Volume 01 / Issue 01 / March 2013 / 11-18  |  www.maralte.

com/ghp
2212-8832. http://dx.doi.org/10.5645/ghp2013.01.01.03

Efficacy of resting boxes baited with carbon dioxide versus CDC

light trap for sampling mosquito vectors: A comparative study

Eliningaya J. Kweka1 ,*, Eunice A. Owino2, Abstract

Ming-Chieh Lee3, Amruta Dixit3, Yousif E. Himeidan4, Background: Odours used by mosquitoes to locate the source of a blood meal are diverse
Aneth M. Mahande1 and can be synthesized either singly or in blends to reflect the different individual kairo-
mones that are released by the host body for attracting mosquitoes. Baited methods with
1
Tropical Pesticides Research Institute, Division of these kairomones are scarcely used to sample mosquito vectors in the field. Herein, we
Livestock and Human Health Disease Vector Control,
PO Box 3024, Arusha, Tanzania developed and compared CO2-baited resting boxes (BRBs) trap against standard Centres
2
School of Biological Sciences, University of Nairobi, for Disease Control miniature (CDC) light trap as a possible alternative field device for sam-
PO Box 30197-00100, Nairobi, Kenya pling mosquito populations in the field.
3
Program in Public Health, University of California, Irvine, Methods: Indoor samplings with BRB and CDC light trap were done for 6 consecutive
CA 92697, USA
days in six houses in Lower Moshi rice irrigation schemes, northern Tanzania, during the
4
Vector Health International, Africa Technical Research
Centre, PO Box 15500, Arusha, Tanzania
dry season of January–February, 2011. Different ratios of sugar–yeast culture were used
to release different amounts of CO2 in the BRB trap. Outdoor sampling was also done for
* Corresponding author: pat.kweka@gmail.com
comparing BRB with unbaited resting boxes (UBRBs). The sampling efficiency of BRB, URB,
and CDC light traps was measured by comparing mean densities of mosquitoes for each
Info trap in the same room using analysis of variance.
Article history: Results: The proportions of mosquitoes sampled with BRB technique were 4.8-folds
Received 24 May 2012 higher than URB, but 9.5-folds lower than the CDC light traps, indicating that BRB was less
Received in revised form 22 June 2012 effective and competitive for sampling mosquito vector populations in poor resource set-
Accepted 22 June 2012 tings and high burdens of vector borne-diseases in Sub Saharan of Africa.
Available online 5 July 2012 Conclusions: The BRB could not serve as a simple tool for field trapping, bearing on opera-
tional costs of yeast and sugar to be met by the local community and lower density sampled.
Keywords Further research might need to be carried out for improving the efficiency of BRB trap.
Mosquito | transmitted | diseases | malaria |
filariasis | dengue

Copyright © Maralte. All rights reserved

1.1 Background
Mosquito-transmitted diseases such as malaria, filariasis, and dengue
­ ccur mostly in tropical countries. There has been a downward trend in
o contact (Costantini, 1996; Costantini et al., 1998; Dekker & Takken, 1998;
the number of malarial cases reported and mosquitoes in several African
countries (Aregawi et al., 2011; Midega et al., 2010; Ministry of Health and
Social Welfare, 2008), including Tanzania (Aregawi et al., 2011; Ministry of
Health and Social Welfare, 2008). Despite the implementation of various
vector control measures, the disease continues to be a periodic health
problem (Greenwood & Mutabingwa, 2002). The most effective vec-
tors of malarial parasites in sub-Saharan Africa are Anopheles funestus,
Anopheles gambiae s.s (anthropophilic species), and Anopheles arabiensis
which can be ­either anthropophilic or zoophilic, depending on host avail-
ability (Besansky et al., 2004; Coetzee et al., 2000; Coetzee, 2004). The level
of attraction of these vectors has been shown to vary even among the
­human hosts. The variation has also been shown to depend on the specific
host odours that influence the rate of human–vector contacts, according
to the index that has been used largely to determine the vectorial capacity
of mosquito vector species (Burkot, 1988; Dekker et al., 2001; Dekker et al.,
2002; Himeidan et al., 2004). Therefore, the emanated host odour has been
considered a key factor in determining host preference and host–vectors
Gillies, 1967; Mboera et al., 2000).
Different chemical compounds released from the body of the host have
been recorded to activate the attraction of the mosquitoes to the host.
Olfactory cues produced by host odour include CO2 (Lacey & Carde, 2011;
Takken & Kline, 1989; Turner et al., 2011), carboxylic and aliphatic acids (Braks
et al., 1999; Costantini et al., 2001; Smallegange et al., 2005; Takken & Kline,
1989), ammonia, and dimethyl sulphide (Bernier et al., 2003), all of which are
encountered by mosquitoes during their host seeking. Many odour recep-
tors are mostly located on the palps of antennae of many disease vectors
including mosquitoes (Carey et al., 2010; Pitts et al., 2004; Zwiebel & Takken,
2004). In recent studies, the species-specific odour receptor genes have
been found to be regulated with the gonotrophic conditions of mosqui-
toes (Day, 2005; Pitts et al., 2004; Zwiebel & Takken, 2004).

