International Journal of Tropical Insect Science Vol. 32, No. 1, pp. 12–23, 2012 doi:10.

1017/S1742758412000045
q icipe 2012

Species composition of fruit flies (Diptera:

Tephritidae) in the Citrus Museum at the
Agricultural Research Centre (ARC),
Kade, Ghana
Caroline Ngichop Foba1,2*, Kwame Afreh-Nuamah2,
Maxwell Kelvin Billah2 and Daniel Obeng-Ofori2
1
icipe – African Insect Science for Food and Health, PO Box 30772-00100,
Nairobi, Kenya and 2African Regional Postgraduate Programme in
Insect Science (ARPPIS), Sub-regional Centre for West Africa,
University of Ghana, Legon, Ghana

(Accepted 9 December 2011; First published online 7 March 2012)

Abstract. To determine species composition of fruit flies on six cultivated varieties of citrus
(Late Valencia orange, Pineapple orange, Ovaleto, Mediterranean sweet lemon, Satsuma
tangerine and Ortanique orange), a study was conducted at the Agricultural Research
Centre, Kade, Ghana. Improvised Lynfield baited traps (methyl eugenol (ME) and
citrus juice (CJ)) and McPhail baited traps (trimedlure (TML)) were used. Ripe infested
fruits from the selected varieties were also collected and incubated. Tephritid fruit fly
species from trapping were identified as Bactrocera invadens Drew, Tsuruta & White,
Bactrocera cucurbitae (Coquillet), Ceratitis ditissima Munro, C. anonae Graham, C. capitata
(Wiedemann), C. bremii Guerin-Meneville, Dacus bivittatus (Bigot), D. punctatifrons Karsch
and Trirhithrum Bezzi. A total of 35,247 fruit flies were collected from the traps, with
densities of 10.38, 1.00 and 0.27 flies/trap/day for ME, CJ and TML traps, respectively.
All incubated fruit varieties showed co-habitation of three different species (C. ditissima,
C. anonae and B. invadens) in each of them. In addition, one Dacus vertebratus was obtained
from dropped Late Valencia fruits. Moreover, three individual Fopius caudatus (Szèpligeti)
parasitoids were recorded from the infested incubated fruits. Ranking of the different
fruit fly species from infested incubated host fruits was as follows: C. ditissima (476) . C.
anonae (74) . B. invadens (71) and D. vertebratus (1). Competitive ability among the
invasive flies in their process to infest the six citrus varieties was observed. These findings
could serve as a useful starting point for the development of a reliable catalogue of host
diversity, fruit fly species diversity and associated natural enemy records in Ghana.

Key words: species composition, tephritid flies, citrus varieties, ranking, Fopius caudatus

