of fruit) (n =7).

Fruit type C. cosyra C. capitata C. rosa B. invadens Trirhithrum sp.

Banana 0.0 0.0 0.0 0.0 0.0

Orange 0.0 0.0 0.0 0.0 0.0

Lemon 0.0 0.0 0.0 0.03±0.03 0.0

Avocado 0.0 0.0 0.1 ± 0.1 0.0 0.0

Naartjie 0.2 ± 0.2 0.9 ± 0.4 0.2 ± 0.2 0.0 0.5 ± 0.5

Guava 1.5 ± 0.9 1.5 ± 0.7 12.9± 4.6 14.9 ± 3.8 0.0

The mean number of adult C. rosa that emerged per fruit from guava was significantly

different to those that emerged from both naartjie and avocado (F = 10.2; df = 20; P = 0.001).

43

More C. rosa emerged from guava than in any other fruit. The mean fruit infestation index

(number of fruit fly adults/kg) for guava was also significantly different to those that emerged

from naartjie and avocado (F = 10.3; df = 20; P = 0.001). However, as fruit fly emergence was

low and absent in some cases, statistical comparisons were limited (Tables 7, 8).

The mean fruit infestation index in naartjies ranged from 0.2 flies/kg (C. cosyra) to 0.9

flies/kg (C. capitata). The mean fruit infestation index for all the fruit flies that emerged from

naartjies revealed no significant difference among the different fruit flies (F = 1.3; df = 34; P

= 0.3). Trirhithrum sp. emerged from naartjie fruit (fruit infestation index of 0.5 flies/kg fruit).

The mean fruit infestation index for guava showed that C. rosa and B. invadens recorded the

highest numbers of adult flies per fruit and these were not significantly different from each

other (Table 9).

No significant differences were observed for C. cosyra and C. capitata in terms of the mean

number of flies/fruit and the mean fruit infestation levels (Table 9). However, B. invadens and

C. rosa were not statistically different from each other but were different from both C. cosyra

and C. capitata.

Table 9. Number (mean ± SE) of adult fruit flies emerging from guava fruit.

Fruit fly species N Number/fruit Number/kg

C. cosyra 7 0.10±0.04 a 1.61±0.68 a

C. capitata 7 0.11±0.06 a 1.72±0.92 a

C. rosa 7 0.82±0.32 b 14.39±6.11 b

B. invadens 7 0.77±0.27 b 13.98±5.70 b

Means within a column followed by the same letter are not significantly different (P < 0.05).

44

4.5 Wing length and hind tibial length as size parameters

Wing length and hind tibial length were used as size parameters to determine which hosts

were preferred by C. cosyra. The right wing lengths and hind tibial lengths are summarized in

Table 10.

Table 10. Right wing and hind tibial lengths of adult male C. cosyra (means ± SE).

Fruit Sampling month wing length (mm) (n = 4)

Hind tibial length (mm) (n = 4)

Naartjie May 2013 4.30 ± 0.20 a 1.40 ± 0.06 ab

Guava May 2013 4.90 ± 0.06 b 1.50 ± 0.06 b

Guava July 2013 4.20 ± 0.20 a 1.30 ± 0.04 a

Means within a column followed by the same letter are not significantly different (P < 0.05).

Adult wing lengths ranged from 4.2 to 4.9 mm with the longest wing length measured from C.

cosyra that emerged from guava in May 2013. In comparison, C. cosyra which emerged from

guava and naartjie in May 2013 had significantly shorter wing lengths (F = 6.4; df = 23; P<

0.007).

The longest hind tibial lengths were measured off C. cosyra that emerged from guava in May

(1.5 mm) and the shortest was of C. cosyra that emerged from guava July (1.3 mm). The tibial

lengths of C.rosa that emerged from naartjie was not significantly different to those which

emerged from both guava in May and July.

45

CHAPTER 5

DISCUSSION

5.1 Fruit fly monitoring

From the 10th to the 24th of June 2013, there was a decline in the tephritid fruit fly populations

captured by the traps set up at the University of Zimbabwe and Marlborough. This decline

could be attributed to the fact that there were no more guava fruits. On the 24th of June, the

fruit fly trap was subsequently decommissioned and only the Marlborough trap remained

operational as guava fruits were still available. Another guava fruit fly trap could not be set up

as the ‘normal” guava season had lapsed four months earlier and only a few scattered trees

were still fruiting. In some parts of Zimbabwe, it has been reported that guava trees can fruit

till end of August. However, these would be few and widely scattered. As few guava trees will

still be fruiting, it is hypothesized that fruit flies will converge on the few fruiting guava trees

resulting in large fruit fly populations on these trees. It is possible that this is what was

observed from the 24th of June to the 8th of July 2013. As the guava fruit run out, fruit flies

leave for citrus, in particular naartjies (Citrus reticulata). Citrus reticulata appeared to be

more favourable for fruit fly infestation than Navel and Valencia oranges (C. sinensis) as no

fruit flies emerged from incubated samples.

At the end of July 2013, fruiting was observed in some early fruiting varieties of peach

(Prunus persica) in Zimre Park and Marlborough, Harare. It is an established fact that peach

is a major host of Ceratitis spp. in summer. Flowering in early fruiting mango trees has

already begun in Harare. Therefore it is likely that the fruit flies will survive the winter season

on guava, citrus and possibly wild fruit hosts and move to infest mangoes, peaches and other

hosts in summer.

46

As with guava trees, the fruit fly trap data revealed a similar pattern for all the other fruits.

There wasa decline in fruit fly populations until the 24th of June and immediately after, there

was an upsurge. However, this upsurge was not sustained as there was an abrupt decline soon

after.

The population dynamics observed could be as a result of several biotic and abiotic factors.

Temperature and humidity are usually considered to be the most important abiotic factors

explaining population dynamics in insect species (Duyck et al., 2004; Vayssières et al., 2008).

The role of temperature as a determinant of abundance in tephritids is mediated either directly

or indirectly through its effects on rates of development, mortality, and fecundity. Rates of

increase (or decrease) of individual populations are dependent upon the values of these

parameters, and they in turn are determined by the multiple influences impinging upon the

individuals from within the population's "life-system" (Clark et al., 1967). Temperature is one

of the most powerful of these influences. It has the dominant role in the determination of rates

of development, and is, therefore, largely responsible for the timing of the population

processes, and their synchronization with changes in the environment (Bateman, 1972).