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 12 Volume 01 / Issue 01 / March 2013 Global Health Perspectives

Among these odour kairomones, carbon dioxide, 1-octen-3-ol, and l-lactic

acid have been found to be the most common components (Bernier et al.,
2000; Gillies, 1988). Trapping of mosquitoes using carbon dioxide from dif-
ferent sources has been shown to influence the trapped density of haema-
tophagous insects in both laboratory and field settings (Mboera et al., 2000;
Saitoh et al., 2004; Takken & Knols, 1999). CO2 has been associated with the
activation of mosquito sensilla during host-seeking in all mosquito species
(Gillies, 1964). It is often accepted that CO2 serves as a powerful olfactory
cue for most haematophagous arthropods (Lehane, 1991; Smallegange
et al., 2010; Takken & Knols, 1999) and it has been used as a bait in traps for
dipteran flies including mosquitoes (Van Essen et al., 1994).
The current methods and sources of CO2 used for sampling mosquitoes
are considered complex, and therefore, are difficult to use on a large-scale
mosquito control in the field settings within Africa (Jawara et al., 2009;
Jawara et al., 2011; Mboera et al., 2000). Yeast (Saccharomyces cerevisiae)
cultures are relatively cheap and are one of the best sources for produc-
ing CO2, particularly when fermented with sugar (Guerenstein et al., 1995;
Smallegange et al., 2010). Such cultures could be useful in attracting haema-
tophagous insects and this method can easily suit the manipulated needs
of different sampling devices. Development of a safe, practical, and cost-­
effective alternative to human landing catch for surveillance of ­malaria
vectors should be incorporated into mosquito attractants, which resem-
bles those released by hosts.
This study was designed to quantify the attractiveness of baited resting
box (BRB) in sampling An. gambiae s.l, with Centres for Disease Control
(CDC) miniature light trap as the standard tool. The BRB traps were devel-
oped and tested as an alternative novel sampling device for incorporating Figure 1.  A map showing the study and houses in lower Moshi irrigation
the use of CO2 as a lure for surveillance of the vector population in the field. scheme, Northern Tanzania.

1.2 Material and Methods

1.2.1 Description and design of study areas

The study was conducted in Lower Moshi rice irrigation schemes in
northern Tanzania (3°21'S, 37°21'E) (Figure 1) during the rice transplanta-
tion period of the dry season in January–February, 2011. Six houses located
within the irrigation scheme were selected for sampling mosquitoes for
both outdoor and indoor resting behaviour. Six different concentrations of
the yeast–sugar culture were used in the boxes. BRB and URB were paired
outdoor and indoor in the six houses for 6 days of mosquito trapping (6 × 6
Latin square design). Indoor and outdoor samplings were done separately
in different rotations and not at the same time. Each room selected for this
study was occupied by two individuals who slept under untreated bed net
so as to avoid the effect of insecticides-treated bed nets.