Introduction in fruit consumption (Lux et al., 2003; Weinberger

Fruit production and export is one of the fastest
growing agricultural sectors in Africa, providing
income and employment. Besides export, the
changing dietary patterns have led to an increase
*E-mail: chopcarolilyn@yahoo.ca
and Lumpkin, 2007; Ekesi, 2010).
In Ghana, citrus is a major cultivated cash crop
yielding the highest income per unit area com-
pared with other cash crops (Ofosu-Budu et al.,
2007). In Ghana, the crop is cultivated in the semi-
deciduous forest zone that covers parts of the
Ashanti, Brong-Ahafo, Eastern, Western, Central
 Species composition of tephritid fruit flies in Citrus Museum
and Volta regions (Ofosu-Budu et al., 2007). About
26,000 – 30,000 ha of land has been cropped with
citrus in both the Eastern and Ashanti regions
(Ofosu-Budu et al., 2007) with a production level
estimated at over 20,000 metric tonnes annually
(GEPC, 2006). Many constraints, however, hinder
this important horticultural crop from realizing its
full potential in Ghana as well as in other African
countries. Ranking high among these constraints is
serious infestation with fruit flies, especially since
the introduction of the invasive species Bactrocera
invadens Drew, Tsuruta & White (Diptera: Tephriti-
dae) into Africa in 2003 (Lux et al., 2003). In Ghana,
tephritid fruit flies have been reported to cause yield
losses ranging between 60 and 85%, depending on
citrus cultivar, level of infestation and season (Billah
et al., 2006). This led to the reduction in the fruit
quality for both domestic and foreign consumption
in Ghana and many other African countries.
Most tropical fruits are exported to countries that
regard fruit flies as a major threat (because of its
quarantine pest status), thereby restricting infested
fruits from international markets.
Information on the seasonal abundance and
the peak of pest damage, as well as estimates of
changes in pest numbers are important components
of any pest management strategy (Dent, 1992). This
is because information on the timing and extent
of pest outbreak can improve efficiency of control
measures (Dent, 1992). Reliable identification of
the pest species is an important prerequisite for its
effective subsequent management and quarantine
measures especially if integrated pest management
(IPM) or biological control is applied.
Fig. 1. Map of the study area showing the various citrus varieties grown and other nearby fruit fly host orchards
13
Until recently, damage to citrus fruits at the
Agricultural Research Centre (ARC), Kade, in the
Eastern Region, has always been attributed to
Ceratitis capitata (Weidemann) (Diptera: Tephritidae)
as the dominant species of fruit fly in citrus plan-
tations (Afreh-Nuamah, 1985, 1999, 2007; Appiah
et al., 2009). However, recent studies indicated that
there were other fruit fly species attacking citrus in
Ghana (M. K. Billah, unpublished data). Thus there
is the need to determine the prevalent species in
the study area since knowledge of the tephritid
spectrum in any given area is a prerequisite for the
development of an IPM programme to alleviate the
pest problem (Mwatawala et al., 2006). The research
was, therefore, undertaken to catalogue the range
of fruit fly species attacking six cultivated varieties
of citrus at the ARC, Kade, to determine the pest
status of the different species of fruit flies and
thereby confirm whether C. capitata is the fruit fly
causing damage to citrus at the Research Centre.
Materials and methods
Study area
The study was conducted at the Citrus Museum of
the ARC, Kade, in the Eastern Region of Ghana
(Fig. 1). The Citrus Museum, which was established
in 1995, is an orchard of about 18 ha with a collection
of all citrus varieties grown at the Research Centre.
Six plotted sites all situated in the Citrus Museum
at W00853.8510 (longitude), N06808.5990 (latitude)
and 179 masl (altitude) were selected for the study.
All citrus plants of the same variety are planted in
Regional capital
Volta Lake
River Vegetation
Coastal scrub and Grassland
Guinea Savanna
Mosit-Semi Deciduous Forest
Rain Forest
Strand and Mangrove Zone
Scale 1:1131164647939 Sudan Savanna
14 C.N. Foba et al.
rows of ten plants within four columns making a
total of 40 plants per plot. The distance between
plants is evenly spaced at 6 m apart. Each of the
plotted sites covers an area of about 1440 m2. Mature
fruits are always present at any given time since the
six citrus varieties flower and therefore mature at
different times of the year. The age of the trees within
the orchard was 14 years and the average height of
citrus trees in the orchard was approximately 7 m.
Trapping technique
The trapping technique used was identical to that
described by Billah et al. (2006) and Manrakhan
(2006). Improvised methyl eugenol (ME)- and
trimedlure (TML)-baited traps were used to attract
Bactrocera and Ceratitis species males, respectively,
while improvised citrus juice (CJ)-baited traps were
used to attract both male and female fruit flies. The
TML (tert-butyl 4 (and 5)-chloro-2-methylcyclohex-
ane-1-carboxylate)-baited trap (Plate 1) was a
modified liquibaitor trap medfly (a new version of
the McPhail trap). One strip of dichlorvos insecti-
cide was used per TML trap. The TML-baited traps
consisted of a two-piece cylinder-shaped invagi-
nated plastic container with a diameter of 14.5 cm
and a height of 18.5 cm, through which the green
bait basket was incorporated at the top of the trap.
The ME (4-allyl-1,2-dimethoxybenzene)-baited trap
(Plate 2) and the CJ (250 ml CJ with a Brix of about
10.508Bx and a titratable acidity (TA) of about
0.70%)-baited traps (Plate 3) consisted of a two-piece
plastic container with four holes (2 cm in diameter)
evenly spaced around its upper half. The ME-baited
trap (8 cm in diameter and 13 cm in height) and CJ-
baited trap (6.1 cm diameter £ 21.6 cm height) had
a small hole on the lid through which the traps
were suspended on the branches at approximately
2 m from the ground. CJ lure was used for the
detection of both male and female fruit flies because
Plate 1. TML-baited trap
Plate 2. ME-baited trap
of its affordability and easy accessibility to the local
citrus farmers. The TML-baited traps were supplied
by USDA-APHIS-PRQ, USA and ME-baited traps
were supplied by Agrisence Ltd, UK and Messrs
Ransford Attatsi Enterprises, Ghana.
Grease was smeared on the middle third portion
of the strings that were used to hang the traps on the
trees to prevent entry of ants and other predators. To
ensure that the flies did not get stuck outside the
traps, hand gloves were used with great care to avoid
contamination of the outer parts of the traps. Two
traps of ME, TML and CJ were placed in each of the
six citrus plots. The distance between the traps was
30 m to prevent inter-trap interference (Ekesi and
Billah, 2006). Traps were inspected and emptied
twice every week throughout the sampling period
from September 2008 to May 2009 and the total
number of tephritid flies caught in the orchard was
recorded. The total number of tephritid flies trapped
in a given month in a particular study site was
obtained by adding the daily captures. Each ME
block was replaced every 16 weeks and each TML
Plate 3. CJ-baited trap
 Species composition of tephritid fruit flies in Citrus Museum 15
plug was replaced every 6 weeks after careful
washing of the traps. This was based on the
manufacturer’s recommendation and personal obser-
vation from preliminary studies in the field, when fly
capture started to decline. CJ was replaced every
week after careful washing of the traps.

