Aspects of the ecology of fruit flies in uganda

Diversity, Host Utilization and Ecological Niche
of Fruit Flies (Diptera: Tephritidae) in Uganda
ISABIRYE BRIAN ERIPHAZ, Ph.D
brianisabirye@yahoo.com

Background…
Agriculture…Global and Uganda
Employs 45% of the working
global population and over 80%
in most parts of Africa and Asia!
Uganda
•Export: 90%
•Employment: 80%
•People living in rural areas : 85%
•Source of raw materials……. 3

Lucrative Horticulture Industry…..
4

Trade: Dynamic and highly vibrant!
Center on Globalization, Governance & Competitiveness, Duke University, 2011
5

Key Players in the fruit trade
6
• Global import of fruits hit US$4.3 million tons in the year 2010. In
which 87% or 3.8 million tons were imported by developed
countries.
• The US and the EU market represents 70% of global import of
tropical fruits.
• The EU is the largest tropical fruit importer with the major consumer
of France and the main transshipment port of the Netherlands.
• The US and Japan, Canada and Hong Kong are also large importers
(USDA, 2007).

Fruit industry in Uganda….the positive side!
7

Bad news for most fruit producers!
0
1000000
2000000
3000000
4000000
5000000
6000000
0
1000
2000
3000
4000
5000
6000
7000
8000
9000
Y2003 Y2004 Y2005 Y2006 Y2007 Y2008 Y2009 Y2010
(Source: UNEPB)
Value(US$)
Volume(Tonnes)
Period (Years)
Volume (Tonnes) Value (US$)
8

Common Challenge: Tephritid FF
Life Cycle
9

Negatively affect fruit trade
10

Problem/ Motivation…
• Fruit flies cause about 40% fruit loss in Africa, and about 73% in Uganda
• Design of IPM strategies for fruit flies requires knowledge of their
biology.
• Was limited to Nakasinga, 2002; Nemeye, 2005; Okullokwany, 2006.
• It is not clear how:
• Diversity has been shaped by hosts, distribution and envital
variability.
• Highly cryptic and inter-intra-specific morphological variation (Clarke
et al., 2005; Drew et al., 2008) among Bactrocera spp. turns out.
• Will change in climate alter the suitability and distribution of species?
11

Objectives and Hypothesises
Main Objective
To describe the diversity, host utilization and ecological niche of major tephritid fruit flies in
Uganda.
Specific Objective
1. Determine the species diversity of fruit flies across selected agro ecological zones
2. Assess fruit fly host utilization in the different agro ecological zones.
3. Characterise the morphometric variability of the most important fruit fly species
among hosts and mango growing zones
4. Determine the current and potential future spatial distribution of the major Tephritid
fruit fly species in Uganda.
Hypotheses
1. There is no significant difference in the diversity of fruit flies in the different ecological
zones in Uganda.
2. There is no significant difference in fruit fly host utilisation patterns in the different
ecological zones and among host types in Uganda.
3. There is no significant morphometric heterogeneity among B. invadens populations
infesting different hosts in the different ecological zones in Uganda.
4. Fruit fly species’ current and future distribution and ecological niches is random across
the different ecological zones in Uganda 12

Study IV: Morphometric (intra species) Diversity
Diversity, Host Utilisation and Ecological Niche of Tephritid (Diptera: Tephritidae) Fruit flies in Uganda
Ecological Nichie and Distribution Studies
Fruit Fly Diversity Studies
Study I: Species Diversity
Study III: Effect of Host Type and Variety on Fitness/ SurvivalStudy II: Fruit fly Host Utilisation in Uganda
Study VI: Projected Effect of Climate Change on
Distribution
Study V: Actual and potential Distribution of Fruit Flies in Uganda
Host Utilisation Studies
Results scheme and flow…
13

STUDY ONE: INTER SPECIES DIVERSITY
14
“When you have seen one ant, one bird, one tree, you have not seen them all” E. O. Wilson

Introduction
• FF are key pests of several fruit crops (Ekesi et al., 2006; Mayamba et al., 2015)
• Yield losses can exceed 80% (Ekesi et al., 2006; Mayamba et al., 2014)
• Correct identification is key in sustainable management (Jang et al., 2003)
• Regional efforts (Mwatawala et al., 2006; 2009; Rwomushana et al., 2008;
Geurts et al., 2012), but in Uganda (Nakasinga, 2002, Okullokwany, 2006)
• This study set out to:
1. Identify the fruit fly species present in the country, and
2. Assess the fruit fly community structure across three mango production
AEZs
15