In the present study, C. rosa consistently outnumbered C. capitata both in trap catches and

from ‘fruit rearing’. Studies revealed that C. rosa might be more sensitive to low humidity and

more tolerant to colder, wetter conditions than medfly. It has a lower larval development

threshold than Medfly─ 3.1°C compared to 10.2°C for C. capitata (Duyck and Quilici, 2002;

Duyck et al., 2004; Duyck et al., 2006). This probably enables it to thrive during cold winter

periods. The drop in fruit fly populations coincided with the coldest month in the 2013 winter.

June was the coldest month with an average daily minimum temperature of 6.7°C with the

47

coldest day of the year (June 22) recording a low temperature of 2.2 °C (www.weather-

spark/history/29149/2013/Harare-Mashonaland-East-Zimbabwe).

In most parts of the world, fruit flies are distinctly seasonal in abundance, with numbers high

in summer and low in winter. The multivoltine species may produce up to six overlapping

generations in a single season. Characteristically, their numbers build up to a peak in late

summer and early autumn, and then decline fairly rapidly (Baker et al., 1944; Bot, 1965).

The development of the immature stages of tephritids is generally possible between 10°C and

30°C. Fecundity is also dependent upon temperature, with maximum production of eggs

within the range 25-30°C. For oviposition, however, thresholds fall between 9°C and 16°C for

various species. Overwintering in the more tropical species is normally accomplished by

adults. They tend to congregate in locations which provide shelter and food. These

overwintering groups often form fairly stable populations because birth rate is zero, death rate

is low, and movements are inhibited by low temperatures (Monro, 1966). They are usually

restricted to patches of evergreen foliage such as citrus (Monro, 1966) and other "favourable"

plants (Nishida, 1963). They may become active enough to feed during the warmer hours of

the days, but tend to return to the same sheltered foliage when temperatures fall.

An analysis of the mean fruit fly trap data revealed that C. rosa was overally the most

prevalent species in all the fruits studied. This result is in agreement with Weems and Fasulo

(2002) who reported that C. rosa has traditionally been considered the most common fruit fly

of economic importance in Zimbabwe. On guava and banana, C. rosa was followed by B.

invadens, C. capitata and lastly C. cosyra. On oranges, the order of prevalence was C. rosa,

C. capitata, B. invadens and C. cosyra.

48

The high numbers of male B. invadens caught using methyl eugenol traps confirm the

observations of Lux et al. (2003), Mwatawala et al. (2004) and Drew et al. (2005) that methyl

eugenol is the bait of choice in detection and delimitation surveys of the species across

tropical Africa. No beneficial organisms such as honey bees or fruit fly parasitoids were

captured from both the methyl eugenol and Biolure®-baited traps. However, non-target

Drosophilidae, Neeridae, Hymenoptera and Dacinae flies were caught in the Biolure® traps.

Foraging ants were among the insects caught in the Biolure® traps. The absence of any

beneficial organisms caught in the methy eugenol traps suggests that it is more

environmentally-friendly as it preserves non-target insects.

Given the current results and what is know from literature, we can speculate on the

implications of the current results on the probability of fruit fly infestation of particular fruit

trees. As male lure trap catches vary with locality and attract flies from large distances and

also from other fruit trees, they are probably of limited value in predicting numbers of fruit

flies within small fruit orchards with several different fruit trees. This is the case in most

residential areas and smallholder farms where homeowners typically have a small orchard

with different fruit trees (in particular mangoes, guavas, bananas, lemons, oranges and

avocadoes). On the other hand, protein bait traps capture females and attract flies from short

distances, and therefore give a better indication of female flies found within orchards.

Whilst the use of trapping systems are useful in analyzing the dynamics and the population

abundance of fruit flies, the capture of adults from a trap placed in a certain tree does not

necessarily imply a preference for that species or that it should be considered as a host

(Putruele, 1996). The actual implication for fruit infestation can only be determined from

naturally-infested fruit samples.

49

5.2 Fruit rearing

Fruits were collected from Harare’s Mbare Musika fruit and vegetable market because it is the

country’s major distribution point of fruits and vegetables which originated from all over

Zimbabwe. It is also located near a major bus terminus linking Harare to towns and cities

throughout Zimbabwe. Thus, infested fruit can be transported to and from other towns, cities

or rural areas. This greatly increases the probability for the establishment and dispersal of fruit

flies.

A total of five fruit fly species emerged from the fruits under study: C. cosyra, C. capitata, C.

rosa, B. invadens and Trirhithrum sp. No parasitoids emerged from all the incubated fruit

samples. Ceratitis capitata was observed to co-habitate with C. rosa and C. cosyra in guava

and naartjie fruits whilst B. invadens co-habitated with C. rosa and C. cosyra in guava fruits.

Populations of fruit flies were generally low for all the fruit samples. No fruit flies emerged

from Navel and Valencia oranges and one B. invadens fruit fly emerged from lemon. These

results are in agreement with work carried out by Lloyd et al. (2013) who suggested that citrus

fruits have low susceptibility to tephritid fruit flies. The toxicity of essential oils in citrus peel

to the eggs and larvae of C. capitata has been confirmed in recent studies (Papachristos et al.,

2008, 2009). However, susceptibility to tephritid fruit flies can vary according to species and

cultivar of the citrus host (Greany, 1989). This was observed in naartjies, where C. capitata

was the most abundant species and this concurs with Wharton et al.’s (2000) conclusion that

the Medfly is by far the most notorious pest species in citrus.

Traditionally, the native afrotropical fruit flies C. rosa, C. capitata and C. cosyra have been

the most prevalent in Zimbabwe (Hancock, 1986). Baseline study results carried out during

the last part of the 2012/2013 summer season concurred with Hancock (1986). Ceratitis

50

cosyra outnumbered both C. rosa and B. invadens accounting for 54.9% of all the fruit flies

that emerged from avocado, naartjies, mango, Mexican apple and guava fruits.

