International Journal of Tropical Insect Science

https://doi.org/10.1007/s42690-020-00152-5

ORIGINAL RESEARCH ARTICLE

Fine-scale infestation pattern of Bactrocera dorsalis

(Diptera: Tephritidae) in a mango orchard in Central Mozambique
Luis Bota 1 & Braine Fabião 1 & Marc De Meyer 2 & Lourenço Manuel 3 & Maulid Mwatawala 4 & Massimiliano Virgilio 2 &
Laura Canhanga 3 & Domingos Cugala 3

Received: 25 October 2019 / Accepted: 16 April 2020

# African Association of Insect Scientists 2020

Abstract
The production of mango in Mozambique is under threat due to fruit fly infestation, and most of the farmers cannot afford the cost
of control. Spatio-temporal dynamic of Bactrocera dorsalis was assessed at farm level in Manica Province to provide information
for better calibration of pest management strategies and thereby minimize the use of pesticides and other costs associated to pest
control. 64 Chempac Bucket traps baited with torula yeast were monitored weekly at a 10 ha mango orchard. From the species
captured on the traps only B. dorsalis were considered for the study due to its importance on mango. A universal spatio-temporal
kriging model was fitted to investigate the spatio-temporal pattern of the fly. Results of the analysis showed high spatial
heterogeneity of the fly over time, with the occurrence spreading from the margins of the mango orchard and infesting the whole
orchard during the period of peak of abundances reaching densities of more than 500 fly per trap per week. These results shows
that the flies that infest this particular orchard may come from the marginal area, especially from local varieties which get matured
earlier. The findings of this study provides information to be taken into consideration by farmers about when and where apply the
control measures.

Keywords Spatio-temporal . B. dorsalis . Kriging interpolation . Hotspot . Mango orchard

Introduction fruit flies including Bactrocera dorsalis Hendel is the most

important factor hampering the production of the crop in
Mango (Mangifera indica L.) is considered an important crop Africa in general and Mozambique in particular (Ekesi et al.
in sub-Saharan Africa as a source of income for both rural 2009; Mwatawala et al. 2006; Cugala 2011). Yield losses due
population and commercial farmers contributing to the reduc- to fruit fly infestation are reported to be more than 40% with-
tion of poverty, as well as providing nutritional supplements out control (Ekesi et al. 2016). Some of the control measures
(Vayssières et al. 2008). In Mozambique, mango is the fruit for this group of pests includes male Anihilation techniques,
commodity with highest production after banana, largely by biological control, orchard sanitation, mass trapping and
small scale farmers (FAOSTAT 2015). The occurrence of baiting (Ekesi and Billah 2007). The costs of control can be
very high, exceeding about $7.5 Million per annum in South
Africa’s Western Cape (Barnes 2016) and about $6–10
* Luis Bota
luisbota@yahoo.com.br
Million per annum in Maghreb region (IAEA 1995). This
costs can be reduced or optimized if measures are applied
1
before the population reaches the economic threshold
National Fruit Fly Laboratory, Provincial Directorate of Agriculture (Kogan 1998). Insect population including fruit flies are spa-
and Food Security, Po Box 42, Chimoio, Manica Province,
Mozambique tially heterogeneous in their densities (Papadopoulos et al.
2 2003), and this heterogeneity together with temporal changes
Royal Museum for Central Africa, Invertebrates Section & JEMU,
Leuvensesteenweg 13, B-3080 Tervuren, Belgium constitute an important element in development of manage-
3 ment programs. Spatio-temporal patterns of organisms are
Faculty of Agronomy and Forest Engineering, Eduardo Mondlane
University, Maputo, Moçambique driven by the natural environmental heterogeneity
4 (Kounatidis et al. 2008) and by intrinsic factors of the species
Department of Crop Science and Horticulture, Sokoine University of
Agriculture, Morogoro, Tanzania such as developmental rate, species behavior or resource use