Mat. and Methods
Western Medium High Altitude
Farmlands (WMHF), Lake Victoria
Crescent (LVC) and Northern Moist
Farmlands (NMF) (Wortman and Eledu,
1993)
%[
%[%[
%[
%[%[
%[%[
%[
%[
%[
%[
%[
%[
%[
%[ %[
%[
LIRA
APAC
GULU
OYA M
KASE SE
AMURU
RA KAI
SORO T I
W AKISO
MUKO NO
PADER
MIT YANA
KABA ROLE
MPIG I
MASA KA
IG ANG A
AGA GO
MAYUG E
IBA NDA
BUSIA
RUK UNGIRI
DO KO LO
RUB IRIZI
KIB ING O
TO RORO
AMO LOT AR
LA MW O
KAMULI
KIRYA NDONG O
NW O YA
NT UNG AMO
BUNDIBUG YO
KALUNGU
KIYUNG A
KAYUNG A
KABA LE
AMURIA
MBARARA
KIB OG A
BUDAKA
MASINDI
200 0 200 400 K
N
L
D
L
N
W
M
%[ M
%[
KEY
Agro
• Trapping with baited traps
• Methyl eugenol
• Trimedlure
• Torula yeast
• Cuelure
• Terpenyl Acetate
16
Collecting mango fruits and other fruits
and incubate them to assess fruit fly
infestation.

Results 1
Fruit fly community composition
5 10 15 20
0246810
sites
speciesrichness
LVC
LVC
NMF
NMF
WMHF
WMHF
LVC
NMF
WMHF
2 4 6 8 10
1e+011e+021e+031e+041e+05
species rank
abundance
LVCNMFWMHF
LVC
NMF
WMHF
0 0.25 0.5 1 2 4 8 Inf
0.00.51.01.52.0
alpha
H-alpha
LVC
LVC
NMF
NMF
WMHF
WMHF
LVC
NMF
WMHF
0
20,000
40,000
60,000
80,000
100,000
120,000
140,000 119,245
152 339 75 66 5 10 312 956 478
122,112
3 401 3 62 0 0 32 2 1
122,982
4 272 2 69 12 0 8 485 244
LVC NMF WMHF
17

Results 2
Fruit fly community structure
100
22
43 2243 85
22
64
85
0.55
0.6
0.65
0.7
0.75
0.8
0.85
0.9
0.95
Similarity
T.coffeae_
C.cosyra_
B.curcubitae_
C.rosa_
D.bivitattus
D.ciliatus_
C.fasciventris_
C.capitata_
B.invandens_
C.anonae
18
LVC
NMFWMHF
-2
2
-6 5
B.invandens
C.Anonae
C.cosyra
C.capitata
C. fasciventris
C. rosa
T.coffeae
B.curcubitae
D.bivitattusD.ciliatus
-1
1
-1 1
P < 0.000

Results 3 Displacement by B. invadens
0 1 2 3 4 5 6 7 8 9
Rank
-0.8
0
0.8
1.6
2.4
3.2
4
4.8
5.6
logAbundance
0 1 2 3 4 5 6 7 8 9 10
Rank
0
0.6
1.2
1.8
2.4
3
3.6
4.2
4.8
5.4
6
logAbundance
0 1 2 3 4 5 6 7 8
Rank
-0.8
0
0.8
1.6
2.4
3.2
4
4.8
5.6
logAbundance
Conclusion
1. At least 10 species in the country but B. invadens is the most widely distributed.
1. Significant diff in richness and abundance of fruit flies but not in evenness and
diversity of fruit flies across zones.
1. Differences across zones may be in turn attributed to the inherent environmental and19

Distribution
20

Introduction
• Fruit industry provides livelihoods World-wide (Lux et al., 2003; Ekesi and Billah,
2006).
• FF cause variable losses (Lux et al., 2003; Vayssie`res et al., 2005).
• Limited host status knowledge in Uganda, save for regional studies (De Meyer et
al., 2002; Copeland et al., 2002; Rwomushana et al., 2008).
• Makes design of mgt options hard (Mwatawala et al., 2009a).
• This study:
– To profile the host range of the main fruit fly pests in the three main mango
agro ecological zones; and
– Determine the susceptibility of selected fruits and mango varieties grown to
the various fruit fly pests in the country
STUDY TWO: HOST USE
22