A few months after the baseline survey, C. cosyra populations were greatly depressed as

observed both from trap data and ‘fruit rearing’. This begs the question ─ what is happening

to the native Afrotropical fruit flies? Is it possible that B. invadens is displacing the native

fruit flies and in particular C. cosyra? The genus Bactrocera is renowned for its strong

competitive abilities and capacity to displace other (indigenous) fruit fly species (Duyck et al.,

2006a, 2006b). The laws of interspecific competition dictate that for two or more competing

species to share the same ecological niche, equilibrium has to be established. This is achieved

either through the elimination of one of the species or the establishment of a new stable

equilibrium in which the two species coexist but at different relative population levels (Duyck

et al., 2004). From the data collected, it seems probable that B. invadens is displacing C.

capitata and C. cosyra. However, no such conclusion is made in this paper as the data was

collected over a very short period and not across the full range of fruit fly hosts. Further

ecological and behavioural studies are required.

Mwatawala et al. (2006) noted that the spread and colonization of B. invadens could be

limited by climatic conditions and interspecific competition with cold-tolerant species like C.

rosa. Since the ability of B. invadens to displace other fruit flies has been demonstrated, the

cold temperatures could explain why C. rosa was consistently more prevalent than B.

invadens during the winter period. If that is the case, then as the temperatures increase, so will

the likelihood of B. invadens outnumbering C. rosa.

In guava, B. invadens was the most abundant fruit fly species along with C. rosa,

outnumbering the indigenous fruit flies C. cosyra and C. capitata. Goergen et al. (2011) listed

51

naartjie as a host for B. invadens in West and Central Africa. However, in current studies, no

B. invadens emerged from naartjie. This may not in any way mean that naartjie fruit is not a

major host of B. invadens (naturally) but just be reflective of the limited time in which the

study was conducted. Thus, more detailed work needs to be done to establish the host status of

naartjie to B. invadens in Zimbabwe.

Of note was the adult eclosure of Trirhithrum sp. from naartjie. Trirhithrum sp. is typically a

pest of coffee (Ekesi and Billah, 2006). Its abundance and fruit infestation levels on naartjie

(24.1% abundance and 0.5 adults/kg of fruit) were quite high considering that it was not

known to infest naartjie fruit. Possibly, in the absence of its preferred hosts – coffee,

Trirhithrum sp. rely on naartjie for survival as a conditional host.

Observations made during the study showed that adult fruit flies emerging from fruit survived

longer (on average 7 days) in cages where the fruit remains were not removed as opposed to

cages where the fruit remains were removed (on average 4–5 days). It appeared that the

insects derived nutrition from the decaying fruits. This observation is in agreement with

Bateman (1972) who reported that adult flies feed on a considerable variety of other natural

products, including the juices and tissues of damaged or decaying fruit, plant sap, nectar from

flowers, and bird faeces.

It was also observed during the current study that collecting fruit from the ground below fruit

trees tended to increase the likelihood of collecting infested fruit. However, this also increases

the likelihood of contamination by microbes. For purposes of rearing fruit flies, picking up

fruit from the ground is the ideal target area as plucking fruit from the tree results in less fruit

fly infestation levels. The high numbers of fruit flies in fallen fruit has a direct consequence in

52

fruit fly suppression. Thus, an important recommendation for breaking the fruit fly cycle is to

collect and destroy all fallen fruit in orchards (Ekesi and Lux, 2006).

5.3 Host suitability studies

The results obtained in this study concur with what other authors have already determined that

body size in insects is largely a product of the complex relationship between temperature,

food quality, food quantity and genotype (Edgar, 2006; Nijihout et al., 2006). According to

Navarro-Campos et al. (2011), the most common factors that influence body size are

temperature and food resources. In ectotherms, decreasing temperature causes reduced growth

and development but a larger body size. This follows the evolutionary Bergmann’s rule,

where the size of organisms increases with latitude (Hoffmann et al., 2007).

Following Bergmann’s rule, the cold winter temperatures are expected to result in larger C.

cosyra adults emerging from guava in winter than from the same fruit in summer. However,

that was not the case as C. cosyra adults that emerged from July-sampled guava were of

significantly smaller size than those that emerged from May-sampled guava. This result

concurs with work done by Stamp (1990) who suggested that diet quality can interact with

temperature and can alter the normal thermal reaction norms of the body. Therefore, the C.

cosyra body size variations observed may therefore indicate different nutritional qualities of

the guava that was utilized by the flies in May compared to the naartjie and guava utilized in

July. Furthermore, Dantharayana (1976) and Chapman (1998) demonstrated that insects grow

to smaller sizes on lower quality diets. We can therefore conclude that the guava and naartjie

available to fruit flies in winter provide a lower quality diet than the guava available during

the “normal” in-season guava. For the purposes of this study, the “normal” guava season was

taken to end in May when guava fruits are no longer on sale at Mbare Musika, Harare. In this

53

regard, guava and naartjie serve as conditional or overwintering hosts for C. cosyra. However,

the data collected from naturally-infested fruit from the field also suggests that there are too

many variables (temperature, food quality and quantity and genetics, etc.) that can ultimately

determine insect body size. For this reason, it is not possible to attribute the body size

variation observed in this study to host quality alone but to a combination of factors, chief

among them diet and temperature.

54

CHAPTER 6

CONCLUSIONS AND RECOMMENDATIONS

6.1 Conclusions

This study has provided baseline data on the tephritid fauna of fruits in the Harare area and

some major fruit producing areas of Zimbabwe during the cold season. On the basis of the

results obtained, we may conclude that tephritid fruit fly populations, in particular C. rosa, C.

capitata, C. cosyra and B. invadens are low during winter. This was confirmed both from trap

data and fruit sampling.

This study also confirms that the invasive fruit fly, B. invadens, is now well established in the

study area where it occurs at high densities and is becoming the most abundant species over

the native fruit flies species in attacked fruits. The high B. invadens infestation levels in guava

suggest that guava is a preferred host of the B. invadens in winter. As evidenced by the low

infestation levels, banana and avocado, lemon, orange and naartjie are less important in B.

invadens population dynamics.

The knowledge of host plant’s role in B. invadens population dynamics in winter is important

in the development and implementation of B. invadens integrated pest management

programmes and in this case, guava should be the main target as it was shown to be an

important winter bridging host for the pest.

