1 Introduction
Climate change and infectious disease present some of the greatest challenges of our age. Their devastating impacts are increasingly clear (McMichael 2013), and have potential to impact every aspect of life including ecosystem function, human and veterinary health, food security, economic and political stability. While the independent impacts of climate change and infectious disease are sizeable; the greatest threats may arise from their interaction whereby the occurrence of one directly impedes ability to address the other.
We hypothesize this scenario is highly likely to arise in the context of mosquito vector-borne diseases (VBD s). VBD s such as malaria are a leading source of mortality and morbidity within Low and Middle Income Countries. Amongst the VBD s, malaria has the largest mortality burden; causing 627,000 deaths in 2021 alone (WHO 2021). This burden is disproportionately concentrated in sub-Saharan Africa where more than 96% of malaria-related deaths occur; mostly in young children under 5 years old (WHO 2021). While the upscaling of vector control interventions including Insecticide Treated Nets (ITN s) and Indoor Residual Spraying (IRS) have significantly contributed to the halving of malaria prevalence in Africa since the year 2000 (Bhatt et al. 2015), this disease still poses an unacceptable public health burden. Of particular concern, progress towards elimination has stagnated in recent years; with malaria prevalence and mortality staying level or even increasing in some African countries since 2015 (Noor and Alonso 2022). The causes for this slow down are complex, but likely principally driven by a combination of biological challenges such as insecticide resistance and outdoor biting in malaria vectors, and reduced investment, economic constraints, and disruption due to COVID (WHO 2018, Lindsay et al. 2021, Weiss et al. 2021, Sherrard-Smith et al. 2019).
Numerous studies have demonstrated that malaria transmission is highly sensitive to climate (e.g. (Kelly-Hope and Thomson 2005, Mabaso et al. 2007, Caminade et al. 2014, Reiner et al. 2015, Fall et al. 2022)). This dependency arises because the survival, reproduction and behaviour of the major African malaria vectors (Anopheles arabiensis, An.coluzzii, An. gambiae and An. funestus) are highly sensitive to environmental conditions such temperature, humidity and rainfall (Afrane et al. 2012, Charlwood 2019; Parham et al. 2012). Also, malaria parasite development within vectors is temperature dependent (Paaijmans and Thomas 2013). Notably, temperature influences almost all mosquito life-history (Christiansen-Jucht et al. 2015, Agyekum et al. 2021) and demographic processes (Parham et al. 2012). The sporogonic success (development of infectious stages) of malaria parasites within vectors is also temperature dependent; with the length of the extrinsic incubation period decreasing with temperature up to a maximum threshold beyond which sporogony fails (Beier 1998; Murdock et al. 2016). The environmental dependencies of these key mosquito vector and parasite processes make malaria transmission highly likely to change with climate.
While the potential impacts of climate change on malaria have received much attention (Martens et al. 1999, Tanser et al. 2003, Thomas 2004, Gething et al. 2010, Ermert et al. 2013, Yamana and Eltahir 2013, Caminade et al. 2014, Diouf et al. 2021), there is another crucial question that has been largely overlooked: how effective will malaria vector control and elimination strategies be under modified climates? Here we hypothesize that the efficacy and ability to implement core vector control interventions for malaria could be significantly reduced by climate change due to direct and indirect impacts on mosquito vectors and interventions. If confirmed, such climate-mediated impacts could slow or even reverse progress towards malaria elimination even as the geographical area suitable for transmission in Africa may fall. To explore the potential for such a scenario, we first briefly review knowledge on how climate is expected to change in Africa, and its potential impact on transmission.
1.1 Future climate change predictions for Africa
While the effects of climate change will be global, it is hypothesized that sub-Saharan Africa is particularly vulnerable to severe and catastrophic impacts due to extreme reliance on small-scale rain-fed agriculture, socio-economic constraints and other factors (Connolly-Boutin and Smit 2016). Many studies have attempted to characterize and forecast the types of climate change anticipated in different regions of Africa; with predictions often varying between regions. Such predictions are generally derived from fitting a range of different Global Circulation Models (GCM s) to a series of Representative Concentration Pathways (RCP s) as proposed by the Intergovernmental Panel on Climate Change to reflect plausible future greenhouse gas emission scenarios (IPCC 2020). Key outputs of such forecasts are expected temperatures and precipitation patterns.
