Malaria Journal

Soma et al. Malar J (2017) 16:357

DOI 10.1186/s12936-017-2012-8

RESEARCH Open Access

Does mosquito massrearing produce an

inferior mosquito?
DieudonnD.Soma1,2,3*, HamidouMaga1,2, WadakaMamai2,4, NanwintounS.BimbileSomda1,2,
NeliusVenter5, AdelB.Ali2, HananoYamada2, AbdoulayeDiabat1, FlorenceFournet6, GeorgesA.Oudraogo3,
RosemaryS.Lees7, RochK.Dabir1 andJeremieR.L.Gilles2*

Abstract
Background: The success of the sterile insect technique depends, among other things, on continuous releases of
sexually competitive sterile males within the target area. Several factors (including high rearing density and physi
cal manipulation, such as larvae and pupae separation) can influence the quality of males produced in mass-rearing
facilities. The different steps in mass production in the laboratory may modify the behaviour of mosquitoes, directly
or through loss of natural characters as a result of adaptation to lab rearing, and lead to the competitiveness of sterile
male being reduced. In the present study, the objective was to evaluate the effect of mass-rearing conditions on ster
ile male sexual competitiveness in semi-field cages compared to routine small scale laboratory rearing methods.
Methods: Anopheles arabiensis immature stages were reared both on a large scale using a rack and tray system
developed by the FAO/IAEA (MRS), and on a small scale using standard laboratory rearing trays (SRS). Mosquito life his
tory traits such as pupation rate, emergence rate, adult size as well as the effect of irradiation on adult longevity were
evaluated. Moreover, 56day old mosquitoes were released into field cages and left for two nights to mate and the
mating competitiveness between sterile mass-reared males and fertile males reared on a small scale when compet
ing for small scale reared virgin females was investigated. Resulting fertility in a treatment ratio of 1:1:1 (100 irradiated
males: 100 non-irradiated males: 100 virgin females) was compared to control cages with 0:100:100 (non-irradiated
control) and 100:0:100 (irradiated control).
Results: No significant differences in life history parameters were observed between rearing methods. The competi
tiveness index of mass reared males (0.58) was similar to males reared on a small scale (0.59). A residual fertility rate of
20% was observed in the irradiated control (100:0:100), measured as the percentage of eggs collected from the cages
which developed to adulthood. No significant difference was observed (t=0.2896, df=4, P=0.7865) between the
rearing treatments (MRS and SRS) in the fertility rate, a measure of mating competitiveness.
Conclusions: The results showed that the FAO/IAEA mass-rearing process did not affect mosquito life history param
eters or the mating competitiveness of males.
Keywords: Anopheles arabiensis, Sterile insect technique, Mass-rearing, Competitiveness

Background malaria control strategies are mainly based on the use

Malaria remains a serious threat to world health, caus- of insecticides, chemoprevention and case management
ing an estimated 212 million malaria cases and 429,000 [1]. Vector control has been and continues to be an effec-
deaths in 2015 [1]. With no vaccine available, current tive means of disease control [1, 2], though the current
malaria control strategies are being undermined by the
rapid spread of resistance to common insecticide classes
*Correspondence: [email protected]; [email protected] in major malaria vectors [36] and of Plasmodium to
2
Insect Pest Control Laboratory, Joint FAO/IAEA Division ofNuclear available anti-malaria drugs [7]. Therefore, innovative
Techniques inFood andAgriculture, Vienna, Austria
Full list of author information is available at the end of the article

The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License
(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license,
and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/
publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Soma et al. Malar J (2017) 16:357 Page 2 of 8