The study also revealed that C. capitata is the most abundant fruit fly in naartjie fruit. Efforts

to suppress C. capitata can therefore, be aimed at naartjie as it proved to be an important

reservoir of the fruit fly. Finally, the study results identified guava and naartjie as the main

overwintering hosts for C. cosyra in Zimbabwe. Guava was also found to be the major

55

overwintering host for B. invadens. Considering the polyphagous nature of these fruit flies, it

is possible that their survival outside the normal fruit season is also achieved via utilization of

wild hosts which were beyond the scope of this study. On these overwintering hosts, diet and

temperature could be the most important factors determining the fitness of the mango fruit fly,

C. cosyra.

6.2 Recommendations

The following recommendations are made:

• Nation-wide surveys need to be carried out to establish a national fruit fly database. The

database can include insect-host relationships, host preferences, alternative hosts,

population dynamics, life history and behaviour. Currently, published work on the

taxonomy and ecology of fruit flies in Zimbabwe is outdated and in serious need of

updating.

• Carry out local studies to determine the role of climatic factors (e.g. temperature, rainfall

and humidity) in determining fruit fly diversity in different geographical locations of the

country. This knowledge can be used to model the likelihood of insect invasion and

establishment and hence help policy makers to make informed pest management decisions.

• Conduct studies to quantify yield losses attributable to fruit flies. Currently, no such work

has been carried out in Zimbabwe and references are made to yield losses recorded in other

countries. This information would enable local farmers and vendors to grasp the gravity of

the fruit fly problem and stimulate concerted efforts to address the problem. As it is, the

yield losses recorded appear foreign and not something they ought to be worried about.

56

• Investigate how Geographic Information Systems (GIS) and Remote Sensing (RS) can be

used in fruit fly research and management studies in Zimbabwe. Field-based data collection

is time-consuming and costly whereas GIS is rapid and cheaper in the long run. Insect

infestation produces stress on the host plant. This stress can be visually detected as wilting,

discolouration, etc. If this stress can be recorded by satellite imagery, it is possible to

quantify level of infestation and possible yield losses. Similar work has been done to

evaluate the effect of water stress in maize and sugar cane plantations using GIS and RS

tools.

• Educate farmers on the need to decimate fruit fly populations ahead of the rainy season by

carrying out full cover and spot sprays on host trees during winter. This has the advantage

of reducing the amount of pesticide subsequently used in fruit trees in summer as the initial

population of fruit flies would be low.

• Conduct studies on the use food-based protein baits under Zimbabwean conditions in the

control of fruit flies. Examples of protein hydrolsates are Nasiman®, Htmlure®, Ready for

Use®, Buminal® and Hymlure®. These protein hydrolsates can be used in combination

with insecticides such astrichlorfon or Mercaptothion®.

• Investigating the effectiveness of botanicals in the control of fruit flies.

• Make concerted efforts to raise awareness on the problems of fruit flies and fruit fly

management in general. From discussions held with farmers and fruit vendors at Mbare

Musika, it was apparent that the small scale farmers were not well informed on the dangers

of fruit fly on the horticultural industry. Some of the vendors and farmers assumed that the

fruit rotting was attributable to the rising levels of atmospheric pollution in Harare.

57

REFERENCES

Abdullahi, G., Obeng-ofori, D., Afre-Nuamah, K. and Billah, M.K. 2011. Laboratory

evaluation of the susceptibility of adult African invader fly Bactrocera invadens (Diptera:

Tephritidae) to Nulure-based bait of some selected insecticides commonly used by mango

farmers in Ghana. Global Journal of Science Frontier Research 11 (1): 1-8.

Allwood, A.J. and Drew, R.A.I. (eds.) 1997. Management of fruit flies in the Pacific. A

regional symposium. Nadi, Fiji, 28–31 October 1996. ACIAR Proceedings Number 76, pp.

171-176. ACIAR, Canberra, Australia.

Aluja, M. 1984. Manejo Integrado de las Moscas de la Fruta. Talleres gráficos de la Nación,

México.

Aluja, M. 1994. Bionomics and management of Anastrepha. Annual Review of Entomology

39: 155-178.

Baker, A.C., Stone, W.E., Plummer, C.C. and McPhail, M. 1944. A review of studies on the

Mexican fruit fly and related Mexican species. United States Department of Agriculture

Miscellaneous Publications 531, 155 pp.

Barros, H.C.H.and Zucoloto, F.S. 1999. Performance and host preference of Ascia monuste

(Lepidoptera, Pieridae). Journal of Insect Physiology 40: 7-14.

Barry, J.D., Miller, N., Pinero, J., Tuttle, A., Mau, R.F.L.and Vargas, R.I. 2006. Effectiveness

of protein baits on Melon fly and Oriental fruit fly (Diptera: Tephritidae): Attraction and

feeding. Journal of Economic Entomology 99: 1161–1167.

Bateman, M.A. 1972. The ecology of fruit flies. Annual Review of Entomology 17: 493-518.

Bodenheimer, F.S. 1951. Citrus entomology. Hoitsema Brothers, Groningen (Holland)

Netherlands.

58

Bot, J. 1965. Census of a Dacinae population. Journal of the Entomological Society of South

Africa 28 (1):66-78.

Chapman, R.F. 1998. The insects: Structure and function. 4th edition. Cambridge University

Press. United Kingdom.

Clarke, A.R., Armstrong, K.F., Carmichael, A.E., Milne, J.R., Raghu, S., Roderick, G.K.

andYates, D.K. 2005. Invasive phytophagous pests arising through a recent tropical

evolutionary radiation: The Bactrocera dorsalis complex of fruit flies. Annual Review of

Entomology 50: 293-319.

Clark, L.R., Geier, P.W., Hughes, R.D., Morris, R.F. 1967. The ecology of insect populations

in theory and practice. London: Methuen.

Clements, A. 1992. The biology of mosquitoes: Development, nutrition and reproduction.

Volume 1. Chapman & Hall.

Courtney, S.P., Chen, G.K. and Gardner, A. 1989. A general model for individual host

selection. Oikos 55: 55-65.

Cowley, J.M., Baker, R.T. and Harte, D.S. 1992. Definition and determination of host status

for multivoltine fruit fly (Diptera: Tephritidae) species. Journal of Economic Entomology

85: 312-317.

CTA. 2007. How to control the Mango fruit fly. CTA Practical Guide Series 14. 6 pp.

Cunningham, R.T. 1989. Parapheromones, pp. 221-229. In: Robinson, A.S. and Hooper, G.