Materials and Methods
Three major mango AEZs: WMHF, LVC and NMF (Wortman and Eledu, 1993)
STUDY TWO: HOST USE
1. Intensive collection of commercial and non-commercial fruit hosts.
1. Selected important fruits and mango cultivars in each zone at random sites.
1. Fruits included sweet orange, tropical almonds, avocado, guava and mango.
1. The mango cultivars: Apple Mango, Biire, Boribo, Dodo, Glen, Kagogwa, Kate, Keitt,
Kent, Tommy Akinson, Palvin and Zillatte.
1. The 12 cultivars were classified according to their maturity seasonality into early,
mid and late maturing cultivars (Ambele et al., 2012).
1. Fruits were transported to the rearing unit at the NARL (Copeland et al. 2002).23

Results 1
Fruit fly Host Range
• 38 fruit species, from 30 genera in 18 plant families were sampled.
• Among these, 633 (35.0%) samples were positive for fruit fly infestation.
• B. invadens was the dominant species: recorded in 29 out of the 38 plant species, while out of the 633 positive samples, 483
(76.3%) were due to B. invadens.
• Host infestation incidence for the rest of the fruit fly species was low
STUDY TWO: HOST USE
6 9
9
9 8
5 4
3 2
6 5 4 4 3 2 1 1 1
0
2
4
6
8
10
12
14
16
Annonaceae
Solanaceae
Rutaceae
Anacardiaceae
Myrtaceae
Cucurbitaceae
Moraceae
Sapotaceae
Rosaceae
Lauraceae
Rubiaceae
Caricaceae
Combretacaea
Sterculiaceae
Vitaceae
Euphorbiaceae
Musaceae
Verbenaceae
SpeciesRichness
Plant Richness Fruit Fly Richness
24

STUDY TWO: HOST USE
25
…………………………………………………… ……………………………… ……………… ………………. ……………
…………………………………………………… ……………………………… ……………… ………………. ……………

Results 2: Species Associations
STUDY TWO: HOST USE
Annacardium_occidentale
Mangifera_indica_
Sclerocarya_birrea
Annona_cherimola
Annona_muricata
Annona_reticulata
Annona_senegalensis
Annona_squamosa
Cananga_odorata
Carica_papaya
Terminalia_catappa
Momordica_charantia
Cucumis_melo_Cucurbita_spp.
Drypetes__natalensis
Persea_americana_
Antiaris_toxicaria_
Artocarpus_sp._
Ficus_sp._
Musa_sp.
Acca_sellowiana
Eugenia_uniflora
Psidium_guanjava
Cydonia_oblonga
Prunus_Spp._
Coffeae_arabica
Citrus_limon
Citrus_reticulata
Citrus_sinensis
Citrus_Spp._
Chrysophyllum_albidum
Manilkara_zapota_
Capsicum_annum
Lycopersicon_esculentum
Solanum_Spp._
Theobroma_cacao_
Vitex_sp._
Vitis_vinifera
Bactrocera_cucurbitae
Bactrocera_invadens
Ceratitis_anonae_Ceratitis_capitata
Ceratitis_cosyra
Ceratitis_fasciventris_
Ceratitis_punctata_
Ceratitis_rosa
Dacus_bivittatus_
Dacus_cilliatus
Trirhithrum_coffeae_
-300 -240 -180 -120 -60 60 120 180 240 300 360
Axis 2 (38.2%)
-300
-250
-200
-150
-100
-50
50
100
150
200
250
300
350
Axis3(20.8%)
26
First time infestation of B. invadens on T. catappa, A. toxicaria, E. uniflora, A. selllowiana, Musa
spp. and C. Arabica, T. cacao and C. oblonga in Uganda.

Results 3
STUDY TWO: HOST USE
0.0
20.0
40.0
60.0
80.0
100.0
120.0
Combretacaea
Anacardiaceae
Myrtaceae
Annonaceae
Moraceae
Cucurbitaceae
Sterculiaceae
Solanaceae
Lauraceae
Rosaceae
Caricaceae
Vitaceae
Sapotaceae
Rubiaceae
Musaceae
Euphorbiaceae
Rutaceae
Verbenaceae
MeanPositivity(%)
Plant Families
0
10
20
30
40
50
60
70
80
90
100
0.0
10.0
20.0
30.0
40.0
50.0
60.0
70.0
80.0
90.0
Terminaliacatappa
Psidiumguanjava
Mangiferaindica
Perseaamericana
Citruslimon
Citrussinensis
Citrusreticulata
B.invadens(%)
Positivity(%)
Fruit Species
B. invadens (%) Overall Positivity (%)
27