It is expected that temperatures in southern Africa may rise faster than the global average; generating a much higher frequency of heatwaves and droughts (Chersich et al. 2018). For example, a model developed for the Eerste River in South Africa predicted that climate change in the ‘near’ (2022–57) and ‘far’ (2058–2093) future will increase evaporation and decrease rainfall by 2% and 8% respectively, leading to a reduction in water availability between 8–18% (Du Plessis and Kalima 2021). Similar modelling of the hydrology of the Kabombo sub-basin within the Zambezi Basin indicates that stream flow will become much more variable; and decrease by up to 3% even under intermediate scenarios (RCP 4.5) (Ndhlovu and Woyessa 2021). Thus the overall assessment for southern Africa is much warmer and drier conditions.
Predicted impacts of climate change are more variable across the East African region. Specifically, predictions of the magnitude and direction of climate impacts vary somewhat between different GCM and RCP scenarios. Many East African countries are already classified as ‘water stressed’, and are expected to become increasingly so as climate changes. For example, per capita water availability is expected to fall below scarcity levels in Ethiopia, Kenya, Malawi, Mozambique, Rwanda, Uganda, Tanzania and Zambia by the end of the century (Adhikari et al. 2015). This is based on predictions of temperature rises between 0.9–3.4 °C by the 2060s, and 1.3–5.5 °C by 2090s (Adhikari et al. 2015). However, there is some discrepancy between predictions depending on the modelling approach, focal area and scale applied. One study of future rainfall over the Lake Victoria region of East Africa predicted no significant change in mean monthly rainfall by the 2040s, and only a slight increase by 2075 (Akurut et al. 2014). While changes to precipitation across East Africa may be locally variable, there is consensus that temperatures will rise.
Analysis of time series data from the in Sahel region of west Africa indicate there has already been a substantial long-term decline in rainfall and increasing temperature between 1970–2000 (Ben Mohamed 2011). The ability to predict future climate is uncertain given some existing models do not fit well to historical data (Ben Mohamed 2011). However mean temperatures are expected to rise by at least 1–1.5 °C in the medium term (Amoussou, Awoye et al. 2020, Diedhiou, Bichet et al. 2018), and potentially considerably more in some areas (Chou et al. 2020). Predictions about rainfall are more variable, but there is an expectation of substantial alterations in frequency, seasonal duration and intensity of precipitation. For example, daily extremes in rainfall are expected to rise in the Mono Basin in Togo (Amoussou et al. 2020). More heatwaves of longer duration are predicted throughout the region, but with an intensification of rainfall in some areas and considerable drying and increase in drought conditions in others (Diedhiou et al. 2018). General trends and differences are evident between the four agro-ecological zones in Sahel region (UNHCR 2022). Higher temperature increases are projected for arid and semi-arid zones in the North compared to subhumid and tropical zones. However the subhumid and semi-arid zones will experience the largest increase in the proportion of ‘very hot days’ (e.g. temperature >35 °C, UNHCR 2022). Finally while the number of heavy precipitation days will decline in the northwest, pronounced increases are expected in the eastern Sahel (e.g. Northern Chad, Niger, Nigeria and Cameroon). Although predictions for specific regions are variable, substantial changes to climate are expected across the continent as whole; characterized by rising temperature, substantial shifts in rainfall and a higher frequency of extreme weather events.
1.2 Predicted impacts of climate change on malaria in Africa
The potential impacts of climate change on malaria in Africa have been investigated for more than 20 years (Martens et al. 1999, Tanser et al. 2003). Early work focussed on the use of biological models to estimate the geographical area suitable for malaria transmission based primarily on temperature requirements of mosquitoes and parasites (Martens et al. 1999). Such models predicted that climate change would lead to substantial increases in malaria distribution and people at risk. For example, one model estimated that approximately 300 and 150 million more people would be a risk of P. falciparum and P. vivax respectively by 2080 due to climate change (Martens et al. 1999). However, these models were subsequently questioned due to their failure or incomplete incorporation of other key environmental drivers of transmission (e.g. rainfall). Later work using more complex spatiotemporal models predicted less dramatic changes to the African malaria map; with little change predicted in the latitudinal range, but altitudinal increases (Tanser et al. 2003). This and other work indicated a more complex pattern of epidemiological impacts; including predictions of significant reductions in transmission in some parts of sub-Saharan Africa (Thomas 2004, Thomas et al. 2004, Lafferty 2009, Gething et al. 2010, Ermert et al. 2013). The need to incorporate more detailed consideration of related changes in land use, urbanization and socioeconomic factors has also been highlighted (Gething et al. 2010, Yamana and Eltahir 2013, Caminade et al. 2014).