1.2.2 Boxes trap: Preparation and trapping

Paper boxes of 60 × 60 × 30 cm used for packing goods were used as the
resting traps after some modifications. The inner walls of the box were
lined with black cotton clothing material that provided a good resting
surface for the mosquitoes (Figure 2A). These resting boxes have been
described in other previous studies (Guerenstein et al., 1995; Kweka et al.,
2009; Kweka et al., 2010; Mahande et al., 2010; Smallegange et al., 2010). The
front entry side of the box was left open (Figure 2B). Boxes were placed
15 cm above the ground outdoors and 105 cm above the ground indoors as
­described in a previous study (Kweka et al., 2010).
In BRB, the inner wall of the boxes was covered with a black cloth mate-
rial incorporated with cow urine, whereas the unbaited resting box (UBRB) Figure 2.  A resting boxes baited (A) with CO2 for trapping mosquitoes 15 m
was lined with clothing material alone, i.e., without the cow urine. outside a house (a resting box setup outdoors).

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 Global Health Perspectives Volume 01 / Issue 01 / March 2013 13

Table 1.  Composition ratio of yeast and sugar used and amount
of CO2 released for each mixture.
Amount of gas
Mixture Yeast Water
Sugar (g) volume release
No. (g) (L)
(mL/minute)

1 17.5 250 2.5 170

2 17.5 500 2.5 300

3 17.5 750 2.5 190

4 35 250 2.5 250

5 35 500 2.5 340

6 35 750 2.5 360

1.2.3 CDC trap setting
CDC light traps were hanged beside the head of a person sleeping under
bed net 60 cm above the floor (Mboera et al., 1998). The person under the
bed net was trained on how to switch the trap on and off.
1.2.4 CO2 production and use in boxes
Different ratios of the sugar–yeast culture were used to release different
amounts of CO2 (Table 1). Each culture ratio was added into 2.5 L of water
in a 5-L container (Figure 2A) to be used overnight for trapping mosquitoes.
The BRB was prepared by connecting the 5-L container (containing sugar
fermenting yeast) to the resting box using a plastic tube (Figure 2A).
1.2.5 Mosquitoes sampling and identification
The BRB, URB, and CDC light traps (Model 512; John W. Hock Company,
Gainesville, FL) were set up at 18:00 h daily. In all traps, sampling from
the traps was done from 6:30 h to 7:30 h during all experimental days.
Mosquitoes in BRB and URB were collected using hand aspirators (WHO,
1975) (Figure 3). The collected mosquitoes were identified morphologically
to species level using standard morphological key protocol using a dissect-
ing microscope (Gillies & Coetzee, 1987; WHO, 1975) and sorted according to
their abdominal conditions and sex (Dekker et al., 2001).
1.2.6 Data analyses
Data were entered twice in a database created in EpiInfo. Data for mos-
quitoes collected by BRB and URB were first normalized by log transforma-
tion (n + 1) and then compared against each other using a paired t-test for
indoor and separately with those of outdoor sampling methods.
The sampling efficiency of BRB, URB, and CDC light traps was measured
by comparing means of the log-transformed mosquito density in the same
room for the different traps using one-way analysis of variance. In this
analysis, mosquito density was considered as an independent variable and
trapping method as a factor influencing mosquito catches.
The general linear model univariate analysis was used to analyze the fac-
tors influencing the trapping systems. In the analysis, mosquito catches
were modelled as a function of two fixed factors, namely, house loca-
tion and the culture of yeast and sugar mixtures. Days were considered
as random factors to reflect the daily variations in mosquito numbers.
Figure 3.  A pair of hand aspirators used for the collection of mosquitoes
from resting boxes.
Tukey–Kramer (honestly significant difference) for multiple comparisons
was performed to estimate the variation between the different means of
fixed and random factors on sampled mosquitoes.
Mann–Whitney test of two independent samples was used to compare
the number of mosquitoes caught by the CDC light traps and those caught
by the BRBs with different mixtures of sugar and yeast. Effects were con-
sidered to be significant when P < 0.05.
1.2.7 Ethical consideration
The study was approved by the Tropical Pesticides Research Institute
and Kilimanjaro Christian Medical College of Tumaini University Research
Ethics Committees. Head of households were made aware of the study ob-
jectives and provided written consent in order to participate in this study.
1.3 Results
1.3.1 Sampling of mosquitoes and species identifications
A total of 17,664 mosquitoes were sampled using the different methods
described. Among these, 17,663 (99.99%) were females while 1 (0.01%) was
a male. Of the samples, 77.7% (n = 13,718) were An. gambiae s.l, and 22.3%
(n = 3946) were Cule. quinquefasciatus.
Abdominal conditions of female mosquitoes sampled by all methods
were as follows, unfed had An. gambiae s.l 15,201 (86.15%) and Cx. quinque-
fasciatus 1154 (6.54%) fed mosquitoes were An. gambiae s.l 178 (1.01%) and
Cx. quinquefasciatus 7 (0.04%), semi gravid were An. gambiae s.l 783 (4.44%)
and gravid were An. gambiae s.l 321 (1.82). No Cx. quinquefasciatus were
found with semi gravid and gravid abdominal status.
1.3.2 Comparison of sampling efficiency of CO2 BRBs and
UBRBs
Mean densities of mosquito catches by the BRB trap was significantly
higher compared with the URB when used for outdoors sampling (P < 0.001)
(Table 2). Similar result was obtained when the traps were paired for indoors