Results 4: Mango Fruit Host Utilization
STUDY TWO: HOST USE
0
5
10
15
20
25
30
35
40
45
50
0
20
40
60
80
100
120
Keitt
Kate
Biire
Glen
Zillette
Boribo
Kagogwa
Apple
Dodo
Palvin
Kent
Tommy
Positivity(%)
Infestation(Larvae/Kg)
Mean/ Kg Positive (%)ALL ZONES
0
10
20
30
40
50
60
0
10
20
30
40
50
60
70
Keit
Tommy
Kagogwa
Biire
Dodo
Kent
Boribo
Palvin
Apple
Kate
Glen
Zillette
Positivity(%)
Mean Positive (%)WMHF
0
5
10
15
20
25
30
35
40
45
50
0
20
40
60
80
100
120
140
Kate
Kagogwa
Biire
Tommy
Apple
Keitt
Boribo
Palvin
Zillatte
Glen
Dodo
Kent
Positivity(%)
Infestation(Larvea/Kg)
Mean/ Kg Positive (%)LVC
0.0
50.0
100.0
150.0
200.0
250.0
300.0
0.0
10.0
20.0
30.0
40.0
50.0
60.0
70.0
80.0
Zillette
Biire
Kagogwa
Apple
Dodo
Kent
Glen
Tommy
Kate
Boribo
Palvin
Keitt
Positivity(%)
Mean/Kg Positive (%)NMF
28

Results 5: Stages of the fruiting season
Early and late season
maturing mango varieties
were more susceptible.
STUDY TWO: HOST USE
Conclusion
• Fruit Flies have a diverse range of commercial and noncommercial or wild hosts in Uganda.
• Tropical almonds and B. invadens were the most suitable host and dominant fruit fly species,
respectively. Guava, Mangoes, Avocadoes and Citrus were also favorable hosts.
• Mango varieties varied in their susceptibility to fruit fly infestation within and across zones.
• New fruit ﬂy-host associations were probably due to the adaptive evolution or new records
29

STUDY THREE: PP HYPOTHESIS
30
Does mother know best?

Introduction
• Preference of oviposition vs offspring performance (P-P) is of interest (Bonebrake
et al., 2010; Heard, 2012).
• P–P hypothesis: females evolve oviposition behaviors that maximize offspring
growth and survival (Thompson, 1988).
• Positive P-P (Rossi and Strong, 1991; Hanks et al., 1993), and negative (Karban and
Courtney, 1987; Horner and Abrahamson, 1992) correlations have been recorded.
• Due to the polyphagous nature of B. invadens it was important to assess its relative
P-P in the various hosts and mango varieties.
• Hypothesis: Because of its polyphagous nature, B. invadens can obscure the P-P.
31

• Lake Victoria Crescent (Wortman and Eledu, 1993)
• Five host plants: sweet orange, tropical almonds, avocado, guava and
mango.
• Fruits naturally infested by B. invadens were incubated to determined fruit
host preference for oviposition (Aluja et al., 2009).
• Pupae handled as by Copeland et al. (2002), adults as by White & Elson-
Harris (1992).
• The adults were sexed and separately weighed.
• Developmental time of development stages was measured as time (days) for
each pupae to develop into teneral adult stage. 32

Results 1
Fruit host preference for oviposition differed significantly
0.0
10.0
20.0
30.0
40.0
50.0
60.0
70.0
80.0
90.0
Mango Varieties
0
5
10
15
20
25
30
Tropicalalmonds
Guava
Mango
Citrus
Avocado
Numberoflarvae/Fruit
Fruit Species 33

Results 2
Pupal development too varied significantly 1
0
50
100
150
200
250
12 14 16 18 20 22 24 26 28 30 32 34 36
AdultEmergence
Cumulative Days
TA Citrus Guava Avocado Mango
0.00
2.00
4.00
6.00
8.00
10.00
12.00
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
AdultEmergence
Cumulative Days*
Apple Biire Dodo Glen Kagogwa Kate
Keitt Kent Palvin Tommy Zillatte
34

Results 2
Pupal development too varied significantly 2
35

Results 3
Adult survival rates varied1
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
0 10 20 30 40 50 60
Survivaldistributionfunction(%)
Longevity (Days)
Tropical Guava Citrus Avocado Mango
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
0 5 10 15 20 25 30 35 40 45 50
Survivaldistributionfunction(%)
Longevity (Days)
Apple Biire Dodo Glen Kagogwa Kate
Keitt Kent Palvin Tommy Zillate
36

Results 3
Adult survival rates varied2
37

Results 4
Adult weight and sex ratio were significantly higher for TA and least in citrus
38

Results 5
P-P was consistent among species but less for cultivars
B. invadens choice of fruit species for female oviposition is guided by preference performance hypothesis.
However, among varieties of the same species (for instance mangoes), females tend to maximize their
fitness and not necessarily that of offsprings as proposed by the optimal foraging hypothesis!
39