Pest status of the different species of fruit flies

To establish the actual fruit flies causing damage to
citrus fruits at the Research Centre, fruits of six
different citrus varieties were collected and incu-
bated to rear out the tephritid flies from them.
Sampling of mature fruits was carried out from
October 2008 to March 2009 depending on fruit
availability per variety. Pineapple, Ovaleto and
Satsuma fruits were collected from October to early Plate 4. Plastic rearing containers for larvae pupation
November 2008. Mediterranean Sweet fruits were
collected in the month of November 2008 while
Ortanique fruits were collected in January 2009. attain full adult colouration and characteristics.
However, to determine the fly abundance at different Adult flies were fed with an artificial diet consisting
dates of harvesting/maturity stage, fruit collection of yeast hydrolysate powder and sugar in a ratio of
was extended from January 2009 to March 2009 for 1:3. Flies were also provided with water and pure
Late Valencia to include fallen fruits at three stages honey. Misidentifications are possible if reared
of maturity (i.e. at the early stage, peak period and at specimens are not fed for a few days before being
the late stage). Late Valencia is considered the most killed and observed under a microscope (White and
preferred late-season sweet orange in the world Elson-Harris, 1992). Flies were frozen to death and
(Davies and Albrigo, 1994) and the most satisfying preserved in 80% alcohol. The flies were examined
cultivar of sweet oranges in the tropics. In Ghana, it is under a dissecting microscope for taxonomic
also the commonest variety of citrus grown on a details. Identification was done using morphologi-
commercial scale (Ofosu-Budu et al., 2007). Two cal keys and identification keys from the African
hundred harvested ripe fruits were collected for each Fruit Fly Initiative, Nairobi, Kenya (M. K. Billah,
variety at the peak stage of maturity. In addition, 200 unpublished data, 2003). Dr M. K. Billah sent all
fruits each of Late Valencia were collected at the early samples (flies and parasitoids) to the Entomological
and late stages of maturity, making a total of 1600 Museum at the Zoology Department (now Depart-
fruits collected. ment of Animal Biology and Conservation
Fruit incubation was done according to the method Sciences), University of Ghana for further identifi-
described by Ekesi and Billah (2006) and by personal cation and confirmation.
instruction of M. K. Billah. All fruit samples were
held in bulk and weighed and incubated for 2 weeks,
after which each fruit was carefully dissected and the
fruit fly larvae removed and incubated over sieved
sterilized sand (i.e. sand sterilized by baking in an
oven at 120 oC for 24 h) in plastic rearing containers
(0.48 £ 0.29 £ 0.09 m) (Plate 4). After 2 weeks of
incubation, the sand was poured onto a wire mesh to
sieve and collect any pupa that had pupated in it.
Any larva found in the sand after sieving was returned
to the sand to continue with the developmental
process. Pupae collected were counted and placed
in Petri dishes over moistened white tissue paper
and then put into plastic emergence cages of height
21.3 cm and diameter 19 cm (Plate 5). The emergence
containers had an opening at the side and fine netting
on the sides and top to ensure good ventilation.
Adult flies that emerged from puparia were
counted, sexed and transferred to insect cages. Flies
were kept alive for at least 5 days to develop and Plate 5. Plastic emergence containers
16 C.N. Foba et al.
Determination of total or titratable acidity (TA), total
soluble solids (TSS) and peel thickness (PT) of selected
citrus fruit varieties
The TA and the TSS were determined from fruit
juices of the six varieties of citrus sampled. The
juices were extracted from harvested five randomly
selected ripe fruits of each variety. For each variety,
juice from the five fruits was bulked together. For
TA, 25 ml of the juice was taken and diluted with
250 ml of distilled water. Fifty millilitres of the
diluted solution were then taken and titrated
against 0.1 N NaOH solution in a pipette until a
neutral solution was formed. This was determined
by the volume of the 0.1 N NaOH solution that was
required to change the CJ colour from orange to
light pink, and the total acidity calculated as
follows:
1 analysis were applied to the total number of different
% Total acid ¼ £ equivalent weight of acid
10  Citrus Museum and some climatic factors using
£ normality of NaOH