and/or alternative strategies are needed for more effec- loaded with around 15,000 pupae where emerging adults
tive vector control [8, 9]. has access to 5% sugar solution using a Whatman fil-
The sterile insect technique (SIT), involving release of ter paper (58 58 cm). Females were offered defrosted
males sterilized using gamma or X-rays, could be used in bovine blood in the Hemotek membrane feeder (Dis-
the context of integrated vector control as it has already covery Workshops, UK) [19] for 2h. Eggs were collected
been by many control programmes of insect pests or from large cages and quantified according to methods
disease vectors (as reviewed by Lees etal. [10]). The suc- described by Maga et al. [20], and reared to adulthood
cess of the SIT component depends, among other things, on either a mass-rearing scale (mass-rearing MRS) or a
on continuous releases of sexually competitive sterile small rearing scale (SRS) for all experiments.
male within the target area [11]. It is desirable that the
released males be as sexually competitive as wild males Massrearing scale
[10]. The different processes of mass production in the Immature stages were reared in the larval mass-
laboratory may modify the behaviour of mosquitoes, by rearing unit, a tiltable steel rack holding 50 trays
directly impacting their quality or over time through loss (100 60 3 cm) developed at the FAO/IAEA IPCL
of natural characteristics during adaptation to lab rearing [21]. Each tray was filled with 4L of deionized water the
[12]. This can contribute to reducing the competitiveness day before adding the eggs to allow the water to reach
of the sterile males, in addition to the impact of irradia- room temperature (2830 C). An aliquot of 4000 eggs
tion that can affect competitiveness when too high doses was dispensed into a plastic ring floating on the surface of
are used or handling methods are not optimized [13]. the water in each of the fifty rearing trays. The IAEA lar-
The rearing history of the colony and a lack of genetic val diet (1%) was used to feed larvae [22], and pupae were
diversity induced by the laboratory colonization might collected by tilting the rack and separating them from
also alter male sexual vigour under field conditions [14]. remaining larvae following the IAEA guidelines [23].
Therefore, studies in semi-field cages are necessary to
better evaluate the competitiveness of sterile mass-reared Small rearing scale
males and to determine the minimum required release Aliquots of 750 eggs obtained from mass-rearing cages
ratio of sterile male to wild male that could impact wild were hatched and reared in small plastic laboratory trays
insect populations. (30407cm) filled with 1L of deionized water [24].
The semi-field cage system provides a very valuable A 1% solution of the IAEA diet was used to feed larvae:
measure of these parameters, as demonstrated in previ- 10mL per tray for the first 3days, 20mL on the 4thday
ous studies in Anopheles coluzzii [15] and Anopheles ara- and 30mL on each remaining day as described by Mamai
biensis [16, 17]. However, all mosquitoes used in these et al. [24]. Pupae were removed on a daily basis using a
previous experiments were reared using routine labo- pipette, counted and placed into small bowls contain-
ratory equipment at a small scale and no studies have ing 50mL of the same water treatment as they had been
assessed the competitiveness of sterile males reared using reared as larvae to homogenize rearing conditions. Pupae
the FAO/IAEA mass-rearing unit. collected from each rearing method were divided into
This study aimed to assess the effect of mass-rearing two groups, one for irradiation and one for adult size and
conditions on mosquito life history traits and sterile male longevity measurements.
sexual competitiveness in semi-field cages compared to
routine small scale laboratory rearing methods. The effi- Irradiation ofpupae
cacy of the sterilization process was evaluated in terms Pupae collected from both rearing conditions were sep-
of residual fertility which was further assessed when full arated by sex under a stereomicroscope by observing
sterilization was not reached by observing whether the the shape of their genitalia [25]. Individuals pupating
larvae that hatched can reach adulthood. between 9:00 a.m. and 3:00p.m. each day were collected
for irradiation at 11:00 a.m. the following day, so that
Methods
ammacell (Nordion
2026 h old male pupae were irradiated with gamma
Mosquito strain andrearing conditions rays generated by a Cobalt-60 G
The Anopheles arabiensis Dongola strain, originat- 220) source at the IPCL (Seibersdorf, Austria) at a dose
ing from the northern state of Sudan was used in all of 75 Gy. To avoid possible variability related to radia-
experiments. Adults were reared at a temperature of tion exposure, pupae originating from MRS and SRS
27 1 C, 60 10% relative humidity (RH) and main- were irradiated at the same time, 75 pupae per batch
tained under a light regime (light: dark) of 12:12h includ- with most of the rearing water removed. The precise

with a dosimetry system using Gafchromic HD-810 film

ing 1 h each of dusk and dawn. Adult mosquitoes were dose received by pupae in each treatment was measured
mass-reared using large cages (20010020cm) [18]
Soma et al. Malar J (2017) 16:357 Page 3 of 8