Recent models have attempted to incorporate greater complexity and detail on the specific nature of metereological changes. Early models based on simplified assumptions and generalization of rainfall effects have been replaced by more sophisticated approaches based on explicit consideration of hydrology (e.g. water flow, concentration and evaporation across landscapes), land use change, and with predictions made at a finer scale. Such models have reinforced the prediction that increasingly warmer and drier conditions will reduce the length of the malaria transmission season in West Africa, but will increase the risk of highland malaria in East Africa (Alonso et al. 2011, Ermert et al. 2013, Caminade et al. 2014, Leedale et al. 2016, Yamana et al. 2016, Diouf et al. 2021). As an an example, one study in the Western Ugandan Highlands found that that extreme flooding was associated with a 30% increase in the risk of a person having a positive malaria test (Boyce et al. 2016); highlighting the additional risk expected in areas where climate change is expected to increase these events.
In combination, this body of work indicates that the geographical area in which malaria transmission can occur in Africa is unlikely to significantly expand due to climate change; with substantial contractions possible in some areas. However, most models so far have primarily focussed on the direct biological impacts of climate change on parasites and vectors, and not the wider impacts on control activities and health systems. Consideration of these factors may give a very different perspective on how the public health impact of malaria will respond to climate change. As highlighted by (Mordecai et al. 2020), the primary public health impact of climate change on VBD s may arise not through expansions of the ‘malaria map’, but increased exposure within stable areas of transmission. One economic analysis suggested the cost of in patient treatment for malaria as a proportion of annual health expenditures per 1,000 people could rise by up to 20% within some African countries (Egbendewe-Mondzozo et al. 2011). Whether detrimental impacts of this magnitude or greater will arise will ultimately depend on if and how climate change will impact the efficacy and ability to implement surveillance, control and treatment.
2 Impacts of climate change on vector ecology and transmission ability
2.1 Importance of temperature to vector fitness and transmission potential
Climate change is expected to alter the distribution, abundance and species composition of African malaria vectors because their reproduction, survival, behaviour and pathogen transmission capacity are highly sensitive to environmental conditions. Notably, temperature influences almost all mosquito life-history (Christiansen-Jucht et al. 2015, Agyekum et al. 2021) and demographic processes (Parham et al. 2012). Temperature effects are often curvilinear – with a fitness trait or demographic rate increasing with temperature up to maximum followed by a rapid decline (Agyekum et al. 2021). For example, the speed of larval development in the laboratory accelerates with temperature; with development period of An. gambiae sl. being ~10 days shorter at 36 °C compared to 25 °C. However, development is significantly impaired at higher temperatures, with no larvae surviving at >38 °C (Bayoh and Lindsay 2003, Bayoh and Lindsay 2004, Agyekum et al. 2022). At the adult stage, survival, fecundity and the length of the gonotrophic are reduced at high temperatures (Agyekum et al. 2021). Climate change is expected to increase not only mean temperatures across Africa, but also variability in daily temperatures. Increased temperature variability is difficult for ectotherms to cope with (Paaijmans et al. 2013); and may further impair population viability under climate change.
Rising temperatures may also affect the susceptibility and competence of vectors to malaria infection. The sporogonic success of malaria parasites is temperature dependent; with the length of the extrinsic incubation period (EIP) decreasing with temperature up to a maximum threshold beyond which sporogony fails (Ohm et al. 2018). For example, models fit to laboratory data indicate that the EIP of P. falciparum in An. stephensi falls from 16.1 to 8.8 days as temperature rises from 21 to 34 °C (Stopard et al. 2021); with no sporogonic development above 35 °C (Shapiro et al. 2017). Experimental studies indicate that temperature rises as expected under climate change will decrease the vectorial capacity of An. gambiae by reducing parasite sporogonic success. Laboratory experiments on An. gambiae and An. stephensi indicated that their vectorial capacity could be reduced by 51–89% with increases in mean temperature from 27 to 30 °C (Murdock et al. 2016). Furthermore, experimental studies show that Anopheles immune responses that might impair parasite development are also temperature dependent (Murdock et al. 2013, 2014). Taken together with projected impacts on mosquito demography, this suggests that temperature increases as expected under climate change will have complex and diverse impacts on malaria vector ecology and transmission potential.