£ titre
weight of sample :
The formula is simplified as: % total acid ¼
0.140 £ titre.
The equivalent weight of monohydrate citric
acid is 70.0 g (Ruck, 1969).
For TSS determination, 5 ml of the pure extracted
juice was placed on an absolutely dry refractometer
prism, and the Brix value read directly at 20 8C. The
TSS of juice extract was determined in quadruplicate
(four times), and the mean value recorded. These
procedures were repeated for each of the citrus
varieties to determine their required TA and TSS
values (K.G. Ofosu-Budu; a plant physiologist at the
ARC, Kade, personal communication). The determi-
nation of citrus PT also followed the method of Ruck
(1969) and Dr Ofosu-Budu (personal communi-
cation). Fruits were cut into two cross-sections, and
a finely graduated ruler was used to measure the PT
(in mm) by placing the ruler at five different portions
and working out the mean value.
Climatic factors
Daily meteorological data for four variables, relative
humidity (RH) at 15.00 h GMT, maximum tempera-
ture at 09.00 h, total monthly rainfall and wind speed,
were obtained from a local meteorological station at
the Research Centre. Temperature and RH values
were also measured with the aid of a hydrotherm-
ometer at the Entomology Laboratory of the Research
Centre, where rearing of the flies took place.
Data analysis
Analysis of variance and multiple regression
fruit fly species attracted by the different traps in the
GENSTAT packages. Correlation analysis was also
done to determine the strength of the association
between the monthly fly captures, pest abundance
and each of the climatic factors recorded. Two-way
ANOVA was used to test for differences in the effect
of variety on the number of emerged fly species and
means were separated using the Student – New-
man – Keuls test.
Results
Fly abundance
A total of 35,247 fruit flies were collected in the traps
during the study period. In addition, a total of 8910
non-target specimens belonging to eight insect
orders and one arachnid (class Arachnida) (Table 1)
were collected in the traps. Of the total number of
fruit flies trapped, 31,402 (89.1%) were captured in

Table 1. Non-target catches (insect orders) from the different traps

Catches per trap
ME-baited TML-baited CJ-baited
Order (or Class) trap trap trap Total
Diptera 771 78 4356 5205
Coleoptera 113 37 122 272
Hymenoptera (ants) 187 46 761 994
Non-parasitic Hymenoptera 5 5
Arachnida 5 19 15 39
Lepidoptera 3 11 50 64
Neuroptera 2294 2294
Isoptera 1 1
Hemiptera 22 22
Blattodea 14 14
Total 3374 191 5345 8910
 Species composition of tephritid fruit flies in Citrus Museum
the ME-baited traps, followed by 3017 (8.6%) in the
CJ-baited traps and 828 (2.4%) in the TML-baited
traps (Table 2). To allow comparison across different
localities without regard to local conditions, fly
catches were expressed in the standard index of
number of flies per trap per day (F/T/D; IAEA,
2003). These translated to relative density values of
10.38, 1.00 and 0.27 F/T/D for the ME-, CJ- and
TML-baited traps, respectively (Table 2). Nine
different species of fruit flies namely B. invadens,
B. cucurbitae, Ceratitis ditissima, C. anonae, C. capitata,
C. bremii, Dacus bivittatus, D. punctatifrons and
Trirhithrum species belonging to four genera
(Ceratitis, Bactrocera, Dacus and Trirhithrum) were
recorded from the Citrus Museum during trapping.
Three different species belonging to two genera
(Bactrocera and Ceratitis) were captured in the ME-
baited traps. Of the total number (31,402) of fruit
flies captured in the ME-baited traps, 31,390 were B.
invadens, nine C. ditissima and three C. bremii. Of the
total number (828) of flies captured in the TML-
baited traps, seven different fruit fly species
belonging to four genera (Ceratitis, Bactrocera,
Dacus and Trirhithrum) were identified. Five hun-
dred and twenty-two flies of C. ditissima were
recorded, followed by 290 C. anonae and only five
C. capitata were captured in the traps. Of the three
remaining genera, four D. bivittatus, three B. invadens
and two each of D. punctatifrons and Trirhithrum sp.
were recorded. Of the total number (3017) of flies
captured in the CJ-baited traps, five different fruit
fly species belonging to two genera (Ceratitis and
Bactrocera) were recorded. Over 2901 C. ditissima, 77
B. invadens and 32 C. anonae were recorded. Only
four C. capitata and three B. cucurbitae were recorded.
An analysis of variance performed after log
transformation of the data (trap catches) collected
throughout the sampling period showed a signifi-
cant difference (P # 0.001) in the attractiveness of
the three baited traps. The ME-baited trap was
more attractive than the CJ- and TML-baited traps.
Collectively, climatic factors (mean RH at 15.00 h
GMT, mean maximum monthly temperature, rain-
fall and wind speed) influenced the population of
tephritid flies captured in the ME- and CJ-baited traps
by 49% (R 2 ¼ 0.4870) and 42% (R 2 ¼ 0.4170),
Table 2. Fruit fly catches from the ME-, TML- and CJ-baited traps from the Citrus Museum
Type of trap No. of flies No. of traps
ME 31,402 12
TML 828 12
CJ 3017 12
LSD (P , 0.05)
Total 35,247
ME, methyl eugenol; TML, trimedlure; CJ, citrus juice; LSD, least significant difference.
17
respectively. These suggest a weak correlation
between overall climatic factors recorded and the
population fluctuation of tephritid flies in the
ME- and CJ-baited traps. Collectively, there was no
correlation between the climatic factors, the attrac-
tiveness and the population density of flies captured
in the three traps. However, in the TML-baited traps
(Fig. 2), there was a significant effect of both wind
speed (P ¼ 0.008) and mean maximum temperature
(P ¼ 0.027) on the population of tephritid flies
captured with a correlation rate of R 2 ¼ 0.8990.
The monthly average population density of
tephritid flies captured in the TML-baited traps
had a negative correlation with mean maximum
temperature. An increase in temperature from 31 to
33 8C (September to December) resulted in a
corresponding decrease in the density of tephritid
flies (Fig. 2). In the same period, wind speed
correlated positively with the monthly average
population density of the flies captured in the TML-
baited traps where a decrease in wind speed from
633 to 492 m/h showed a corresponding decrease in
the pest density of the flies (Fig. 2).
The total rainfall recorded ranged from 5 to
249 mm, the mean maximum temperature from 30.8
to 33.9 8C, the mean wind speed from 492.2 to
747.73 m/h, and the mean RH from 47.7 to 67.8%
during the study period. The highest and lowest
rainfall values of 249.2 and 5.0 mm were recorded in
the months of January and May 2009, respectively.
Rainfall values less than 100 mm resulted in an
increase in the number of catches while the amount
of rainfall more than 100 mm (i.e. in October and
December) resulted in a decrease in the number of
flies captured by the three traps (Figs 2– 4).
Pest status of the different species of fruit flies reared
from incubated fruits
Four different species of fruit flies belonging to three
genera (B. invadens, C. ditissima, C. anonae and Dacus
vertebratus) were reared out from fruits of all six
varieties sampled (Table 3). From a total of 1600
fruits weighing 148.3 kg collected during the study
period, 622 flies were recorded from the incubated
fruits, with fallen Late Valencia fruits producing
Exposure Mean no.
period (days) Flies/trap/day of catches Non-targets
252 10.38 3.4 3374
252 0.27 1.7 191
252 1.00 2.4 5345
0.2
4099
18 C.N. Foba et al.