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 14 Volume 01 / Issue 01 / March 2013 Global Health Perspectives

Table 2.  Comparison of mosquito sampling efficiency of CO2-baited and unbaited resting boxes (both indoors and outdoors).
    Indoor Outdoor

    Mean density ± SE   Mean density ± SE  

Mixture No. Mixtures CO2 baited Unbaited P CO2 baited Unbaited P

1 Yeast 17.5 g + sugar 250 g 1.96 ± 0.19 0.30 ± 0.19 <0.001 1.80 ± 0.17 0.74 ± 0.12 <0.001

2 Yeast 17.5 g + sugar 500 g 1.82 ± 0.17 0.52 ± 0.07 <0.001 1.22 ± 0.13 0.48 ± 0.09 <0.001

3 Yeast 17.5 g + sugar 750 g 1.58 ± 0.17 0.38 ± 0.07 <0.001 1.46 ± 0.17 0.60 ± 0.07 <0.001

4 Yeast 35.0 g + sugar 250 g 1.72 ± 0.17 0.56 ± 0.07 <0.001 1.18 ± 0.11 0.20 ± 0.06 <0.001

5 Yeast 35.0 g + sugar 500 g 1.98 ± 0.18 0.24 ± 0.06 <0.001 1.26 ± 0.13 0.24 ± 0.06 <0.001

6 Yeast 35.0 g + sugar 750 g 1.78 ± 0.22 0.64 ± 0.07 <0.001 1.46 ± 0.17 0.12 ± 0.07 <0.001

sampling and this was observed among the six combinations of sugar and
yeast cultures (P < 0.001) (Table 2). However, when the efficacy of the differ-
ent mixtures of sugar and yeast in attracting and catching mosquitoes was
compared, no significant difference was found among the means of the dif-
ferent doses (P = 0.840). Therefore, the cheap effective mixture should be of
the lower concentration of 17.5 g of yeast plus 250 g of sugar for the indoor
and outdoor collection. The highest dosage, i.e., 35.0 g of yeast plus 750 g
of sugar, for sampling had no significant difference between outdoor and
indoor samplings (P = 0.176) (Table 3).
1.3.3 Comparison of sampling efficiency of CDC light trap,
CO2 BRBs and UBRBs in a room
The mean densities of mosquitoes sampled by the CDC light traps, the
BRB, and the URB in the same room were significantly different (P < 0.001).
While BRB samples significantly had high number of mosquitoes (4.8-folds)
Table 3. Comparison of mosquito sampling efficiency of
CO2-baited resting boxes (both indoors and outdoors).
Mean density ± SE
Mixture
Indoors Outdoors
No
over UBR, it was still 9.5-folds lower than CDC light traps (Table 4). However,
this comparative efficiency of mosquito sampling by the different traps
was not affected either by days (P = 0.515) or by the location of house
(P = 0.345), but was influenced significantly by both the trap type (P < 0.001)
(Figure 4) and the amount of CO2 released (P = 0.014) (Figure 5). It was also
clear that the efficacy of CDC light trap and BRB, which were compared in
the same room, differed significantly among the different dosages used of
yeast and sugar mixtures (Table 5). Overall and irrespective of species and
location being indoor or outdoor, 15,656 (88.6%), 1663 (9.4%), and 345 (2.0%)
of mosquitoes were sampled by CDC, BRB, and URB traps, respectively. This
difference was statistically significant among the three methods with
CDC light trap being the most efficient method in collecting mosquitoes
(F = 192.23, df = 2, P < 0.001).
1.3.4 Discussion
In this study, we assumed that among the kairomones released by ­human
body that can attract mosquitoes, CO2 is the strongest agent available
(Dekker & Takken, 1998; Jawara et al., 2011; Smallegange et al., 2010; Takken &
Knols, 1999; Turner et al., 2011). Abdominal conditions of mosquitoes col-
lected in the present study can further confirm that among all the mosqui-
toes collected, the highest proportion collected (92.69%) was unfed host-
seeking mosquitoes. This high proportion of unfed mosquitoes collected
P