pattern (Fievet et al. 2007). Fruit flies are known to be good
fliers (Kounatidis et al. 2008) and understanding the pattern of
their spatial distribution over time and related factors is of
great importance for better site-management (Castrignanò
et al. 2012). Methods for spacio-temporal analysis are grouped
into two: deterministic and geostatistic (Mello et al. 2003).
Currently, because of the development of several computer
software packages, geostatistic methods are much better
known among which kriging is the one commonly used
(Mello et al. 2003). Kriging is an estimating geostatic method
which takes into consideration the spatial characteristics of
autocorrelation of regionalized variables (Jakob 2002;
Assumpção et al. 2013). In the regionalized variables there
must be a certain spatial continuity, which allows the data
obtained by sampling of certain points to be used in order to
parameterize the estimation of points where the value of the
variable is unknown (Berveglieri et al. 2011; Yamamoto
2009). However, it may needs many years to fully characterize
the spatial and temporal variability of insect patterns and then
develop pest monitoring and management strategy
(Castrignanò et al. 2012). B. dorsalis is one of the economi-
cally most important fruit fly pests in the world due to its direct
Fig. 1 Map of location of Vandúzi district
Int J Trop Insect Sci
and indirect damages (Bo et al. 2014). Many population dy-
namic aspects of this fly have been studied during the last
decade, mainly in Africa (under its junior synonym
B. invadens) where it is causing huge damages. Most of these
studies analyses the temporal pattern of the fly’s population
(Vayssières et al. 2009, 2014, 2015; Mwatawala et al. 2006;
Mayamba et al. 2014) concluding that B. dorsalis is more
abundant during the raining season, a period that coincides
with the high abundance of its main hosts. Nevertheless, there
are no studies regarding its spatio-temporal dynamics and lit-
tle is known about its infestation dynamics within orchards in
Africa. This study aims at providing a first characterization of
the fine-scale infestation dynamics of B. dorsalis within a
mango orchard during one mango season in Mozambique.
Material and methods
Study area
Data were collected in a 10 ha mango (Mangifera indica L.)
orchard in Mozambique, Manica Province, Vanduzi District
Int J Trop Insect Sci
(−18.94o Latitude; 33.18o Longitude; 700 m) (Fig. 1). Two
varieties of mango are produced in the orchard, Tommy
(occupying more than 80%) and Keitt (less than 20%).
The orchard is bordered by permanent pastures, maize
(Zea mays L.), trees of local mango variety and guava
(Psidium guajava L.) (Fig. 2). The study area has a
tropical climate, with an annual average temperature of
21.2 °C, and annual rainfall of 1000 to 1020 mm. The
soils consist mainly of red oxides, are deep and well
drained, with a rolling topography (MAE 2005).
Trapping
Trapping was done following IAEA guidelines (IAEA
2013). Twenty-six plots were demarcated in the orchard
(13 in the outer sectors of the orchard and 13 in the inner
sectors). Each plot was composed of six labeled trees. Two
replicate traps were placed within each plot on different
trees (Fig. 2). In order to ensure the independence of repli-
cates at each sampling date, the two traps were randomly
shifted among the six trees. Three permanent traps were also
placed as a control on four external points around the or-
chard, making twelve in total. The permanent traps were
placed to assess the abundances of fruit flies outside the
orchard. In total 64 Chempac Bucket traps (©Insect
Science) were placed, baited with torula yeast (©Insect
Science) (250 ml per trap), diluted in water at the propor-
tion of 3 tablets per 1 l of water. The torula solution
was replaced weekly, after washing the traps. All used
torula yeast was removed from the orchard to avoid
contamination. The position of each trap was deter-
mined with a GPS Garmin etrex 30.
Fig. 2 Location of the plots/traps (Source: Google earth 2016)
The data were collected during the mango season 2014–
2015 (from September 2014 till February 2015).
Species identification
All fruit flies captured in the traps were preserved in 70%
ethanol, taken to the Fruit Fly Laboratory of Chimoio and
identified to genus and species level, using the electronic
key developed by Virgilio et al. (2014). After identification
to species level, only B. dorsalis was considered for analysis,
because of its significance and importance as mango pest
(Ekesi et al. 2009; Vayssières et al. 2015). Fruit fly abundance
was expressed according to FTW index (number of adult flies
per trap per week).
Data analysis
A universal spatio-temporal kriging model was fitted to inves-
tigate the spatio-temporal pattern of fruit fly. Let Z (s,t) denote
the density of fruit fly in trap s (defined by coordinates latitude
and longitude) at week t. The model assumes that the spatio-
temporal process of the prevalence of fruit fly is a stochastic
process defined by Eq. 1.
Z ðs; t Þ ¼ η þ εðs; t Þ ð1Þ
Where η is a constant mean and ε is the spatio - temporal
correlated stochastic component with zero mean and covari-
ance structure given by Σ(θ) (Heuvelink and Griffith 2010).
To estimate the spatio-temporal covariance structure of ε
(Σ(θ)), we assumed that the variance of ε is constant and that
the covariance between two positions (s, t) and (s + h, t + u)
only depends on the separation distance (h, u), where h is the
 Int J Trop Insect Sci