Distribution
40

STUDY FOUR: INTRASPECIES DIVERSITY
41
“The millions of species now inhabiting this planet have, evolved from a common ancestor, and the
multiplication in the number of species has been generated as single species have split into two.” Darwin

B. Papayae
Oriental fruit fly
Introduction
Identity of B. dorsalis complex (>70) is difficult, even with molecular tools (Clarke et al.,
2005; Drew et al., 2008).
B. Philippinensis
B. Carambolae
B. Invadens
B. dorsalis/B. papayae/B. philippinensis
B. carambolae
B. opiliae
B. cacuminata
B. musae
B. occipitalis
42

Introduction 2
• Variations may lead to biotypes, host or pheromone races with
variable responses to management (Menken et al., 1996).
• Has site and host specific phynotypic variations taken course
among B. invadens populations in Uganda?
• This study:
– Assess the morphometric variations among three geographic
and hosts B. invadens populations in Uganda.
– Examine fluctuating asymmetry (FA, small random
departures from perfect symmetry among individuals).
43

• WMHF, LVC and NMF (Wortman and Eledu, 1993).
• Terminalia catappa, Psidium guanjava and M. indica.
• Both wings were slide mounted using Canada Balsam.
Once dry, photos were taken using a sony camera
• Euclidean distance matrix analysis and variance
structure coordinate system geometric techniques.
• Size and shape were analyzed throughout 15
landmarks for 360 specimens after symmetrization.
44

Results 1
Host type significantly affected wing size/ shape 1
Almond Guava Mango0.9995
0.9996
0.9997
0.9998
0.9999
1
1.0001
1.0002
1.0003
Size
-4 -3 -2 -1 1 2 3 4
Axis 1
-2.4
-1.6
-0.8
0.8
1.6
2.4
3.2
4
Axis2
(Blue: Mango; Pink: Tropical almonds; Red: Guava).
45

Results 1
Host type significantly affected intraspecific shape variation 2
2
46

Results 2
Geographical Variations in Wing Size/ Shape 1
WMHF NMF LVC
0.9994
0.9995
0.9996
0.9997
0.9998
0.9999
1
1.0001
1.0002
1.0003
Size
-4 -3.2 -2.4 -1.6 -0.8 0.8 1.6 2.4 3.2
Axis 1
-5
-4
-3
-2
-1
1
2
3
Axis2
(Blue: WMHF; Pink: NMF; Red: LVC).
47

Results 2
Intraspecific Geographical Variations in Wing Shape 2
48

Results 3
FA in Zonal and Host B. invadens Populations
Forms of bilateral asymmetry: Fluctuating
asymmetry (Mango), Antisymmetry (NMF) and
Directional asymmetry (WMHF).
Conclusion
B. invadens can exhibit wide
phenotypic variations under
different envi’tal and host conditions
49

Ecological Niche and Distribution Studies
Distribution
50

STUDY FIVE: POTENTIAL DISTRIBUTION
51
“There is no part of natural history more interesting or instructive, than the study of
the geographical distribution of animals.” Alfred Russell Wallace (1823-1913)

Introduction
• Spatial suitability good in the design explicit management strategies for the pest.
• ENM provides an option for potential species distribution.
• ENM allows obtaining range of conditions for species survival/ reproduction
(Pearson, 2007; Rubio and Acosta, 2010).
• Prediction model is a function of species response to the environmental variables,
hence fundamental niche (Austin, 2007).
• This study:
– Determine the geographical regions that are ecologically suitable for fruit fly establishment.
– Explore the climatic profiles underpinning the selected species distribution, to understand their
niche requirements
52

Materials and Methods 1
• Ten species: B.invandens, C.anonae, C.cosyra, C.capitata, C.fasciventris, C.rosa,
T.coffeae, B.curcubitae, D.bivitattus and D.ciliatus.
• Nineteen (19) environmental variables at 30 arc-seconds (~1 km²) partial resolution
were derived from the WorldClim project (Hijmans et al. 2005).
• Models by Maxent and Bioclim (Graham and Hijmans, 2006; Phillips et al., 2006).
• Model evaluation: 75% of the original presence data (training sample), while 25%
was test data (Pearson, 2007; Acosta, 2008; Echarri et al., 2009).
• Accuracy of the model was evaluated by calculating the AUC in a receiver operating
characteristic plot
53

