4. DISCUSSION
Previous studies undertaken in Burkina Faso established that the use of
pesticides against crop pests, especially for cotton protection,
contributes to the selection of insecticide resistance in malaria vector
mosquitoes (Diabate et al. 2002, Gnankiné et al. 2013, Hien et al.
2017).
This original study aims to provide the impact of introduction of a new
method of cotton cultivation, transgenic cotton, that is expected to
reduce the amount of insecticides and the number of their treatments
used against the pests of this crop (Gnankiné et al. 2018) compared to
pre-existing cotton cultivation technologies, essentially conventional
and to a lesser extent organic, on the insecticide susceptibility ofAnopheles mosquitoes. This study represents a great opportunity
to further our knowledge on the effect of cotton growing systems on the
insecticide resistance dynamics of the main malaria vector mosquitos,
belonging to the An. gambiae complex, in connection with the
eco-climatic regions of Burkina Faso.
Consecutive years of intensive use of chemicals in both agriculture and
public health have led to the selection of resistant pests and vector
populations as observed for An. gambiae in Burkina Faso (Gnankiné
et al. 2013). Previous studies have also showed the presence of
resistance in the tomato bollworm Helicoverpa armigera to
Pyrethroids (Martin et al. 2000, 2005, Raj et al. 2002), the whiteflyBemisia tabaci to Pyrethroids, Organophosphates and
neonicotinoids due to intensive use of PY and OP for crop protection
(Gnankiné et al. 2013).
In regard to this situation, the cotton strategy has been modified in
conventional cotton growing areas that consisted in reduction of PY and
OP use and re-introduction of endosulfan insecticide (Martin et al.
2005). At the same time, nationwide surveys have shown phenotypic and
genotypic resistance of An. gambiae s.l populations to PY and OP
in agricultural settings including cotton growing areas in central and
western Burkina Faso (Chouaïbou et al. 2016, Chabi et al. 2018).
In 2008, genetically modified cotton plants expressing both Cry1Ac and
Cry2Ab toxins were implemented in Burkina Faso (Gnankiné et al. 2018).
For transgenic cotton, pesticides belonging to the OP and PY families
are not used in fields but pesticides from neonicotinoids class are used
at the end of the cotton phenological stages (Gnankiné et al. 2018). As
far as species of the An. gambiae complex concerned, An.
gambiae s.s , An. coluzzii and An. arabiensis were
identified and the cotton pest strategies do not affect the distribution
of these species. Moreover, according to the previous studies
investigated in the same climatic zones, the geographical distribution
of these species did not change over the past 10 years (Diabate et al.
2004, Dabiré et al. 2012).
In this current study, the proportions of An. gambiae s.l.
complex populations in Burkina Faso shows that An. gambiae s.spredominates in the west and southwest parts of the country and still
lives in sympatry with An. coluzzii in proportions of 70% and
30% respectively. In central and east-central parts, An.
coluzzii was prevalent and was found in sympatry with An.
arabiensis, being most frequent in the northwest and east-central part
of the country with frequencies between 16.7% and 51.5%.
Human activities leading to the creation of permanent streams and ponds
have also favoured the emergence of An. coluzzii, a
species typical of irrigated areas (Pages et al. 2007) as reported in
the current study in the rice growing area of the Vallée du Kou. So far,An. arabiensis has changed in Soumousso (rural area) where its
proportion has increased significantly in recent years (Namountougou et
al. 2019) compared to the present study (from 2008 to 2014) during the
same sampling period (e.g. rainy season). The expansion of An.
arabiensis in this locality is attributed to global ecological changes
(such as climate change) or local human activities (such as
deforestation) that promote the colonization of this species.
Our phenotypic data exhibited resistance to DDT and permethrin (from
2008-2009) as well as deltamethrin (2008-2014) in all populations ofAn. gambiae s.l. sampled regardless of cotton pest control. The
situation is quite different with Bendiocarb. Although resistance to
this insecticide has been observed in populations collected in
conventional growing areas, the level of susceptibility appears to have
been partially restored from 2009 to 2014 at Dano (organic cotton area)
and completely restored in Fada N’Gourma (transgenic cotton area) where
the mortality rate recorded by bioassays has increased from 90 to 100
%.