800 8

700 7

600 6 Average fly

density/month
Climatic factors

500 5 Total rainfall (mm)

Fly catches
400 4 Wind speed (m/h)

Mean max. temp (°C)

300 3
Mean relative
200 2 humidity (%)

100 1

0 0
Sept Oct Nov Dec Jan Feb Mar Apr May
2008 2008 2008 2008 2009 2009 2009 2009 2009

Fig. 2. The relationship between the relative average fly density captured in the TML-baited traps and some climatic
factors at ARC, Kade

36% (223), followed by 18% (113) from Satsuma,
while 14% (87), 12% (72), 8% (47) 8% (47) and 5% (33)
were recorded from Ortanique, Ovaleto, harvested
Late Valencia, Pineapple and Sweet Mediterranean
fruits, respectively. Additionally, three (one female
and two male) parasitoids identified as Fopius
caudatus (Szèpligeti) were recorded on harvested
Late Valencia and Ovaleto fruits.
All the citrus varieties sampled showed co-
habitation of three different fruit fly species in
them. The species composition of the flies in the co-
habitation was C. ditissima, C. anonae and B. invadens.
In addition to the three species, one D. vertebratus was
reared from fallen Late Valencia fruits. Five hundred
and fifty (88.4%) of the fruit flies recorded belonged
to the genus Ceratitis, 74 (11.4%) belonged to the
genus Bactrocera and one (0.2%) belonged to the
genus Dacus. Of the total number of flies recorded
in the genus Ceratitis, 476 (76.5%) were C. ditissima
and 74 (11.9%) were C. anonae. Flies in the genera
Bactrocera and Dacus, which formed 11.4% (71) and
0.2%, were identified as B. invadens and D. vertebratus,
respectively. In terms of abundance, ranking of the
individual species was as follows: C. ditissima . C.
anonae . B. invadens and D. vertebratus, represented
by 476, 74, 71 and 1, respectively (Table 4). In all the

800 350

700 300

600 Average fly

250
density/month
Climatic factors

500
Total rainfall (mm)
Fly catches

200
400 Wind speed (m/h)
150 Mean max. temp (°C)
300
Mean relative
100 humidity (%)
200

100 50

0 0
Sept Oct Nov Dec Jan Feb Mar Apr May
2008 2008 2008 2008 2009 2009 2009 2009 2009

Fig. 3. The relationship between the relative average fly density captured in the ME-baited traps and some climatic factors
at ARC, Kade
 Species composition of tephritid fruit flies in Citrus Museum 19

800 30

700
25
Average fly
600 density/month
20 Total rainfall (mm)
Climatic factors

500

Fly catches
400 15 Wind speed (m/h)

300 Mean max. temp (°C)

10
200 Mean relative
5 humidity (%)
100

0 0
Sept Oct Nov Dec Jan Feb Mar Apr May
2008 2008 2008 2008 2009 2009 2009 2009 2009