(International Specialty Products, NJ, USA) [23]. After Raton. USA) in a climate controlled greenhouse (average
irradiation, pupae from each replicate were separated temperature of 271C, 505% RH and natural light).
into small cages (303030cm, Bugdorm 1H; Mega A larval tray (100603cm) was introduced into each
View, Taiwan), allowed to emerge overnight, and adults cage containing two 150mL plastic bottles of 5% sucrose
given access to 5% sucrose solution. solution with a filter paper (Melitta 1 4 ORIGINAL
FSC C095206). The trays served as resting sites and as
Adult size attractants, facilitating the location of the sugar sources
Wing lengths were measured as a proxy for adult size [26, by the mosquitoes [1517]. Five to 6day old mosquitoes
27]. Right wings were dissected, placed on a microscope were released into field cages and allowed to mate for two
slide and an image of the wing taken using a digital cam- nights in a treatment cage containing 1:1:1 (100 irradi-
era mounted on a stereo microscope. The wing length, ated males: 100 non-irradiated males: 100 virgin females)
defined as the distance from the axillary incision (alula) or control cages containing either 0:100:100 (non-irradi-
to the apical margin (excluding fringes), was measured ated control) or 100:0:100 (irradiated control). Five repli-
from the digital images using analysis_FIVE software cates of each treatment were randomly positioned within
(Soft Imaging System, Germany). Wing lengths from the greenhouse (Fig. 1). All virgin females used in this
154 male mosquitoes were used to compare SRS and competitiveness experiment provided from SRS and the
MRS treatments (about 3540 wings from each of four males either from MRS or SRS.
replicates). On the 3rdday following release, all females were rec-
ollected from the field cages with a mouth aspirator and
Adult longevity placed inside 303030cm cages. Defrosted bovine
The longevity of newly emerged males was assessed (50 blood in the Hemotek system [19] was used to feed
unirradiated and 50 irradiated) in small rearing cages females for 30 min on each of three consecutive days.
(30 30 30 cm) with females kept under standard Blood fed females were allowed to lay eggs en masse in

hatman, Maidstone, UK) on

insectary conditions (27 1 C and 60 10% RH) for plastic cups (90 mm diameter) containing a filter paper
the duration of the experiment. A 5% sucrose solution (Cat No. 1001 090. 597; W
was supplied in a 150mL plastic bottle with a filter paper. a wet sponge cloth soaked in water until fully saturated.
Dead mosquitoes were removed daily and counted until Eggs were collected daily for 5days and each batch was
the last individual died. For each group, three replicates allowed to hatch over 2days [15].
were performed. The number of pupae and adults resulting from eggs
collected from treatment and control cages were used
Male mating competitiveness to calculate the fertility of each. Pupation rate and
Experiments were conducted in semi-field cages emergence rate were calculated by dividing the num-
(1.75 1.75 1.75 m, 5.36 m3, Live Monarch. Boca ber of pupae and emerging adults by the number of

irradiated males; female; male

Fig.1 Experimental design used to assess Anopheles arabiensis male mating competitiveness. MRS mass-rearing scale, SRS small rearing scale,
#
Soma et al. Malar J (2017) 16:357 Page 4 of 8

collected eggs from each treatment. Induced sterility (n = 156) group (t = 0.3473, df = 152, P = 0.7288)
(IS) [28] was calculated following the method used by (Fig.2).
Yamada etal. [16]. Insemination rate was assessed after
the oviposition period by dissecting the spermatheca Adult longevity
of the recaptured females under a stereomicroscope. A Log-Rank (Mantel-Cox) test comparison of longev-
Females that died before oviposition were also dis- ity (Fig. 3) showed no significant difference in longevity
sected. The presence/absence of spermatozoa was con- between irradiated or unirradiated males either from SRS or
firmed using a compound light microscope at 400 MRS (2=2.473, df=3, P=0.4801). Time to 100% mortal-
magnification. ity was 41 days for SRS males and 42 days for those from
MRS, a difference that was not statistically significant (Log-
Parameters measured andstatistical analysis rank (Mantel-Cox) test, 2=0.6782, df=1, P=0.4102).
The mean number of eggs laid per cage (females recap-
tured from semi-field cages) was counted using a ster- Recapture rate
eomicroscope and a mean fecundity for each treatment The average percentage of females recaptured from semi-
was calculated by dividing the number of eggs laid daily field cages after 2 days of mating ranged from 68.20 to
by the number of females still alive (before egg collec- 81.28% across all treatments (Table 1). No statistically
tion) [15]. The mean insemination rate was also used to significant difference in female recapture rate between
estimate the average number of females that laid eggs treatment and control cages (ANOVA, F = 0.8776,
and the average number of eggs laid per female. Egg df=5, P=0.5059) was observed.
hatch rate (fertility) was assessed by dividing the num-
ber of first instar larvae (L1) counted by the number
of eggs laid. After hatching and being counted, larvae
were transferred into plastic trays (30407cm) and
reared according to the protocol developed by Mamai
etal. [24].
The competitiveness index (C) described by Fried [29]
was calculated for each treatment using egg hatch rate
from the unirradiated control (Ha), irradiated control
(Hs) and competitiveness treatments (Ho) as follows:
C=((HaHo)/(HoHs))(N/S); where N is the num-
ber of unirradiated males and S the number of irradiated
males.