Euclidean spatial distance (metres) and u is the distance in
time (weeks). We assumed ε to be stationary and spatially
isotropic. The spatio-temporal covariances are usually de-
scribed using a spatio-temporal variogram (γ), which mea-
sures the spatio-temporal dependence between data separated
in the spatio-temporal domain using the distance vector (h, u)
defined as follows:
1 h
i2
γ ðh; uÞ ¼ E εðs; t Þ−ε s þ h; t þ u ð2Þ
2
Where γ (h,u) denotes the semivariance of ε and E denotes the
mathematical expectation. In this study, we use an inseparable
model called “Sum-metric” model. This assumes that the
spatio-temporal variogram consists of three stationary and in-
dependent components:
qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
γ ðh; uÞ ¼ γ s ðhÞ þ γ t ðuÞ þ γ joint h2 þ ðk:μÞ2
point where Z was not observed. The universal kriging in
the spatio-temporal domain is defined as:
^εðs0 ; t 0 Þ ¼ c0 T c−1 ε ð4Þ
Where c is the n × n variance-covariance matrix of the resid-
uals at the n observation space-time points, as derived from
the spatio-temporal variogram, c0 is a vector of covariances
between the residuals at the observation and prediction points,
T denotes matrix transpose, and ε is a vector of residuals at the
n observation points. The final prediction of density of fruit fly
Z at a point (s0, t0) is defined as follow:
Z^ ðs0 ; t 0 Þ ¼ η þ ^εðs0 ; t 0 Þ ð5Þ
All analysis were carried out using R software (R
Development Core Team 2011) package spacetime
(Pebesma 2012).
ð3Þ

Where γ s(h) and γt (u) are purely spatial and temporal

variograms respectively, γjoint(.) is a joint variogram and k is
a real coefficient. The Sum-metric model can be seen as a
surface with six parameters: two parameters for each
variogram (sill and range) and a joint spatio-temporal sill
and nugget. According to Hu et al. (2015) the parameters of
each variograms are used in spatio-temporal kriging to com-
pute the best linear unbiased predictor for any space-time
Results
The spatio-temporal distribution of the density of B. dorsalis
from 4th September 2014 up to 27th February 2015 is repre-
sented in Fig. 3. It shows that the prevalence of fruit fly varies
spatially and temporally during the period of the study. The
prevalence of fruit fly trends to increase from low prevalence