Current range prediction
Geographic Space Ecological Space
occurrence points on current distribution
ecological niche modeling
Projection back onto geography
Future range prediction
temperature
Model of niche in ecological
dimensions
precipitation
Current
Correlative Vs Mechanistic Models
Distri. a good indicator
of ecological needs Detailed physiological data

Defining Niches
( )j
ir e
( ; )j j j
i ix R
( ; )j
x T
Grinnell,
scenopoetic
Elton, bionomic
Movements
G
BAM Diagram
B
M
A
1
( ) ( ; ) ( ; )
j
j j j j ji
i i ij
i
dx
r e x x
x dt
   R T
Fundamental niche
Intrinsic Growth Rate
(Scenopoetic)
Resource-consumer
dynamics, competitors,
predator-prey (bionomic).
Migration
colonization, history
• Physiological tolerances,
migration limitations and
evolutionary forces that limit
adaptation
• A starting point for abiotic
factors is often climate.
Climate variables often also
correlate with other variables
Environmental Gradient
(Hawkins et al., 2003)
55

Results 1
Records of Fruit Flies and Potential Distribution 1
56
Species are diverse and widely distributed!

Results 1
Bioclimatic profiles of fruit fly species
57

Results 2: Potential Distribution
I (D. punctatifrons), II (T. coffeae), III
(C. fasciventris), IV (B. cucurbitae),
V (D. cilliatus), VI (C. cosyra), VII (C.
capitata), VIII (D. bivittatus), IX (C.
anonae), X (B.invadens) & XI (ALL).
58

Results 2: Limiting Factors
59

STUDY FIVE: POTENTIAL DISTRIBUTION: Limiting Factors for selected species

Results 2: Limiting Factors
61

Results 3
Conclusion
• Fruit flies pose a signiﬁcant threat to the country; countrywide
potential distribution of native and exotic species was demonstrated.
• Precipitation and temperature significantly determined distribution.
• Central & mid north zones were most suitable habitats, while the
western, north eastern & areas around Albert Nile were marginal.
62

STUDY SIX: CLIMATE INDUCED RANGE SHIFTS
Projections of Climate-Induced Future Range Shifts among
Fruit Fly Species in Uganda.
Charles Masembe, Brian E. Isabirye, I. Rwomushana, A. M. Akol, Caroline K. Nankinga
Journal of Plant Protection Science
“Led by a new paradigm, scientists adopt new instruments and look in new places...”
Thomas S. Kuhn (1922-1996)

Introduction
• Knowledge on geographical suitability of the pest is needed in the design of
spatially and temporally explicit management strategies for pests.
• Global climate continues to change (IPCC, 2007).
• For agriculture, climate change will be significant, as such changes are associated
with shifts in pest and disease ranges, posing new risks (Cooper et al., 2013).
• Considerable effort has gone into predicting the effect of future climate scenarios
(Walther et al., 2002; Chambers et al., 2005, Shi et al., 2006; McKenney et al.,
2007).
• This study:
 How fruit fly local-level distribution patterns may be expected to change under
future climate change and the comparative potential range shifts among
species.
64

• Species assessed were: Bactocera invandens, Ceratitis anonae, Ceratitis cosyra, Ceratitis capitata,
Ceratitis fasciventris, Dacus punctatifrons, Trirhithrum coffeae, Bactrocera curcubitae, Dacus bivitattus,
and Dacus ciliatus.
• Annual mean temperature and mean temperature of wettest quarter were chosen, while moisture
gradients were represented by mean annual precipitation and precipitation of coldest quarter.
• Climatic controls on current fruit fly distributions were summarized using the climate envelope (CE)
approach (Nix, 1986).
• From the extent of the current CE for each fruit fly species, Future climate variables were generated by
two GCMs: HADCM and CCCMA under emission scenarios A2 and B2.
• In the full-dispersal scenario, changes in CE area were calculated by expressing the future CE area as a
percentage of the current CE area.
• For the no-dispersal scenario, future maps were overlaid on current maps and only the area of overlap
was taken as the future distribution.
• Predicted current and future local species richness and turn over of each of the regions were
estimated
65

Results 1
Effect of dispersal on future climate envelope size and location
Climate change resilience varied significantly, but Dacus ciliatus > Bactrocera invadens >
Ceratitis cosyra pose a serious management challenge as their future habitats are predicted to
increase!
66

Results 2
Range Shift: Increase
Baseline: 1950-2000 Future: 2000-2050
D. ciliatus
B. invadens
C. cosyra
67

Results 2
Range Shift: Decrease
Baseline: 1950-2000 Future: 2000-2050
D. bivittatus
B. cucurbitae
C. anonae 68