(eds.). Fruit flies: Their biology,natural enemies and control. Volume 3A. Elsevier,

Amsterdam.

Daly, H.V., Doyen, J.T. and Purcell, A.H. 1998. Introduction to insect biology and diversity.

2nd ed. Oxford University Press, New York.

59

Danthanarayana, W. 1976. Environmentally cued size variation in the light-brown apple moth

Epiphyas postvittana (Walk.)(Tortricidae), and its adaptive value in dispersal. Qecologia

26: 121-132.

De Beer, M.S. and DeGrove, T. 2001. Fruit flies, pp. 200–207. In: De Villiers, E.A. and

Joubert, P.H. (eds.). The cultivation of mango. ARC- Institute for Tropical and Subtropical

Crops. Nelspruit, South Africa.

Delgado, C.L. and Siamwalla, A. 1997. Rural economy and farm income diversification in

developing countries. MSSD Discussion Paper Number 20, International Food Policy

Research Institute, Washington, D.C.

De Meyer, M. 2001. On the identity of the Natal fruit fly, Ceratitis rosa Karsch (Diptera,

Tephritidae). Bulletin de I’Institut Royal des Sciences Naturelles de Belgique, Entomologie

71: 55-62.

De Meyer, M., Capeland, R.S., Lux, S.A., Mansell, M., Quilici, S., Wharton, R., White, I.M.

and Zenz, N.J. 2002. Annotated checklist of host plants for Afrotropical fruit flies (Diptera:

Tephritidae) of the genus Ceratitis. Musee Royal de l’Afrique Centrale Tervuren, Belgique

27: 1-91.

Dimbi, S., Maniania, N.K., Lux, S.A. and Mueke, J.M. 2004. Effect of constant temperature

on germination, radial growth and virulence of Metarhizium anisopliae to three species of

African tephritid fruit flies. Biological Control 49: 83-94.

Dhillon, M.M., Singh, R., Naresh, J.S. and Sharma, H.C. 2005. The Melon fruit fly,

Bactrocera cucurbitae: A review of its biology and management. Journal of Insect

Science 5: 40-47.

Drew, R.A.I. and Hancock, D.L. 1994. The Bactrocera dorsalis complex of fruit flies

(Diptera: Tephritidae: Dacinae) in Asia. Bulletin of Entomological Research 2: 1-68.

60

Drew, R.A.I., Tsuruta, K. and White, I.M. 2005. A new species of pest fruit fly (Diptera:

Tephritidae: Dacinae) from Sri Lanka and Africa. African Entomology 13: 149-154.

Duyck, P.F. and Quilici, S. 2002. Survival and development of different life stages of three

Ceratitis spp. (Diptera: Tephritidae) reared at five constant temperatures. Bulletin of

Entomological Research 92: 461-469.

Duyck, P.F., David, P. and Quilici, S. 2004. A review of relationships between interspecific

competition and invasions in fruit flies (Diptera: Tephritidae). Ecological Entomology 29

(5): 511–520.

Duyck, P.F., David, P., Junod, G., Brunei, C., Dupont, R. and Quilici, S. 2006a. Importance of

competition mechanisms in successive invasions by polyphagous tephritids in La Reunion.

Ecology 87 (7): 1770–1780.

Duyck, P.F., David P., and Quilici, S. 2006b. Climatic niche partitioning following successive

invasions by fruit flies in La Reunion. Journal of Animal Ecology 75 (2): 518–526.

Ebeling, W. 1959. Subtropical fruit pests. University of California, Berkeley.

Economopoulos, A.P. and Haniotakis, G.E. 1994. Advances in attractant and trapping

technologies for tephritids, pp. 57-66. In: Calkins, C.O., Klassen, W. and Liedol, P. (eds.).

Fruit flies and the sterile insect technique. CRC Press, Boca Raton.

Edgar, B.A. 2006. How flies get their size: genetics meets physiology. Nature Reviews

Genetics 7: 907–916.

Ekesi, S., Nderitu, P.W. and Chang, C.L. 2004. Adaptation to and small-scale rearing of

invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) on artificial diet. Annals of the

Entomological Society of America 100: 562-567.

Ekesi, S. 2006. Tephritid fruit flies in Africa – Fact sheets of some economically important

species, pp. B1-17. In: Ekesi, S. and Billah, M.K. (eds.). A field guide to the management

61

of economically important tephritid fruit flies in Africa. ICIPE Science Press, Nairobi,

Kenya.

Ekesi, S. and Lux, S.A. 2006. Fruit fly suppression- Purpose, tools and methodology, pp. D1-

5. In: Ekesi, S. and Billah, M.K. (eds.). A field guide to the management of economically

important tephritid fruit flies in Africa. ICIPE Science Press, Nairobi, Kenya.

Ekesi, S. and Billah, M.K. (eds.) 2006. A field guide to the management of economically

important tephritid fruit flies in Africa. ICIPE Science Press, Nairobi, Kenya.

Elnagar, S., El Sheikh, M.A.K., Hashem, A.G. and Afia, Y.E. 2008. Relative abundance of

Bactrocera zonata and Ceratitis capitata on fruit hosts in Egypt. Proceedings of the 23rd

International Congress of Entomology, 6–12 July 2008, International Convention Centre,

Durban, South Africa.

Elzinga, R.J. 2004. Fundamentals of entomology, 6th ed. Pearson Prentice Hall, New Jersey.

Fletcher, B.S. and Giannakakis, A. 1973. Sex pheromone production in irradiated males of

Dacus (Strumeta) tryoni. Journal of Economic Entomology 66: 62-64.

Fletcher, B.S. 1987. The biology of Dacine fruit flies. Annual Review of Entomology 32: 115–

144.

Fletcher, B.S. 1989. Ecology: Movements of tephritid fruit flies, pp. 209-219. In: Robinson,

A.S. and Hooper, G. (eds.). World crop pests 3(B). Fruit flies: Their biology, natural

enemies and control. Elsevier, Amsterdam, Netherlands.

Fitt, G.P. and O’Brien, R.W. 1985. Bacteria associated with four species of Dacus (Diptera:

Tephritidae) and their role in the nutrition of the larvae. Oecologia 67: 447-454.

Food and Agriculture Organisation (FAO). 1999. Glossary of phytosanitary terms.

ISPM/NIMP/NIMF Publication Number 5. Rome. 77 pp.