2014−09−04 2014−09−11 2014−09−18 2014−09−25 2014−10−02 2014−10−09 800

700

2014−10−16 2014−10−23 2014−10−30 2014−11−06 2014−11−13 2014−11−20

600

500
2014−11−27 2014−12−04 2014−12−11 2014−12−18 2014−12−26 2015−01−02

400

2015−01−09 2015−01−16 2015−01−23 2015−01−30 2015−02−06 2015−02−13 300

200

2015−02−20 2015−02−27
100

0
Fig. 3 Spatio-temporal distribution of fruit fly from September 2014 up to February 2015 in mango orchard
Int J Trop Insect Sci
Fig. 4 Spatio-Temporal sample variogram for prevalence of fruit fly
in September, October and November (less than 100 individ-
uals/trap/week) until high densities in December, January and
February (more than 100 individuals/trap/week).
Figures 4 and 5 show respectively the empirical spatio-
temporal variogram and the sum metric variogram for the
prevalence of the fruit fly in mango orchard during the period
of the study. The high variability at both spatial and temporal
dimension in both sample variogram and sum metric model
indicates that spatio-temporal correlation is present when
Fig. 5 Sum metric variogram model for prevalence of fruit fly in mango
orchard from September 2014 up to February 2015
analysing the density of fruit fly in mango orchard from
September 2014 up to February 2015.
Table 1 summarizes the parameters estimates of the Sum
metric variogram model. All variogram components were
modelled using exponential function. The results show that the
range of spatial dependency and temporal dependency is 1.4 km
and 93 days, respectively. This indicates that the prevalence of
fruit fly in mango orchard is spatially auto correlated up to a
distance of 1.4 km, which means that there is a similarity in the
occurrence of fruit for distance less than 1.4 km. If any region
into the mango orchard present high density of fruit fly, it is also
likely to observe high densities in distances less than 1.4 km. In
the other hand, the temporal auto correlation of 93 days indicates
that the prevalence of fruit fly has similarity over the time. Values
of fruit fly density trend to be similar or related for a period up to
93 days (3 months). In fact, this is observed over the first
3 months of the period of the study (September – November)
where the fruit fly density trends to be low (Fig. 3). High densi-
ties of fruit fly are verified from December to February (period of
3 months), although with highest densities in January.
Table 1 Parameters estimates for sum metric Variogram model
Components Parameters
Nugget Sill Range
Spatial 1135.95 1941.29 1461.86
Time 1.00 809.63 93.41
Space-time 1282.51 11,667.60 1685.63