1 Yeast 17.5 g + sugar 250 g 1.96 ± 0.19 1.80 ± 0.17 <0.001 Table 4.  Proportions of mosquito sampled by each sampling
method used during the study period.
2 Yeast 17.5 g + sugar 500 g 1.82 ± 0.17 1.22 ± 0.13 <0.001 Trapping An. gambiae Cx.
Total
tool s.l quinquefasciatus

3 Yeast 17.5 g + sugar 750 g 1.58 ± 0.17 1.46 ± 0.17 <0.001 CDC miniature
79.23% (12,404)* 20.77% (3252) 100% (15,656)
Light trap†

Unbaited resting
4 Yeast 35.0 g + sugar 250 g 1.72 ± 0.17 1.18 ± 0.11 <0.001 85.22% (294) 14.78% (51) 100% (345)
Boxes

CO2-baited
5 Yeast 35.0 g + sugar 500 g 1.98 ± 0.18 1.26 ± 0.13 <0.001 61.33% (1020) 38.67% (643) 100% (1663)
resting boxes

6 Yeast 35.0 g + sugar 750 g 1.78 ± 0.22 1.46 ± 0.17 0.176 * The number in parentheses shows the total mosquito collected in study period.
†
Light trap was not baited with CO2.

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 Global Health Perspectives Volume 01 / Issue 01 / March 2013 15

1.60 suggests that, sampling using CDC light trap can be a good method for
­ ffective detection of disease transmitting mosquitoes and species com-
e
Mean density per trap per night

position (Dia et al., 2005; Kweka & Mahande, 2009; WHO, 1975). Fully blood-
1.20 fed mosquitoes are not expected to be attracted by host odours. They can
(transformed log (n +1)

only be attracted if they are partially blood fed at the first instance (Day,
2005). However, the proportions of males caught in the present study were
0.80 highest in the BRB. They might have been attracted by other by-products of
yeast-fermented sugar because males feed only and mostly in flower nec-
tarines (Foster, 1995; Foster & Takken, 2004; Gary et al., 2009).
0.40 In general, the efficiency of BRB in trapping mosquitoes indoor and out-
door depends on environmental factors such as wind and rainfall, i.e., high
wind speed dilutes the concentration of CO2 in BRB to levels undetectable
0.00
by mosquito plumes, whereas rainfall restricts the flight of mosquitoes
BRB URB CDC trap
outdoors (Dekker & Carde, 2011; Kweka & Mahande, 2009). In this study, sig-
Traps nificantly low densities of outdoor-resting mosquitoes were observed. This
perhaps, required more significant amounts of CO2 to be released in order
Figure 4.  The mean variation of mosquito densities sampled by the CDC to obtain a reliable number of outdoor-resting mosquitoes. The number of
light trap, unbaited resting boxes (URBs), and CO2-baited resting boxes mosquitoes caught by indoor BRB was 1.2-folds compared with their coun-
(BRB) in a room. terparts outdoors. Similar scenario was found in resting boxes baited with
cow urine (Kweka et al., 2010).
The BRB and URB were located 15 m away from human houses. Hence,
An. gambiae s.l Cx. quinquefasciatus
CO2 released was considered to be within the medium range for mosquito
1.2 antennae plume stimulant during host searching (Gillies & Wilkes, 1982;
Mboera et al., 2000). The incorporation of CO2 in trapping system elsewhere
Mean density/trap/night

has proved to increase mosquito catches using the sampling tools (Mboera
(log transformed)