62

Foote, R.H., Blanc F.L., Norrbom, A.L. 1993. Handbook of the fruit flies (Diptera:

Tephritidae) of America north of Mexico. Ithaca, NY/London: Comstock. 571 pp.

French, C. 2005. The new invasive Bactrocera species. Insect Pest Control Newsletter 65: 19-

20.

Goergen, G., Vayssières, J., Gnanvossou, D. and Tindo, M. 2011. Bactrocera invadens

(Diptera: Tephritidae), a new invasive fruit fly pest for the Afrotropical region: Host plant

range and distribution in West and Central Africa. Environmental Entomology 40 (4): 844-

854.

Greany, P.D. 1989. Host plant resistance to tephritids: An under-exploited control strategy,

pp. 353-362. In: Robinson, A.S. and Hooper, G. (eds.). Fruit flies: Their biology,natural

enemies and control. Elsevier, New York.

Grimaldi, D. and Engel, M.S. 2005. Evolution of insects. Cambridge University Press, Hong

Kong.

Gu, H. and Walter, G.H. 1999. Is the common Sowthistle (Sonchus oleraceus) a primary host

plant of the Cotton bollworm, Helicorvepa armigera (Lep., Noctuidae)? Oviposition and

larval performance. Journal of Applied Entomology 123: 99-105.

Gullan, P.J. and Cranston, P.S. 1996. The insects: An outline of entomology. Chapman & Hall,

New York, London.

Grove, T., De Beer, M.S., Droyer, S. and Steyn, W.P. 1998. Monitoring fruit flies in avocado

orchards. South African Growers Association Yearbook 21: 80-82.

Hagen, K.S. 1958. Honeydew as an adult fruit fly diet affecting reproduction, pp. 25-30. In:

Becker, E.C. (ed.). Proceedings of the 10th International Congress of Entomology.

Mortimer, Ottawa.

63

Hadven, W.L., Small, A., Kitching, R.L. and Drew, R.A.I. 1998. Potential suitability of North

Queensland rainforest sites as habitat for the Asian papaya fruit fly Bactrocera papaya

Drew & Hancock (Diptera: Tephritidae). Australian Journal of Entomology 37: 219-227.

Hancock, D.L. 1986. A taxonomic basis for the study of fruit flies (Diptera: Tephritidae) of

Zimbabwe. DPhil.Thesis, University of Zimbabwe.

Hancock, D.L. 1989. Pest status: Southern Africa, pp. 51-58. In: Robinson, A.S. and Hooper,

G. (eds.). World crop pests 3(A). Fruit flies:Their biology, natural enemies and control.

Elsevier, Amsterdam, Netherlands.

Heath, R.R., Epsky, N.D., Bloem, S., Acajabon, F., Guzman, A. and Chambers, D. 1994. pH

effect on the attractiveness of corn hydrolysate to the Mediterranean fruit fly and several

Anastrepha species (Diptera: Tephritidae). Journal of Economic Entomology 87: 1009–

1013.

Heath, R.R., Epsky, N.D., Dueben, B.D., Rizzo, J. and Jeronimo, F. 1997. Adding methyl-

substituted ammonia derivatives to a food-based synthetic attractant on capture of

Mediterranean and Mexican fruit flies (Diptera: Tephritidae). Journal of Economic

Entomology 90: 1584-1589.

Hendrichs, J.P. and Hendrichs, M.A. 1990. Mediterranean fruit fly (Diptera:Tephritidae) in

nature: location and diel pattern of feeding and other activities on fruiting and non-fruiting

hosts and non-hosts. Annals of the Entomological Society of America 83: 632-641.

Hendrichs, J.P., Katsoyannos,B.I., Papaj, D.R. and Prokopy, R.J. 1991. Sex differences in

movement between natural feeding and mating sites and trade-offs between food

consumption, mating success and predator evasion in Mediterranean fruit flies (Diptera:

Tephritidae). Oecologia 86: 223-231.

64

Hendrichs, J.P., Katsoyannos, B.I. and Prokopy, R.J. 1993. Bird faeces in the nutritionof adult

Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) in nature. Mitteilungen

der Deuschen Gesellschaft für Allgemeine und Angewandte Entomologie 8: 703-707.

Hendrichs, J.P. and Prokopy, R.J. 1994. Food foraging behavior of frugivorous fruitflies, pp.

37-55. In: Calkins,C.O., Klassen, W. and Liedo, P.(eds). Fruit flies and the sterile insect

technique. CRC Press, Boca Raton.

Hoffman, A.A., Ratna, F., Sgrò, C.M., Barton, M., Blacket, M., Hallas, R., De Garis, S. and

Weeks, A.R. 2007. Antagonistic selection between adult thorax and wing size in field

released Drosophila melanogaster independent of thermal conditions. Journal of

Evolutionary Biology 20: 2219-2227.

Huffacker, C.B. and Rabb, R.L. (eds.) 1984. Ecological entomology. John Wiley & Sons,

New York.

Huk, T. and Kuhne, B. 1999. Substract selection by Carabus elatratus (Coleoptera:

Carabidae) and its consequence for offspring development. Oecologia 121: 348-354.

IAEA [International Atomic Energy Agency]. 2003. Trapping guidelines for area–wide fruit

fly programmes. VIENNA, TG/FFP-2003.

Jaenike, J. 1990. Host specialization in phytophagous insects. Annual Review of Ecology and

Systematics 21: 243-273.

Jang, E.B. and Light, D.M. 1996. Olfactory semiochemicals of tephritids, pp.73–84. In:

McPheron, B. A. and Steck, G. J. (eds.). Fruit fly pests: A world assessment of their

biology and management. CRC Press/Lewis Publishers. CRCpress.com Boca Raton

Florida.

Javaid, I. and De Lima, C.P.F. 1979. Attack of mangoes in Zambia by the fruit fly

Pardalaspis cosyra. Bulletin of African Insect Science 3: 17.

65

Javaid, I. 1986. Causes of damage to some wild mango fruit trees in Zambia. International

Pest Control 28: 98-99.

José, L., Cugala, D. and Santos, I. 2012. Assessment of invasive fruit fly fruit infestation and

damage in Cabo Delgado province, Northern Mozambique. African Crop Science Journal

211: 21-28.