were performed using Microsoft Excel 2013 ( Microsoft,

Graphics were produced and all statistical analyses

USA) and Graph Pad Prism v.5.0 software. Fecundity,

egg hatch rate, insemination rate, pupation rate and Fig.2 Mean wing length in Anopheles arabiensis reared at MRS and
emergence rate were analysed using analysis of vari- SRS
ance (ANOVA) with Tukeys honestly significant dif-
ference (HSD) post hoc tests. Wing length was tested
for normality with the KolmogorovSmirnov test and
mean length of male and female mosquitoes obtained
from SRS and MRS compared using the Students t test.
The KaplanMeier method was used to assess adult
longevity. All data expressed as a proportion were arc-
sine-square-root transformed to stabilize variance and
normalize distribution before analysis. The alpha level
was P<0.05.

Results
Adult size
No significant difference was observed when wing
lengths of males from the SRS treatment (n = 154) Fig.3 Longevity curves of Anopheles arabiensis males reared at MRS
were compared to those from the MRS treatment and SRS
Soma et al. Malar J (2017) 16:357 Page 5 of 8

Table1 Mean proportion ofrecaptured females, female insemination rate andfecundity ofAn. arabiensis followingmat-
ing competitiveness experiments insemi-field cages
Treatments Ratio S:F:F Mean ofRSE (minmax) IR F (meanSE)
n % meanSE

Unirradiated control-MRS 0:100:100 81.283.81 (7092) 212 64.304.15 691.75177.46

Unirradiated control-SRS 0:100:100 76.205.62 (5484) 199 60.174.36 234.50148.05
Irradiated control-MRS 100:0:100 68.203.26 (5976) 211 53.225.85 370.75281.13

MRS#:SRS:SRS
Irradiated control-SRS 100:0:100 73.837.94 (4994) 235 57.345.30 598.50337.80

SRS#: MRS:SRS
100:100:100 75.086.23 (5797) 280 53.842.40 155.0089.83
100:100:100 72.434.12 (5789) 271 50.021.47 206.0055.75
R (%SE) average percentage of recaptured females, (minmax) minimum and maximum, IR (%SE) proportion of dissected females per treatment, n number of
dissected females, F (%SE) average number of eggs laid per female, SE standard error, S irradiated male, F unirradiated male, F virgin female

Insemination rate andfecundity Competitiveness index, egg hatch rate andinduced

Insemination rate did not differ significantly between sterility
control and treatment cages (ANOVA, F = 0.1831, The competitiveness indices of irradiated males com-
df = 5, P = 0.9663). The number of eggs collected pared to controls calculated from treatment cages at
from different treatments varied from 155.00 to 691.75 1:1:1 ratio (irradiated males: unirradiated males: virgin
(Table1); but no significant difference between treatment females) were 0.58 0.10 and 0.59 0.07 for irradi-
and control cages was observed (ANOVA, F = 1.137, ated MRS and SRS males, respectively (Table2). The egg
df=5, P=0.3733). hatch rate in treatment cages was not significantly dif-
The number of eggs per female, calculated based ferent (t = 0.5145, df = 4, P = 0.6340). Egg hatch rates
on insemination rate and total number of eggs, was were significantly different (ANOVA, F=1.179, df=5,
49.3228.23 and 12.697.28 for unirradiated control P=0.3484) between control cages (unirradiated and irra-
MRS and SRS treatments, respectively (Tukey Multiple diated) and competition treatment cages. The induced
Comparison Test, P > 0.05). Females mated with irradi- sterility was similar in 1:1:1 ratio cages: 27.81 3.79
ated males (in the sterile control) from the MRS treat- and 27.94 2.21% in MRS and SRS male treatments,
ment laid 16.689.90 eggs and 29.2219.95 eggs when respectively.
mated to irradiated males from the SRS (Tukey Multi- Overall, pupation rate from eggs collected from experi-
ple Comparison Test, P>0.05). Females from treatment mental cages was significantly higher in controls (unirra-
cages where males were in competition (irradiated males diated and irradiated) cages compared to the treatment
from MRS competing with unirradiated SRS males, cages (ANOVA, F=3.778, df=5, P=0.0115). However,
and irradiated males from SRS competing with unir- when the average pupation rate was compared between
radiated MRS males) laid 6.24 2.70 and 19.85 4.94 the rearing treatments (MRS and SRS), no significant dif-
eggs, respectively (A Tukey Multiple Comparison Test, ference was observed (t = 0.2896, df = 4, P = 0.7865).
P>0.05). Similar observations were made in emergence rate in