Results 3
CO2 emission scenarios and species habitat size
-150
-100
-50
0
50
100
150
200
250
300
Scenario-A2 Scenario-B2
Change(%)
Carbon dioxide Scenarios
Species-B.cu Species-BI
Species-C.ano Species-C.ca
Species-C.co Species-C.fa
Species-D.bi Species-D.ci
Species-D.pu Species-T.co
Proportional changes
in habitat size of
predictions under
the two carbon
dioxide emission
scenarios for the 10
fruit fly species and
box plots for carbon
dioxide scenarios
from a 1950-2000
baseline to the 2050
future period. 69

Results 4
Predicted species richness and turnover under the four models and two dispersal
scenarios in the three main mango-growing regions.
70

Results 5
Conclusion
• Most species are vulnerable and will likely be unable to keep pace with
climate change, with habitat losses averaging 25.4% by 2050 future period.
• Fruit fly climate change resilience varied: Dacus ciliatus > Bactrocera
invadens > Ceratitis cosyra > Trirhithrum coffeae > Ceratitis capitata >
Ceratitis fasciventris > Dacus punctatifrons > Ceratitis anonae > Bactrocera
cucurbitae > Dacus bivittatus.
• Dacus ciliatus > Bactrocera invadens > Ceratitis cosyra pose a serious
management challenge as range will likely increase
• Future ranges are predicted to shift northwards, mainly to the Northern
Moist Farmlands.
71

GENERAL CONCLUSIONS, DISCUSSIONS AND RECOMMENDATIONS I
At least ten tephritid fruit fly species; but B. invadens is the most
abundant, and was observed to be displacing the other fruit fly fauna
 Difference in zonal faunal composition can be attributed to their (zones)
inherent differences in envital conditions, hosts and farming systems.
 NMFs recorded lesser alternative hosts for fruit flies, which was converse to
the LVC and the WMHF, hence differences in composition
 Dominance of B. invadens can be attributed to competition efficiency (Ekesi et
al., 2009), and reproduction and resource distribution (Kiesecker et al., 2001).
 The LVC offers opportunities for resource distribution, which avoids clumping,
converse to the NMFs, which might also explain the difference in displacement
pressures between the two zones.
72

GENERAL CONCLUSIONS, DISCUSSIONS AND RECOMMENDATIONS II
A wide range of hosts was recorded, albeit with signiﬁcant variability in
preference and infestation levels among types, varieties and zones.
Fruits have speciﬁc adaptations in their ecological requirements, which
ultimately determine their (fruit) susceptibility in their respective
environments.
Preference of the flies for the local selection and Kagogwa varieties may be
attributed to an increase in performance on these varieties or due to
experience or learning (Szentesi and Jermy 1990; Dukas and Bernays, 2000).

GENERAL CONCLUSIONS, DISCUSSIONS AND RECOMMENDATIONS III
B. invadens does undergo rapid phenotypic variability which can lead to
biotypes, host races, etc…
May lead different populations to adapt and survive in difficult conditions such
as the stress caused by control practices and subsequently cause resistance
among populations.
The recorded fine-scale intraspecific population phenotypic variations may
simply be evidence of phenotypic divergences rather than interspecific
differences (Schutze et al., 2012).
Such differences may be irresolvable using techniques such as molecular
analysis, hence the current lack of molecular markers to discriminate between
these eco- and host types.
74

GENERAL CONCLUSIONS, DISCUSSIONS AND RECOMMENDATIONS IV
The most suitable niches encompass areas around Central and mid north
zones, while the western, northeastern and areas around Albert Nile were
characterized as marginal.
Current and future niches offer the optimum bioclimatic tolerance limits.
Current and future potential distributions of fruit flies will be determined not
only by climate but also dispersal ability, biotic interactions, genetic adaptation,
and abiotic factors.
The Ethiopian fruit fly (D. ciliatus), B. invadens and D. ciliatus should be of great
concern as range is predicted to increase.
75

GENERAL CONCLUSIONS, DISCUSSIONS AND RECOMMENDATIONS III
The ecology of fruit flies needs to be further explored to understand
how community composition evolves in the other landscapes and mgt
options.
Habitat suitability maps for these species could be improved by
inclusion of edaphic and host plant data.
Further studies on biology of fruit flies in the different edapho-
climatic conditions of Uganda are recommended
Achievement of optimum management of fruit flies across farming
landscapes is possible, with IPM and area-wide mgt (Ekesi and Billah,
2006; Dyck, Hendrichs and Robinson, 2005). 76