0.8 et al., 2000). The inclusion of CO2 in resting boxes increased the mosquito
catches relative to unbaited control boxes. This accounts for higher
­efficiency of BRB compared with URB. The use of traps baited with CO2
0.4 was reported to be efficient in the laboratory, semifield, and field settings
studies using MM-X traps baited with CO2 from sugar-fermented yeast
(Smallegange et al., 2010).
0.0 However, the lesser number of mosquito catches in the BRB than the CDC
170 300 190 250 340 360 light trap is a major drawback in the sampling tool design for replacing
CO2 Volumes in mL/minute the traditional human landing catch practices for sampling malaria vectors,
which will reduce the risk to human volunteers without compromising on
Figure 5.  Density variations of mosquitoes in CO2-baited resting boxes for ethical considerations in African countries (Kilama, 2009, 2010). BRB could
different volumes of CO2 produced from sugar-fermented yeast. not show efficiency in sampling ability of higher densities that can provide
more information with regard to indoor malarial transmission scenarios
than the CDC light trap. This could be relevant only in lower income com-
munities where the disease burden is higher if BRB could perform better
Table 5.  Sampling efficiency of CDC light trap versus CO2-baited than the CDC light trap (Gallup & Sachs, 2001). However, the overall perfor-
resting box in a room by comparing the total mosquitoes mance of BRB was 9.55-folds lower than CDC light traps. Similar trends have
sampled by each. been shown in a previous study carried out in the same area during the
same dry season, when clay pots were compared against CDC light traps
Mosquitoes mean ranks
for vector sampling (van den Bijllaardt et al., 2009).
Amount The current technique used for BRB includes release of CO2 through a
CDC plastic tube connected with a plastic container of fermentation culture
Mixture of CO2 gas Z
light CO2-baited box P
No. released test of yeast and sugar. The findings presented for this technique showed poor
trap*
(mL/min) ­efficiency of BRB in sampling mosquitoes, not only when compare with
CDC light trap but also with the boxes baited with fresh and ageing cow
1 170 73.43 27.57 –7.96 <0.001
urine (Govella et al., 2011; Kweka et al., 2009; Kweka et al., 2010; Mahande
2 300 74.70 26.30 –8.37 <0.001 et al., 2010). This provides an opportunity to develop alternative technique
for these boxes as community tools for sampling malarial and nonmalarial
3 190 74.66 26.34 –8.36 <0.001
vector mosquitoes. This concludes that the used technique of baiting in
4 250 73.57 27.43 –7.97 <0.001 BRB with carbon dioxide is not a worthy tool for community sampling
as it is not reliable and efficient in sampling mosquito vectors. Moreover,
5 340 75.50 25.50 –8.64 <0.001 the technique is relatively expensive in term of resources used as com-
6 360 75.09 25.91 –8.52 <0.001
pared with mosquitoes sampling using cow urine in different ageing days
(Kweka et al., 2010; Kweka et al., 2011). This is due to the fact that cow urine
* CDC light trap was not baited with CO2. is available for free and does not cost anything like sugar and yeast .

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 16
1.4 Conclusion
We conclude that the BRB cannot be used as a human exposure free
tool to catch mosquitoes due to its low sampling efficiency and higher
operational costs. Better trapping techniques using kairomones should be
­designed and optimized.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
E.J.K. conceived; designed the experiments and performed data analysis.
E.J.K. and Y.E.H. wrote the paper and revised the manuscript critically. M.C.L.
Y.E.H., A.M.M., A.D., F.M., M.N., E.O., E.J.K., J.R.M. revised the manuscript. All
­authors approved the final version for submission.
1.5 Acknowledgements
The authors wish to acknowledge Augustine Mtui and Charles Massenga
for experiment supervisions and identification of mosquitoes during
field work conducted in the Lower Moshi region of Northern Tanzania.
The continued support of the house owners and community in general is
­appreciated. This study received financial support from Tropical Pesticides
Research Institute.
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