Table2 Competitiveness index ofirradiated Anopheles arabiensis males andinduced sterility inlarge cage experiment
Treatments Ratio S:F:F Hatch rate (% meanSE) C (meanSE) IS (%SE)

Unirradiated control-MRS 0:100:100 84.222.88a

Unirradiated control-SRS 0:100:100 86.222.70a
#
Irradiated control-MRS 100:0:100 19.141.45b

MRS :SRS:SRS
#
Irradiated control-SRS 100:0:100 20.850.77b

SRS : MRS:SRS
#
100:100:100 61.072.32c 0.580.10 27.813.79
#
100:100:100 61.792.05c 0.590.07 27.942.21
Significantly differences between hatch rates are indicated by different letters (Tukeys posthoc test, P<0.05)
C competitiveness index, IS induced sterility, SE standard error, S irradiated male, F unirradiated male, F virgin female
#
Irradiated male
Soma et al. Malar J (2017) 16:357 Page 6 of 8

eggs collected from treatment cages (t=0.5968, df=4; across all treatments and the relatively low number of
P=0.5828) (Fig.4). eggs produced by the females could be attributed to
female specific factors, such as the success of insemi-
Discussion nation or the volume of blood meal taken, which are
Rearing conditions have been shown to play a vital role known to affect insect fecundity [35]. The en masse egg
in adult competitiveness of fruit flies and tsetse flies [30, collection method could partly explain the differences
31], among other insect species. In this study, a compara- observed in the average number of eggs laid per female
tive approach was employed to assess two rearing types between treatments because it cannot take into account
in terms of their effect on a number. Life history traits of the exact number of females that laid, thus making esti-
An. arabiensis and male mating competitiveness in semi- mates very approximate, as noted previously [36].
field cages. The face that neither adult body size nor longevity were
In this experiment, neither body size nor longevity significantly different between rearing treatments indi-
were adversely affected by the mass-rearing process com- cates that there was no major difference in the overall
pared to the small scale rearing routinely used. Although, quality of males produced by these two rearing systems
the rearing was done for one generation, it would be (MRS and SRS). Laboratory reared males may be less
important for further analysis to evaluate these param- competitive than wild males, even without considering
eters over multiple generations. The combination of rear- the damage caused by sterilization techniques, but there
ing at high larval density and the processes of tilting and is a lot of controversy around how much of an impact
larvae/pupae separation of thousands of mosquitoes dur- colonization and mass-rearing has on subsequent mat-
ing mass-rearing did not appear to adversely affect the ing success (see for example [37]). However, the results
adults. This result is interesting because for SIT release of these semi-field assays used to compare rearing treat-
programme to be successful, sterile males must be of suf- ments (SRS and MRS) reported in this study suggest that
ficient quality to disperse into the environment, survive male competitiveness was not impacted by mass scale
long enough to locate and attract wild females, in com- rearing.
petition with wild counterparts, and copulate with as A release ratio of 1:1 irradiated to fertile males induced
many as wild females as possible. The size of adult male about 27% of sterility, suggesting that in practice a higher
mosquitoes is thought by many to be an important pre- ratio of irradiated to unirradiated males will need to be
dictor of their mating success [15, 3234]. Pupae of the released to cause significant population reduction [38
same age and adult males of the same size were used here 40]. It is important to note that although the number of
in order to minimize any effect of adult size and age on larvae hatching from cages where irradiated males were
the mating competition between males from the SRS and competing for mates was high, only half of larvae that
MRS treatments. The observed variability in fecundity hatched reached pupation and less than 20% survived
to adult emergence. The apparently low competitiveness
and high residual fertility of sterile males was therefore
not as high as it first seemed, which is reassuring for
the predicted success of releases of these males in an
SIT programme. A competition experiment conducted
in the same conditions as in this study by Yamada etal.
[16] has shown that a 10:1 release ratio of An. arabiensis
genetic sexing strain ANO IPCL1 irradiated with a dose
of 75 Gy and competing with fertile counterparts that
would be necessary to induce about 80% sterility [17].
Munhenga et al. [17] have recorded a competitiveness
index of 0.36 for an An. arabiensis strain which has been
lab reared since 2010 while an An. coluzzii strain colo-
nized in the lab for about 6years has shown a competi-
Fig.4 Proportion of Anopheles arabiensis larvae, pupae and adults tiveness index of 0.53 under semi-field conditions [15].
emerging from eggs collected from different treatment cages. In addition to rearing conditions and irradiation,
Proportion of larvae=black bars; pupae=grey bars; adults=white inbreeding among laboratory reared mosquitoes nega-
bars; UC-MRS/UC-SRS unirradiated control male from mass or small
rearing scale, IC-MRS/IC-SRS irradiated control male from mass or
tively impacts a variety of male reproductive traits (for
small rearing scale, MRS# vs SRS/SRS# vs MRS irradiated male versus example, sperm vigor and size of mating plugs) which are
unirradiated male. Within each parameter were found not to be sig crucial to their reproductive success [40]. It is therefore
nificantly different from each other (Tukeys posthoc test, P<0.05) good practice in operational SIT programmes to refresh
Soma et al. Malar J (2017) 16:357 Page 7 of 8