Fig. 4. The relationship between the relative average fly density captured in the CJ-baited traps and some climatic factors
at ARC, Kade

six varieties of citrus sampled, the proportion of
Ceratitis species, especially C. ditissima, reared was
overwhelmingly higher, ranging from 72.4 to 95.7%.
A two-way ANOVA showed that there were
significant differences in both the number of
emerging flies from the six incubated citrus
varieties (P ¼ 0.005) and the species composition of
the emergent flies (P ¼ ,0.001). Pairwise mean
separation using the Student–Newman–Keuls test
showed that Satsuma was the most preferred variety
followed by Ortanique, while Sweet Mediterranean
was the least preferred. Similar pairwise comparisons
revealed that C. ditissimia was significantly the most
abundant fruit fly species followed by C. anonae and
B. invadens. The latter two were not statistically
different from each other.
Of the total number (47) of flies reared from
Late Valencia fruits harvested at different stages of

Table 3. Fruit fly species reared from the different varieties of citrus
Tephritid Non-tephritid
Citrus variety species No. of flies species
Late Valencia (harvested) C. ditissima 42 Atherigona sp.
C. anonae 3
B. invadens 2
Late Valencia (fallen fruits) C. ditissima 213 Atherigona sp.
C. anonae 8
B. invadens 1
D. vertebratus 1
Pineapple (harvested) C. ditissima 35 Atherigona sp.
C. anonae 5
B. invadens 7
Ovaleto (harvested) C. ditissima 52 Atherigona sp.
C. anonae 6
B. invadens 14
Sweet Mediterranean (harvested) C. ditissima 23 Atherigona sp.
C. anonae 6
B. invadens 4
Satsuma (harvested) C. ditissima 62 Atherigona sp.
C. anonae 32
B. invadens 19
Ortanique (harvested) C. ditissima 49 Atherigona sp.
C. anonae 14
B. invadens 24
Total 622
20 C.N. Foba et al.
Table 4. Status of fruit flies reared from the fruits
Ranking status in
Species Common name Family Number terms of numbers
Flies
C. ditissima — Tephritidae 476 1
C. anonae — Tephritidae 74 2
B. invadens African invader fly Tephritidae 71 3
D. vertebratus Jointed pumpkin fly Tephritidae 1 4
Fruits
Citrus sinensis Late Valencia (H) Rutaceae 47 5
Citrus sinensis Late Valencia (F) Rutaceae 223 1
— Pineapple (H) Rutaceae 47 5
— Ovaleto (H) Rutaceae 72 4
— Sweet Mediterranean (H) Rutaceae 33 6
— Satsuma (H) Rutaceae 113 2
— Ortanique (H) Rutaceae 87 3
H, harvested; F, fallen.

maturity (i.e. early stage, peak period and at the late
stage of maturity), more than 40% of the flies
produced were recorded from Late Valencia fruits
harvested at the peak period of maturity and the late
stage of maturity. These were represented by 22
(47%) and 19 (40%), respectively, and only 6 (13%)
flies were recorded from fruits harvested at the early
stage of maturity.
Effect of total or TA, TSS and PT on adult fly emergence
The highest number (113) of flies was recorded from
incubated Satsuma fruits, with PT of 0.54 cm, TSS
of 10.6 and TA of 0.66 while Sweet Mediterranean
(TA ¼ 0.68, TSS ¼ 10.8 and PT ¼ 0.35 cm) produced
the least number (33) of flies. Late Valencia and
Pineapple, which had almost the same TA and PT
values of 1 and 0.4 cm, respectively, produced equal
numbers of flies (47). Ovaleto, which had the highest
PT and TSS values of 0.61 cm and 12.6, respectively,
recorded 72 flies. Ortanique with one of the smallest
peel thicknesses (0.35 cm) and second highest TA
value (0.70) produced the second highest number
(87) of flies (Table 5).
Discussion
During the survey conducted from September 2008
to May 2009 to evaluate and compare the attractive-
ness of fruit flies to the ME-, TML- and CJ-baited
traps, 35,247 tephritids were collected. Of the total
number of fruit flies, 89.09% were captured in the
ME-baited traps, 8.56% in the CJ-baited traps and
2.35% in the TML-baited traps. Nine species of fruit
flies were identified from the trapping. These were
B. invadens, B. cucurbitae, C. ditissima, C. anonae, C.
capitata, C. bremii, D. bivittatus, D. punctatifrons and
Trirhithrum sp., belonging to four genera (Ceratitis,
Bactrocera, Dacus and Trirhithrum). These four fruit
fly genera have earlier been reported to be of
economic importance in equatorial Africa by several
researchers (White and Elson-Harris, 1992; Thomp-
son, 1998; Billah et al., 2006; Ekesi and Billah, 2006).
There were significant differences (P # 0.001)
in the number of tephritid flies captured in the
different traps. This was probably due to the fact
that the lures attracted different types of fruit flies
and the attractiveness to non-target species other
than the tephritid flies also varied. Methyl eugenol-
baited traps attracted more of the invasive species