Labuschagne, T., Brink T., Steyn, W.P., De Beer, M.S. 1996. Fruit flies attacking mangoes –

their importance and post harvest control. Yearbook South African Mango Growers’

Association 16: 17-19.

Lawson, A.E., Mcguire, D.J., Yeates, D.K., Drew, R.A.I. and Clarke, A.R. 2003. Dorsalis: An

interactive identification tool to fruit flies of the Bactrocera dorsalis complex. Griffith

University, Brisbane, Australia.

Http://www.Arjournals.Annualreviews.Org/Doi/Abs/10.11466/Annurev.Ento.50.071803.1

30428.

Lloyd, A.C., Hamacek, E.L., Smith, D., Kopittke, R.A. and Gu, H. 2013. Host susceptibility

of citrus cultivars to Queensland fruit fly (Diptera: Tephritidae). Journal of Economic

Entomology 106 (2): 883-890.

Lux, S.A., Zenz, N. and Kimani, S. 1998. The African fruit fly initiative: Development,

testing and dissemination of technologies for the control of fruit flies. ICIPE Annual

Scientific Report 1998-1999.

Lux, S.A., Ekesi, S., Dimbi, S., Mohamed, S.A. and Billah, M.K. 2003. Mango-infesting fruit

flies in Africa: Perspectives and limitations of biological approaches to their management,

pp. 277-293. In: Neuenschwander,P., Borgemeister, C. and Langewald, J. (eds.). Biological

control in IPM systems in Africa. CAB International. Wallingford, UK.

66

Malio, E. 1979. Observations on the Mango fruit fly Ceratitis cosyra in the Coast province,

Kenya. Kenya Entomologist’s Newsletter 10: 7.

Manrankan, A. 2006. Fruit fly monitoring – Purpose, tools and methodology, pp. C1-14. In:

Ekesi, S. and Billah, M.K. (eds.). A field guide to the management of economically

important tephritid fruit flies in Africa. The International Centre for Insect Physiology and

Ecology (ICIPE), Nairobi, Kenya.

McQuate, G.T.and Vargas, R.I. 2007. Assessment of attractiveness of plants as roosting sites

for the Melon fly, Bactrocera cucurbitae, and Oriental fruit fly, Bactrocera dorsalis.

Journal of Insect Science 7(57): 1536–2442.

Mohyuddin, A.I. and Mahmood, R. 1993. Integrated control of mango pests in Pakistan. Acta

Horticulturae 341: 467-483.

Monro, J. 1966. Population flushing with sexually sterile insects. Science 151: 1536-1538.

Mwatawala, M.W., White, I.M., Maerere, A.P., Senkondo, F.J. and De Meyer, M. 2004. A

new invasive Bactrocera species (Diptera: Tephritidae) in Tanzania. African Entomology

12: 154-156.

Mwatawala, M.W., De Meyer, M., Makundi, R.H. and Maerere, A.P. 2006. Seasonality and

host utilization of the invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) in

Central Tanzania. Journal of Applied Entomology 130: 530-537.

Mwatawala, M.W., De Meyer, M., Makundi, R.H. and Maerere, A.P. 2009. An overview of

Bactrocera (Diptera, Tephritidae) invasions and their speculated dominancy over native

fruit fly species in Tanzania. Journal of Entomology 6 (1): 18-27.

Nasci, R. 1986. The size of emerging and host-seeking Aedes aegypti and the relation of size

to blood-feeding success in the field. Journal of the American Mosquito Control

Association 2 (1): 61-62.

67

Navarro-Campos, C., Martínez-Ferrer, M.T., Campos, J.M., Fibla, J.M., Alcaide, J., Bargues,

L., Marzal, C. and Garcia-Mari, F. 2011. The influence of host fruit and temperature on the

body size of adult Ceratitis capitata (Diptera: Tephritidae) under laboratory and field

conditions. Environmental Entomology 40 (4): 931-938.

Navarro-Llopis, V., Vacas, S., Zarzo, M. and Primo, J. 2012. Dispersal ability of Ceratitis

capitata (Diptera: Tephritidae): Edge effect in area-wide treatments. Journal of Applied

Entomology doi:10.1111/jen.12029.

NERC. 2010. Trans-boundary plant pests and diseases in the Near East; with the emphasis on

wheat stem black rust. Report of The Thirtieth Near East Regional Conference (NERC),

held in Khartoum, Sudan, 4-8 December 2010. FAO Regional Office for the Near East.

Nijihout, H.F.G., Davidowitz, G. and Roff, D.A. 2006. A quantitative analysis of the

mechanisms that control body size in Manduca sexta. Journal of Biology 5: 1-15.

Nishida, T. 1963. Zoogeographical and ecological studies of Dacus cucurbitae in India.

Hawaii Agricultural Experimental Station Technical Bulletin 54: 28.

Nishida, T. 1980. Food system of tephritid fruit flies in Hawaii. Proceedings of the Hawaiian

Entomological Society 23: 245-253.

Ng, D. 1988. A novel level of interactions in plant-insect systems. Nature 334: 611-613.

Norrbom, A.L., Carroll, L.E., Thompson, F.C., White, I.M. and Freidberg, A. 1999.

Systematic database of names. Fruit fly expert identification system and systematic

information database. Myia 9: 65-251.

ODI/DFID [Overseas Development Institutes/ Department for International Development].

2004. Rethinking global agricultural commodities. London. Available at: http://dfid-

agricultureconsultation.nri.org/summaries/wp10.pdf

68

Papachristos, D.P., Paradopoulos, N.T. and Nanos, G.D. 2008. Survival and development of

immature stages of the Mediterranean fruit fly (Diptera: Tephritidae) in citrus fruit. Journal

of Economic Entomology 101: 866-872.

Papachristos, D.P., Kimbaris, A.C., Paradopoulos, N.T., and Polissiou, M.G. 2009. Toxicity

of citrus essential oils against Ceratitis capitata (Diptera: Tephritidae) larvae. Annals of

Applied Biology 155: 381-389.

Paull, R.E. and Armstron, J.W. (eds.) 1994. Insect pests and fresh horticultural products:

Treatments and responses. CABI Publishing, UK.

Peña, J.E., Mohyuddin, A.I. and Wysoki, M. 1998. A review of the pest management situation

in mango agroecosystems. Phytoparasitica 26: 129-148.