laboratory-kept colonies with field collected mosquitoes Availability of data and materials
The datasets used during the current study are available from the correspond
on a regular basis in order to reduce the effect of colo- ing author on reasonable request.
nization and inbreeding on mating competitiveness [17].
Consent for publication
Not applicable.
Conclusions
In this study, males reared under mass and small rearing Ethics approval and consent to participate
conditions were compared, and mass production condi- Not applicable.
tions (high population density, close space, tilting, larvae
and pupae separation) were found not to affect mosquito Publishers Note
Springer Nature remains neutral with regard to jurisdictional claims in pub
life history traits, male competitiveness or induced steril- lished maps and institutional affiliations.
ity. The current technology and protocols developed at
the FAO/IAEA IPCL for An. arabiensis mass-rearing are Received: 2 February 2017 Accepted: 4 September 2017
thus apparently adequate and ready to be implemented in
SIT programmes. However, it is important in the context
of SIT programmes to further assess the competitiveness
of colonized and mass-reared males in semi-field condi- References
tions with females and males from wild-collected larvae 1. WHO. World malaria report 2016. Geneva: World Health
or eggs to more accurately predict their performance Organization; 2016. http://www.who.int/malaria/publications/
world-malaria-report-2016.
after release. Other procedures involved in mass-rearing 2. Brady OJ, Godfray HCJ, Tatem AJ, Gething PW, Cohen JM, Ellis McKenzie
and production for release, including packing, chilling F, etal. Adult vector control, mosquito ecology and malaria transmission.
and handling before releases, not included in the scope of Int Health. 2015;7:1219.
3. Dabir KR, Diabat A, Djogbenou L, Ouari A, Guessan RN, Oudraogo J,
this study, also need to be investigated for their impact on etal. Dynamics of multiple insecticide resistance in the malaria vector.
male quality. Malar J. 2008;7:188.
4. Namountougou M, Simard F, Baldet T, Diabat A, Oudraogo JB, Martin T,
etal. Multiple insecticide resistance in Anopheles gambiae s.l. populations
Abbreviations from Burkina Faso, West Africa. PLoS ONE. 2012;7:e48412.
ANOVA: analysis of variance; FAO: Food and Agricultural Organization; IAEA: 5. Mosqueira B, Soma DD, Namountougou M, Poda S, Diabat A, Ali O, etal.
International Atomic Energy Agency; IPCL: Insect Pest Control Laboratory; LD: Pilot study on the combination of an organophosphate-based insecti
light: dark; MRS: mass-rearing scale; SIT: sterile insect technique; SRS: small cide paint and pyrethroid-treated long lasting nets against pyrethroid
rearing scale; RH: relative humidity; WHO: World Health Organization. resistant malaria vectors in Burkina Faso. Acta Trop. 2015;148:1629.
6. Reid MC, McKenzie FE. The contribution of agricultural insecticide use
Authors contributions to increasing insecticide resistance in African malaria vectors. Malar J.
SDD, MH, MW, RSL and JRLG contributed to the design of the study. SDD, 2016;15:107.
MH, MW, B-SNS, VN and ABA performed the experiments.SDD analysed the 7. Agomo CO, Oyibo WA, Sutherland C, Hallet R, Oguike M. Assessment of
data and wrote the manuscript which was critically revised by MH, MW, RSL, markers of antimalarial drug resistance in Plasmodium falciparum isolates