Publications I
77
Refereed Journal Papers
1. Isabirye BE, Masembe C, Akol AM, Muyinza H, Rwomushana I, Nankinga CK (2015) Modeling the Potential
Geographical Distribution and Ecological Niche of Selected Fruit Fly (Diptera: Tephritidae) Species in Uganda, Journal
of Plant and Pest Science, 2 (1): 18-33
1. Alex Mayamba, Caroline Kukiriza Nankinga, Brian Isabirye, Anne Margaret Akol (2014). Seasonal Population
Fluctuations of Bactrocera invadens (Diptera: Tephritidae) in Relation to Mango Phenology in the Lake Victoria
Crescent, Uganda. Fruits, 2014, vol. 69, p. 473–480
1. B.E. Isabirye, A. M. Akol, H. Muyinza, C. Masembe and I. Rwomushana, C. K. Nankinga (2015). Fruit Fly (Diptera:
Tephritidae) Host Status and Relative Infestation of Selected Mango Cultivars in three Agro Ecological Zones in
Uganda. International Journal of Fruit Science. (In Press).
1. B.E. Isabirye, C. Masembe, C. K. Nankinga, A. M. Akol, 2013. Geometric Morphometrics of Geographic and Host-
Associated Population Variations of Bactrocera invadens in Uganda. American Journal of Agriculture and
Environment.
1. B.E. Isabirye, A. M. Akol, C. K. Nankinga, C. Masembe, I. Rwomushana (2015). Species Composition and Community
Structure of Fruit Flies (Diptera: Tephritidae) Across Major Mango-Growing Regions in Uganda. International journal
of Tropical Insect science, 1-12.
1. A. M. Akol, C. Masembe, B. E. Isabirye, C. N. Kukiriza, and I. Rwomushana (2014). Oviposition Preference and
Offspring Performance in Bactrocera invadens (Diptera: Tephritidae). International Research Journal of Horticulture.
IRJH 2014, 2(3): 36-44.
1. Brian E. Isabirye, Charles Masembe,, I. Rwomushana, Caroline K. Nankinga, A. M. Akol (Review). Projections of
Climate-Induced Future Range Shifts among Fruit Fly Species in Uganda. Journal of Plant Protection Science

Publications II
78
Extended Abstracts
1. Anne Akol, Brian Isabirye, Caroline Nankinga, Charles Masembe and Ivan Rwomushana, 2014. Species Composition and
Community Structure of Fruit Flies across Major Mango-Growing Regions in Uganda. 9th International Symposium on
Fruit Flies of Economic Importance (ISFFEI).
1. Anne Akol, Charles Masembe, Brian Isabirye, Caroline Nankinga and Ivan Rwomushana, 2014. Oviposition Preference
and Offspring Performance in Phytophagous Fruit Flies: The African invader, Bactrocera invadens. 9th International
Symposium on Fruit Flies of Economic Importance (ISFFEI).
1. Brian Isabirye, Charles Masembe, Caroline K. Nankinga, I. Rwomushana, Harriet Muyinza, Anne M. Akol, 2014.
Projections of Climate-Induced Future Range Shifts among Fruit Fly Species in Uganda. 9th International Symposium on
Fruit Flies of Economic Importance (ISFFEI).
1. Brian Isabirye, Charles Masembe, Caroline Nankinga, Harriet Muyinza and Anne Akol, 2014. Geometric Morphometrics
of Geographic and Host-Associated Population Variations of Bactrocera invadens in Uganda. 9th International
1. Caroline Nankinga, Brian Isabirye, Mayamba Alex, Harriet Muyinza, Winnifred Aool, Ivan Rwomushana, Philip
Stevenson and Anne Akol, 2014. Status of Fruit Fly Infestation of Mango and Other Fruits in Uganda. 9th International
1. B. E. Isabirye, C.K. Nankinga, H. Muyinza, C. Masembe and A.M.Akol, 2012. Effect of Three Host Species on Infestation
Levels, Offspring Survivorship, Sex Ratio and Body Weight of Bactrocera invadens (Diptera: Tephritidae). 2nd
International Symposium of TEAM.

All of us should be worried about fruit flies as serious
pests, because of their diversity; direct larval feeding on the host
fruit (economic loss); long list of host plants; flexibility in
developing
different life history strategies, including rapid adaptation to
new habitats; efficient habitat utilization; an ability to
rapidly develop host and geographic races (particularly true for
Bactocera species); and short generation time (rapid multiplication)
(Brian E. Isabirye, 2015)
Take Home ….

Supervisors:
Mwebale inhoo!!!
“Though the road's been rocky it sure feels good to me.”
― Bob Marley

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