Fig. 6 Spatio-temporal kriging using sum metric model for fruit fly in
mango orchard from September 2014 to February 2015
The spatio-temporal kriging in the mango orchard from
September 2014 to February 2015 is presented in Fig. 6.
The result showed that the density of fruit fly in mango or-
chard trends to be lower than 100 individuals per trap during
the first 12 weeks (from 04th September 2014 – 20th
November 2014). From the 13th week up to the 18th week
the fruit fly prevalence trends to increase from low values up
to 200 individuals per trap. High densities of fruit are observed
from the 19th week up to 22nd week with the highest densities
from 09th January to 23rd January. The occurrence of fruit fly
spreads from the border of the mango orchard and infests the
whole orchard during this period reaching densities more than
500 individuals per trap. After the 23rd week up to 26th week
the prevalence of fruit fly trends to decrease substantially.
Discussion
This study showed that B. dorsalis was present in the orchard,
with fluctuating abundances, across the entire sampling peri-
od. Densities of B. dorsalis were low from September to
November and high from December to February. As already
observed in other studies (Mwatawala et al. 2006) abundance
variations of B. dorsalis are related to the phenology of its host
plant. In this study area, the maturity of mango occurs from
late November to February. Similar results were reported by
Mayamba et al. (2014), where the peak periods of B. dorsalis
trap catches corresponded to the harvesting period when man-
go fruits were at physiological maturity to ripeness, while the
Int J Trop Insect Sci
lowest trap catches corresponded to periods of fruit set when
fruits were very small and immature.
The spatio-temporal diagrams from kriging interpola-
tion showed a highly variable distribution of B. dorsalis
within the orchard thus suggesting associated heterogene-
ity of biotic or abiotic factors throughout the orchard,
affecting the relative abundance of the fly. It is known
that agricultural systems are heterogeneous systems con-
taining different arrangements of soils, habitat, microcli-
mate, and plant communities and productivity (Sciarretta
and Trematerra 2014). These environmental variability
proved to be the key that drives the spatial and temporal
pattern of organisms (Kounatidis et al. 2008). Israely et al.
(2005), reported on a study conducted in Israel that the
spatial heterogeneity demonstrated in their spatio-
temporal analysis was affected by the phenology of dif-
ferent hosts within or outside the orchard, the difference
in the period of maturation, fruit host abundance and dis-
tance between them.
The dispersion pattern of B. dorsalis during the study
progressed from the borders throughout the entire orchard.
This may suggest that fruit flies move from the orchard to
the neighborhoods when ripe mangoes are not available with-
in the orchard and move back to the orchard when host is
present again. In the neighborhood of the orchard local varie-
ties of mango are present and their maturation occurs 1 month
before varieties of mango produced within the orchard. We
can speculate that B. dorsalis relies on external mango trees,
as a stepping-stone before moving to the orchard when fruits
are present. Majacunene (2014) reported in Manica Province
that alternative hosts serves as a refuge for fruit flies during
periods of no availability of fruits in the orchards, and later
became a source of infestation. Deguine et al. (2012) reported
that fruit flies spend more time outside the orchard roosting,
feeding and for protection against natural enemy, going to the
orchard only for oviposition activity. So far there is no record
of studies related to the spatio-temporal distribution of
B. dorsalis at such a fine scale. However, Balagawi et al.
(2014) reported that, at the beginning on the fruiting season,
the abundance of Bactrocera tryoni was higher at the edges of
a strawberry orchard and it was gradually increasing within
the orchard as the strawberry season progressed.
Papadopoulos et al. (2003) reported a spatio-temporal hetero-
geneity of the female population of C. capitata related to the
phenology of host trees and to sequential availability of ripe or
semi ripe fruits in the orchard. Alemany et al. (2006) reported
the existence of hotspots of high densities of C. capitata
around and outside citrus orchards, from where the
population dispersed throughout the orchard. Similarly,
Wahab et al. (2006) using kriging interpolation identified
hotspots of C. capitata population in the orchard borders
which progressively extended to the rest of the orchard.
Kriging analysis seems to be an extremely useful complement
Int J Trop Insect Sci
to the FTD index. Information about the local fine-scale dis-
tribution of target pests could enable a more calibrated imple-
mentation of control measures (i.e. on the most suitable or-
chard areas), thus reducing the economic and environmental
costs of pest control (Alemany et al. 2006).
With respect to pest management, the high population
of B. dorsalis along the border of the mango orchard
earlier in the season would justify concentration of control
measures at the borders during this period. However, sim-
ilar studies should be repeated across multiple seasons for
better consistency of the conclusion since environmental
factors can vary from one season to another. Similarly,
these results cannot be extrapolated to other farms due
to the difference of biotic and abiotic conditions between.
Nevertheless, the results of this study provide a first quan-
titative information on the fine-scale distribution of
B. dorsalis and have the potential of assisting in the man-
agement of B. dorsalis by providing tools for the timely
implementation of control measures in the areas of higher
abundance of flies, before the population grow up and
disperse to other parts of the orchard.
Conclusions
Our results demonstrate that the distribution of B. dorsalis
were heterogeneous on the orchard, with the population build-
ing up from the border to the internal region of the orchard.
The population peak were observed in January with densities
of more than 500 flies per trap per week.
Acknowledgments We thank the Royal Museum for Central Africa for
the funding of the study, project S1TNZ_MOZ_IPM, to Eduardo
Mondlane University and Sokoine University of Agriculture through
the Framework Agreement with the Belgian Development Cooperation.
And thanks to the technicians from the National Fruit Fly Laboratory for
their technical assistance and help during the field work.
Authors’ contributions Not applicable.
Funding information This study was funded by the Belgian
Development Cooperation through the Framework Agreement with the
Royal Museum for Central Africa (Belgium) under project “Spatio-tem-
poral population dynamics of fruit fly populations and optimization of
IPM program in Manica Province, Mozambique” (Project Number: S1_
TNZ_MOZ_IPM).
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Availability of data and material Not applicable.
Code availability Not applicable.
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