HY, GAO, FF, AD, RKD. JRLG supervised the entire work. All authors read and from pregnant women in Lagos, Nigeria. PLoS ONE. 2016;11:e0146908.
approved the final manuscript. 8. Enayati A, Lines J, Maharaj R HJ. Shrinking the Malaria Map: A prospectus
on malaria elimination. Feachem RGA, Phillips AA, Targett GA, editors.
Author details Chapt. 9: Suppressing the Vector. San Francisco: The Global Health Group,
1
Institut de Recherche en Sciences de la Sant/Centre Muraz, BP 2009. p. 14054.
545BoboDioulasso, Burkina Faso. 2Insect Pest Control Laboratory, Joint FAO/ 9. Bouyer J. Integrated management of insect vectors of human and animal
IAEA Division ofNuclear Techniques inFood andAgriculture, Vienna, Austria. diseases. Developing genetic control. Perspect Heal. 2015. www.cirad.fr/
3
Universit Nazi Boni, BoboDioulasso, Burkina Faso. 4Institut de Recherche publications-ressources/edition/perspective-policy-brief.
Agricole pour le Dveloppement (IRAD), Yaound, Cameroon. 5Vector Control 10. Lees RS, Knols B, Bellini R, Benedict MQ, Bheecarry A, Bossin HC, etal.
Reference Laboratory, Centre forOpportunistic, Tropical & Hospital Infec Review: improving our knowledge of male mosquito biology in relation
tions, National Institute forCommunicable Diseases / Wits Research Institute to genetic control programmes. Acta Trop. 2014;132:S211.
forMalaria, School ofPathology, Faculty ofHealth Sciences, University ofthe 11. Dame DA, Lowe RE. Assessment of released sterile Anopheles albimanus
Witwatersrand, Johannesburg, South Africa. 6Institut de Recherche pour le and Glossina morsitans morsitans. In: Pal R, Kitzmiller J, Kanda TA, editors.
Dveloppement (IRD), MIVEGEC, BP 64501, 34394Montpellier Cedex 5, France. Cytogenetics and genetics of vectors. Netherlands: Elsevier Biomedical;
7
Liverpool Insect Testing Establishment (LITE), Vector Biology Department, 1981. p. 23148.
Liverpool School ofTropical Medicine, Pembroke Place, LiverpoolL3 5QA, UK. 12. Helinski H, Knols J. Mating competitiveness of male Anopheles arabiensis
mosquitoes irradiated with a partially or fully sterilizing dose in small and
Acknowledgements large laboratory cages. J Med Entomol. 2008; 698705.
The authors are grateful to Marc J. B. Vreysen for the useful comments on the 13. Helinski MEH, Parker AG, Knols BGJ. Radiation biology of mosquitoes.
manuscript. Authors thank reviewers and editor for their useful comments and Malar J. 2009;8(Suppl 2):S6.
suggestions which have led to an improved manuscript. SDD received a grant 14. Benedict MQ, Knols BGJ, Bossin HC, Howell PI, Mialhe E, Caceres C, etal.
from the International Master of Entomology (MIE), University of Montpelier, Colonisation and mass rearing: learning from others. Malar J. 2009;8:S4.
France and Universit Alassane Ouattara, Ivory Coast. This work has been 15. Maga H, Damiens D, Niang A, Sawadogo SP, Fatherhaman O, Lees RS,
funded and supported by the FAO/IAEA. etal. Mating competitiveness of sterile male Anopheles coluzzii in large
cages. Malar J. 2014;13:460.
Competing interests 16. Yamada H, Vreysen MJB, Gilles JRL, Munhenga G, Damiens DD. The effects of
The authors declare that they have no competing interests. genetic manipulation, dieldrin treatment and irradiation on the mating com
petitiveness of male Anopheles arabiensis in field cages. Malar J. 2014;13:318.
Soma et al. Malar J (2017) 16:357 Page 8 of 8