Prokopy, R.J. 1976. Feeding, mating, and oviposition activities of Rhagoletis fausta flies in

nature. Annals of the Entomological Society of America 69: 899-904.

Putruele, M.T.G. 1996. Host for Ceratitis capitata and Anastrepha fraterculus in the North

Eastern province of Entre Ríos, Argentina, pp. 343-345. In: McPheron, B.A. and Steck,

G.J. (eds.). Fruit fly pests. A world assessment of their biology and management. Florida.

Rausher, M.D. 1985. Variability for host preference in insect populations: Mechanistic and

evolutionary models. Journal of Insect Physiology 31: 873-889.

Rendell, C.H., Mwashayenyi, E. and Banga, D.J. 1995. The Mango fruit fly: Population and

varietal susceptibility studies. Zimbabwe Science News 29: 12-14.

Renwick, J.A.A. 1989. Chemical ecology of oviposition in phytophagous insects. Experientia

45: 223-228.

Rhode, R.H., Perdomo, A., Daxl, R. and Gutierrez, L. 1972. Control of Mediterranean fruit

flies in shade grown coffee with ultra low volume aerial insecticide applications. Journal of

Economic Entomology 65: 1749-1750.

69

Rwomushana, I., Ekesi, S., Gordon, I. and Ogol, C. 2008. Host plants and hosts plant

preference studies for Bactrocera invadens (Diptera: Tephritidae) in Kenya, a new invasive

fruit fly species in Africa. Annals of Entomological Society of America 101 (2): 331-340.

Sadeghi, H. and Gilbert, F. 1999. Individual variation in oviposition preference, and its

interaction with larval performance in a insect predator. Oecologia 118: 405- 411.

Singer, M.C. 1986. The definition and measurement of oviposition preference in plant-feeding

insects, pp. 65-94. In: Miller, J.R. and Miller,T.A. (eds.). Insect-plant interactions.

Springer-Verlag, New York.

Smith, H.T. 1999. USDA Fruit fly Cooperative Control Program, Draft Environmental Impact

Assessment, United States Department of Agriculture, USA.

Southwood, T.R.E. 1966. Ecological methods with particular reference to the study of insect

populations. London, Methuen. 391 pp.

Stamp, N.E. 1990. Growth versus molting time of caterpillars as a function of temperature,

nutrient concentration and phenolic rutin. Oecologia 82: 107-113.

Stark, J.D. 1988. Hind tibial length: A convenient parameter for instar differentiation in

Leptoceridia (Trichoptera). New Zealand Entomologist 11: 76-78.

Steck, G.J. 2000. Ceratitis cosyra (Walker) (Diptera: Tephritidae). Florida Department of

Agriculture & Consumer Services, Division of Plant Industry Circular Number 403

November/December 2000.

USDA NASS. 2006. California County Agricultural Commissioner’s Data, 2005. United

States Department of Agriculture, National Agricultural Statistics Service, California Field

Office, Sacramento, California.

70

Vargas, R.I. and Prokopy, R.J. 2006. Local attraction and feeding response of Melon flies and

Oriental fruit flies (Diptera: Tephritidae) to various protein baits with and without

spinosad. Hawaiian Entomological Society Proceedings 38: 49–60.

Vayssières, J.F., Carel, Y., Coubes, M. and Duyck, P.F. 2008. Development of immature

stages and comparative demography of two cucurbit-attacking fruit flies in Reunion Island:

Bactrocera cucurbitae and Dacus cilitus (Diptera: Tephritidae). Environmental

Entomology 37 (2): 307–314.

Vayssières, J.F., Goergen, G., Lokossou, O., Dossa, P. and Akponon, C. 2005. A new

Bactrocera species in Benin among Mango fruit fly (Diptera: Tephritidae) species. Fruits

60: 371-377.

Waage, J.K., Woodhall, J.W., Bishop, S.J., Smith, J.J., Jones, D.R. and Spence, N.J. 2009.

Patterns of plant pest introductions in Europe and Africa. Agricultural Systems 99: 1-5.

Warburg, M.S. and Yuval, B. 1997. Effects of energetics reserves on behavioral patterns of

Mediterranean fruit flies (Diptera:Tephritidae). Oceologia 112: 314-319.

Wasserman, S.S. and Futuyma, D.J. 1981. Evolution of host plant utilization in laboratory

populations of Southern cowpea weevil, Callosobruchus maculates Fabricius. Evolution

35: 605-617.

Weems, H.V. and Fasulo, T.R. 2002. Natal fruit fly; Natal fly: Ceratitis rosa Karsch (Insecta:

Diptera: Tephritidae). EENY-257 (DPI Entomology Circular Number 51) Entomology and

Nematology Department, Florida Cooperative Extension Service, Institute of Food and

Agricultural Sciences, University of Florida.

Weinberger, K. and Lumpkin, T.A. 2007. Diversification into horticulture and poverty: A

research agenda. World Development 35: 1464–1480.

71

Wharton, R.A., Trostle, M.K., Messing, R.H., Copeland, R.S., Kimani Njongu, S.W., Lux, S.,

Overholt, W.A., Mohamed, S. and Sivinski, J. 2000. Parasitoids of Medfly, Ceratitis

capitata and related tephritids in Kenya coffee: A predominantly koinobiont assemblage.

Bulletin of Entomological Research 90: 517-526.

White, I.M. and Elson-Harris M. 1992. Fruit flies of economic significance: Their

identification and bionomics. International Institute of Entomology/CAB International,

Wallingford.

White, I.M. and Goodger, K.F.M. 2009. African Dacus (Diptera: Tephritidae): New species

and data, with particular reference to the Tel Aviv University collection. Zootaxa 2127: 1-

49.

World Bank, 2008. World Development Report: Agriculture for Development. The World

Bank, Washington.

www.weather-spark/history/29149/2013/Harare-Mashonaland-East-Zimbabwe.

Zwölfer, H. 1979. Strategies and counterstrategies in insect population systems competing for

space and food in flower heads and galls. Fortschritte der Zoologie 25: 331–353.

Zwölfer, H. 1983. Life systems and strategies of resource exploitation in tephritids, pp. 16–30.

In: Cavalloro, R. (ed.). Fruit flies of economic importance. Proceedings of the CEC/IOBC

International Symposium. Rotterdam: Balkema.