Table 5. Effect of some fruit quality parameters on adult fly emergence

Citrus variety PT (cm) Brix (TSS) TA No. of adult flies emerged
Late Valencia (harvested) 0.44 11.2 0.95 47
Pineapple 0.43 11.9 1.06 47
Ovaleto 0.61 12.6 1.04 72
Sweet Mediterranean 0.35 10.8 0.68 33
Satsuma 0.54 10.6 0.66 113
Ortanique 0.35 10.4 0.70 87
PT, peel thickness; TSS, total soluble solids; TA, titratable acidity.
 Species composition of tephritid fruit flies in Citrus Museum
(B. invadens) while the indigenous fly species
(mostly Ceratitis species) were attracted to the
TML-baited traps. However, different members of
the fruit fly species complex were attracted to the CJ-
baited traps.
The highest diversity of fruit flies (seven species)
was captured in the TML traps. However, the total
number of non-Ceratitis fruit fly species recorded in
this attractant trap was less (, 15). This confirms the
findings of Manrakhan (2006) that parapheromones
are highly species-specific. Of the total number of
31,402 flies captured in the ME-baited traps, 31,390
(99.96%) were B. invadens. This also proved that ME
is highly species-specific. The CJ-baited traps
recorded higher diversity of species (five species)
and were both males and females. This confirms the
findings of Manrakhan (2006) who documented that
food baits attract both male and female fruit flies and
are not species-specific.
The relative mean density of flies collected in the
different traps appeared to be influenced by the
availability of hosts (mango, avocado, citrus, sugar
apple, rambutan, pawpaw, guava, banana and
pepper) in the study area. On average, during the
periods (September 2008 and April to May 2009)
when most semi-ripe and ripe fruits were available,
higher relative average population densities of
tephritid flies were recorded. This confirms earlier
studies done by Afreh-Nuamah (1985, 1999, 2007),
Akotsen-Mensah (1999) and Appiah et al. (2009) on
the abundance and distribution of the Mediterra-
nean fruit fly (C. capitata) in Late Valencia citrus
orchards in Ghana. Similarly, Matiola et al. (1990)
also reported that significantly higher numbers of
tephritid flies were captured in pheromone traps in
Brazil during the ripening period in October and
February.
In the present study, however, the population of
tephritid flies in terms of number remained
relatively high even after harvest. This was not
surprising because in a museum situation, mature
fruits were always present in the orchard. Partial
harvesting of citrus fruits was also carried out in
the Citrus Museum during the study period. In
addition, other host fruits (mango, avocado, citrus,
sugar apple and rambutan) were also located
around the Citrus Museum. This resulted in easy
availability of hosts for the flies throughout the year.
Papadopoulos et al. (2001) and Puche et al. (2005)
showed that the availability of host fruits was one of
the most important factors that affected the
population fluctuations of fruit flies. It was also
noticed that the large numbers of fallen ripe citrus
fruits were left to rot under the trees, leading to
carry-over infestation, which increased the popu-
lation of flies during these periods.
Collectively, there was no strong relationship
observed between climatic factors and the relative
21
mean population density of tephritid flies captured
in some of the traps (ME and CJ) used during the
study. This may be due to the relative importance of
microhabitat conditions rather than general con-
ditions outside the studied field. In a closed-canopy
microhabitat like that observed in the Citrus
Museum, the local conditions could have been an
important factor in determining when the flies
moved in and out of the orchard, thereby making
them available to be attracted to the traps. This
observation confirmed the findings of Aluja and
Birke (1993), who stressed the importance of
microhabitat conditions on the presence of Anastre-
pha obliqua (Macquart) and diurnal patterns of
activity in a highly ephemeral and diversified
environment.
The African invader fly, B. invadens, which is
currently expanding its host range in Africa
(Mwatawala et al., 2009; Goergen et al., 2011), was
recorded consistently in all the six citrus varieties
sampled. Three fruit fly species namely C. ditissima,
C. anonae and B. invadens were associated with all
the six incubated citrus varieties sampled during
the study. The dominant species was C. ditissima
followed by B. invadens, which was detected in
Africa in 2003. Prior to its arrival in Ghana, only
C. ditissima and C. anonae were recorded in citrus
(M. K. Billah, unpublished data). In certain varieties,
it ranked as the second of the three species. Citrus
therefore seems to be a preferred host plant. In an
8-year study of fruit flies in Nguruman in Kenya,
Ekesi et al. (2009) documented and produced
evidence of competitive displacement of Ceratitis
cosyra by B. invadens on mango and the mechanisms
contributing to the displacement. Ceratitis cosyra has
long been recognized as the most damaging
tephritid fruit fly pest of mango in Africa including
Kenya (Lux et al., 2003). Mwatawala et al. (2009)
found eight new host plants of B. invadens, thereby
bringing the host list to a total of 37 from 29. More
recently, studies by Goergen et al. (2011) found 46
species from 23 plant families. In Ghana, work to
determine and document the host range of B.
invadens has just started at the University of Ghana
(K. Afreh-Nuamah, personal communication, 2011).
Continuous monitoring is necessary to determine
whether complete displacement of C. ditissima by B.
invadens is possible in citrus as is the case in mango.
The detection of D. vertebratus from Late Valencia