17. Munhenga G, Brooke BD, Gilles JRL, Slabbert K, Kemp A, Dandalo LC, etal. 30. Dyck VA, Hendrichs J, Robinson AS. Sterile insect technique-principles
Mating competitiveness of sterile genetic sexing strain males (GAMA) and practice in area-wide integrated pest management. Book. 2005.
under laboratory and semi-field conditions: steps towards the use of the http://www.springer.com/la/book/9781402040504.
Sterile Insect Technique to control the major malaria vector Anopheles 31. Vreysen MJ, Saleh KM, Ali MY, Abdulla AM, Zhu ZR, Juma KG, etal. Glossina
arabiensis in South Africa. Parasit Vectors. 2016;9:122. austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzi
18. Maiga H, Bimbil-Somda NS, Yamada H, Wood O, Damiens D, Mamai bar, using the sterile insect technique. J Econ Entomol. 2000;93:12335.
W, etal. Enhancements to the mass rearing cage for the malaria vector, 32. Anderson M. Sexual selection. Princeton: Princeton University Press; 1994.
Anopheles arabiensis for improved adult longevity and egg production. 33. Charlwood JD, Pinto J, Sousa CA, Madsen H. Ferreira C, do Rosario VE.
Entomol Exp Appl. 2017. 10.1111/eea.12614. The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera:
19. Cosgrove JB, Wood RJ, Petric D, Evans DT, Abbott RH. A conveni Culicidae) from Sao Tome Island. J Vector Ecol. 2002;27:17883.
ent mosquito membrane feeding system. J Am Mosq Control Assoc. 34. Maga H, Dabir RK, Lehmann T, Tripet F, Diabat A. Variation in energy
1994;10:4346. reserves and role of body size in the mating system of Anopheles gam-
20. Maga H, Damiens D, Diabat A, Dabir R, Oudraogo G, Lees R, etal. biae. J Vector Ecol. 2012;37:28997.
Large-scale Anopheles arabiensis egg quantification methods for mass 35. Damiens D, Soliban SM, Balestrino F, Alsir R, Vreysen MJB. Different blood
rearing operations. Malar J. 2016;15:72. and sugar feeding regimes affect the productivity of Anopheles arabiensis
21. Balestrino F, Benedict MQ. A new larval tray and rack system for improved colonies (Diptera: Culicidae). Entomol Soc Am. 2013;50:33643.
mosquito mass rearing. J Med Entomol. 2012;49:595605. 36. Helinski MEH, Parker AG, Knols BGJ. Radiation-induced sterility for pupal
22. Damiens D, Benedict MQ, Wille M. An inexpensive and effective larval diet and adult stages of the malaria mosquito Anopheles arabiensis. Malar J.
for Anopheles arabiensis (Diptera: Culicidae): eat like a horse, a bird, or a 2006;5:41.
fish? Entomol Soc Am. 2012;49:100111. 37. Baeshen R, Ekechukwu NE, Toure M, Paton D, Coulibaly M, Traor SF, etal.
23. IAEA. Guidelines for standardised mass rearing of Anopheles Mosquitoes. Differential effects of inbreeding and selection on male reproductive
Vienna: International Atomic Energy Agency; 2015. phenotype associated with the colonization and laboratory maintenance
24. Mamai W, Lees RS, Maiga H, Gilles JRL. Reusing larval rearing water and its of Anopheles gambiae. Malar J. 2014;13:19.
effect on development and quality of Anopheles arabiensis mosquitoes. 38. Ndo C, Yamada H, Damiens DD, Ndo S, Seballos G, Gilles JRL. X-ray sterili
Malar J. 2016;15:169. zation of the An. arabiensis genetic sexing strain ANO IPCL1 at pupal and
25. MR4. Separating larvae and pupae. In: Methods in Anopheles research. 4th adult stages. Acta Trop. 2014;131:1248.
edition. Atlanta: Centers for Disease Control and Prevention; 2014. 39. Damiens D, Tjeck PO, Lebon C, Le Goff G, Gouagna LC. The effects of
26. Lyimo EO, Koella JC. Relationship between body size of adult Anopheles age at first mating and release ratios on the mating competitiveness of
gambiae s.l. and infection with the malaria parasite Plasmodium falcipa- gamma sterilised Aedes albopictus males under semi field conditions.
rum. Parasitology. 1992;104(Pt 2):2337. Vector Biol J. 2016;1:16.
27. Koella JC, Lyimo EO. Variability in the relationship between weight and 40. Ekechukwu NE, Baeshen R, Traor SF, Coulibaly M, Diabate A, Catteruccia
wing length of Anopheles gambiae (Diptera: Culicidae). J Med Entomol. F, etal. Heterosis increases fertility, fecundity, and survival of laboratory-
1996;33:2614. produced F1 hybrid males of the malaria mosquito Anopheles coluzzii. G3
28. Curtis CF. Induced sterility in insects. Adv Reprod Physiol. 1971;5:11965. (Bethesda). 2015;5:2693709.
29. Fried M. Determination of sterile insect competitiveness. J Econ Entomol.
1971;64:86972.

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