The first studies on the resistance of An. gambiae s.l. to
pyrethroids in West Africa and more particularly in Burkina Faso began
in the late 1990s when Chandre et al. (1999) reported cross-resistance
to permethrin and DDT in An. gambiae s.l. populations (but these
populations were then susceptible to deltamethrin) in south-western
Burkina Faso. Three years later, this resistance was subsequently
confirmed by the works undertaken by Diabaté et al. (2002) in several
parts of the country. Other studies covering different regions of the
country have shown that the kdr L1014F mutation is the main
mechanism involved in cross-resistance to DDT and pyrethroids inAn. gambiae s.l. populations from Burkina Faso. This resistance
mechanism was detected firstly in An. gambiae s.s and thenAn. coluzzii inherited it by genetic introgression from An.
gambiae s.s (Diabate et al. 2004). Recent phenotypic and genotypic
analysis have shown that resistance to both DDT and pyrethroids is now
widespread among the three species of the An. gambiae complex
occured in Burkina Faso (Dabiré et al. 2014, Hien et al. 2017). These
malaria vectors, although present in sympatric in most of areas, have
divergent ecological preferences and behaviours (Diabaté et al. 2008,
Coulibaly et al. 2016). Thus, An. Arabiensis,, due to its
exophagic and exophilic biting behaviours, would spare to the selective
insecticide pressure from the main vector control tools (essentially
LLINs) as exerted on An. gambiae s.s and An. coluzzii .
Beyond the use of insecticides in public health, particularly through
LLINs, the use of insecticides in cotton growing areas also favoured the
emergence of this cross-resistance to DDT/pyrethroids in An.
gambiae s.l. populations (Diabate et al. 2002). This causality may be
explained by intense and permanent selection pressure throughout the
rainy season, that is exerted on the entire mosquito population at the
larval stage in breeding sites and not only on the proportion of biting
females. In fact, an increase of insecticide resistance in mosquito
vectors was observed during insecticide treatments periods in cotton
growing areas (Dabiré et al. 2012). However, by comparing the
frequencies of kdr L1014F by cotton growing area (transgenic,
organic and conventional), no significant differences were found during
the four years follow-up, except in the transgenic cotton growing
area in 2008 and 2013. Indeed, a slight reduction in the frequency of
the kdr L1014F mutation in this area was detected (from 0.6 to
0.45 in An. gambiae s.l. between 2009 and 2013) coupled with the
bednet campaign. This reduction should improve the susceptibility ofAn. gambiae s.l. to both DDT and pyrethroids as the kdrL1014F mutation is known to be the main mechanism of crossed resistance
to DDT/pyrethroids. Unfortunately, this reduction was observed during a
very short period of time since an increase of the frequency of thekdr L1014F mutation was immediately observed the following
year (2014). The high levels of pyrethroids resistance in malaria
vectors maintained in transgenic and organic cotton growing areas, both
characterized by low insecticide use, are believed to be due to the fact
that the kdr alleles are widespread in all areas of southern and
central Burkina Faso and almost fixed. If the kdr mutation is
fixed, its frequency will not vary even though the selection pressure of
pyrethroid treatments in cotton fields decreases due to its low genetic
cost; except in the case of a large influx of migrants who can bring new
genetic variants, which seems unlikely given its expansion throughout
the West African region.
Moreover, the transgenic and especially organic cotton fields
investigated are close to conventional cotton growing areas, or even
vegetable areas where agricultural insecticide applications are also
practiced. Insecticides residues from conventional or vegetable areas
can retain significant selection pressure on neighboring An.
gambiae sl populations. Furthermore, it is not excluded that some
cotton farmers by fear of seeing developing some secondary pests not
targeted by transgenic Bt , treat in secret their fields by OP and
PY chemicals except those recommended by the technical route.
In addition to molecular resistance mechanism (target site
modification), other mechanism of insecticide resistance like metabolic
resistance may be involved in Anopheles s.l. populations wherekdr gene was almost fixed as shown recently by Namountougou et
al. (2019). These authors found that most of populations of An.
gambiae s.s from cotton growing areas (Conventional cotton) of western
part of Burkina Faso exhibited high level of GSTs and NSEs enzymes with
a level of enzymes might vary in connection with cotton growing areas.
This resistance status is worrying as cotton farmers are heavy consumers
of insecticides that have been and continue to be used at large scale in
the country that may have an negative impact on the vector control
strategies based on insecticides applications (LLINs or IRS). This
situation of insecticide resistance requires regular annual monitoring
for a better vector control management. This could already lead to
predict a possible temporal rotation of the insecticidal classes,
especially in IRS, but also the need to find new insecticides or
innovative methods to prevent and control vector-borne diseases as
recommended by WHO (WHO 2012, 2019).