fruits is new as no record of its attack on citrus has
been documented (M. K. Billah, personal communi-
cation, 2009). Most of the Dacus species recorded in
Ghana have been found on vegetable crops.
However, this observation is not very surprising,
as the citrus fruits from which the fly was detected
were collected from the orchard floor (fallen fruits).
This record may therefore be considered as excep-
tional or accidental introduction in the study area.
22 C.N. Foba et al.
Additionally, all parasitoids recorded were
identified as F. caudatus. Trostle (2005) has already
expressed great excitement surrounding the possi-
bilities for F. caudatus, as its congener F. arisanus
(Sonan), which is also an egg-pupal parasitoid, is
widely regarded as the most successful tephritid
fruit fly parasitoid used in biological control. Fopius
caudatus is also currently being evaluated against B.
invadens in Kenya (M. K. Billah, personal communi-
cation, 2009). It may be useful to study the potential
of F. caudatus as a biological control agent against
B. invadens and other tephritid flies.
Fruit flies must reproduce irrespective of the time
of the season, whether fruits are available or not.
One way they can achieve this is to lay their eggs in
alternative host plants/fruits that will ensure
continuous survival of their progenies. The flies
then re-infest the preferred host plants when the
fruits are in season. This may be true particularly for
B. invadens, considering that they were reared from
almost all the fruits.
The medfly, C. capitata, which most attention had
been focused on, was not recorded from any of the
six citrus varieties incubated during the study. This
fly is extremely polyphagous and had been reared
on over 300 commercial and wild host plants (White
and Elson-Harris, 1992). It is therefore surprising
that C. capitata was not recorded from any of the
six citrus varieties incubated. Earlier research
workers (Akotsen-Mensah, 1999; Appiah, 2007;
Appiah et al., 2009) reported C. capitata as the most
destructive tephritid pest on citrus in Ghana. It is
therefore possible that C. ditissima, which is the most
abundant species in citrus, may have previously
been misidentified as C. capitata. This seemingly
controversial situation could have been resolved if
voucher specimens of these studies were available
for re-examination. Of all the citrus varieties
incubated, Satsuma was the most preferred variety.
Satsuma is a citrus variety in the group of mandarins
with very loose and thin peel, and it has earlier been
reported to be very susceptible to fruit fly attack in
Ghana (Afreh-Nuamah, 1985).
Atherigona species (non-tephritid flies) were also
recorded from all the citrus varieties sampled.
According to White and Elson-Harris (1992),
Atherigona species are often found in abundance in
fruit crops, but they are usually thought to be
secondary invaders because they are often found in
decaying plant materials and sometimes are even
occasionally predacious on other larvae.
Conclusion
Knowledge of the tephritid spectrum in any given
area serves as an important prerequisite for the
development of the sustainable IPM programme to
alleviate the pest problem. This study revealed ten
different species of tephritid flies from both rearing
of infested incubated fruits and trapping, belonging
to four important genera in the Citrus Museum
orchard at the University of Ghana’s ARC, Kade, in
the Eastern Region of Ghana. However, of the ten
different tephritid species recorded, only three
species (C. ditissima, B. invadens and C. anonae)
were identified to be the actual culprits attacking
citrus since they were all reared from the six
incubated citrus varieties sampled. It also showed
that monthly fluctuation of the mean population
density of tephritid flies increased when most fruits
in the Citrus Museum were ripening or ripe and
decreased when most fruits in the Citrus Museum
were harvested or maturing. The high numbers of C.
ditissima and B. invadens collected (which are known
to be the dominant species in citrus and mango,
respectively) suggest that these fruit flies might be
competing for citrus as a preferred host. The co-
habitation of fly species in all six citrus varieties
sampled is an indication of the possible competitive
ability of the invasive fly in those varieties. The
findings of this study may be useful to start building
a reliable catalogue of host records for the country,
especially those of the invasive species, B. invadens.
This may serve as an important bargaining tool in
the import/export trade to trading partners who
assume all produce from every country is attacked
by all the fruit flies. It is possible that C. ditissima,
which is the most abundant species in citrus, may
have previously been misidentified as C. capitata
since the latter was not recorded from fruits of the
six incubated citrus varieties sampled during the
study.
Acknowledgements
The authors wish to thank all the Research Officers
and technical staff at the University of Ghana’s ARC
at Kade for the excellent support and encourage-
ment given to them. The German Academic
Exchange Service (DAAD) provided financial sup-
port through the African Regional Postgraduate
Programme in Insect Science, University of Ghana.
The University of Ghana Research and Conferences
Committee also supported the study through the
Project ‘Development of sustainable and integrated
management strategy against fruit flies for fruit
safety and environmental protection in citrus
plantations in Ghana’. This work forms part of the
MPhil thesis of the first author.
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