While temperature rises will certainly influence malaria transmission, the specific nature of these impacts will vary between settings depending on whether they move local conditions either into or above the optimal threshold for mosquitoes and/or parasite development. Additionally, the effect of temperature may be offset or mitigated by concurrent changes in rainfall. As reviewed above, climate change may lead to much heavier rainfall and flooding in some areas of Africa, and considerable drying and drought conditions in others. Such changes could, for example, boost mosquito populations even in areas where temperature ranges were approaching the upper threshold for their survival. Additionally, the moving of climatic conditions into the optimal temperature range for sporogony may have little impact on transmission if this is accompanied by substantial drying and reduction of habitats for mosquito oviposition. In summary, while temperature will certainly play a crucial role in determining how malaria transmission will be altered by climate change; it’s impacts must be evaluated within the wider context of concurrent conditions.
2.2 Impact of climate change on malaria vector species composition
Whilst all African malaria vectors will be exposed to climate change, impacts will likely vary between species due to differences in their innate habitat preferences and physiological tolerances. In addition to the four primary native African vector species (An. arabiensis, An. coluzzii, An gambiae and An. funestus), the major Asian malaria vector An. stephensi has now been detected in the Horn of Africa (Sinka et al. 2020). All of these vector species differ in ecology, behaviour and environmental adaptations in ways that could modulate their response to climate change (Table 1). First, changes to rainfall and humidity are likely to favour some vector species over others. This could arise through interspecific variation in physiological tolerance such as resistance to desiccation and capacity to store water being favoured (e.g. Table 1). It has been hypothesized that variation in these physiological traits explains why An. gambiae are more likely to be found in wet, saturated environments, and An. arabiensis in drier environments (Lindsay et al. 1998). Additionally, shifts in species composition could arise due to changes in the availability and diversity of aquatic larval habitats under climate change. Typically An. gambiae prefers to use small, temporary aquatic habitats for oviposition, while An. funestus is associated with larger and more permanent habitats (Kahamba et al. 2022). The invasive An. stephensi prefer artificial container habitats in urban settings (Sinka et al. 2020). In areas where climate change leads to drying, An. funestus, and An. stephensi may have an advantage because their larval habitats are most likely to persist (the former because it uses larger and more stable habitats and the latter because people may increasingly store water around houses when rainfall is limited). In contrast, a proliferation of small, temporary puddles in areas where climate change increases rainfall may benefit An. gambiae.
Changes in vector species composition due to climate change will also be determined by the extent of temperature rise. Anopheles arabiensis is generally considered better adapted to survival at high temperatures and more resistant to desiccation than An. gambiae (Table 1). Anopheles funestus may have similar or higher capacity to endure high temperatures than An. arabiensis (Table 1). Few studies have directly compared the environmental tolerances of native African vector species with that of the invasive An. stephensi; probably because until recently they did not co-occur in the wild. However, a recent model based on data from seperate experiments suggests An. stephensi has a higher temperature optimum than An. gambiae (Villena et al. 2022), and is considered better adapted to warmer temperatures than An. gambiae (Mordecai et al. 2020).
Differences in thermal tolerances of current (An. arabiensis, An. coluzzi, An. gambiae and An. funestus) and recently invasive (An. stephensi) malaria vector species in Africa
Of all African vector species, An. funestus may be the best adapted to dry conditions due to its longer persistence throughout the dry season, higher dessication resistance than An. arabiensis (Table 1) and additional adaptations such as aestivation which can facilitate survival through prolonged hot, dry periods (Charlwood et al. 2000, Huestis and Lehmann 2014). However An. stephensi is also likely to thrive in the warmer and drier conditions expected with climate change. In the Horn of Africa, this species has now been detected year round including in extremely hot months in Djibouti (Seyfarth et al. 2019). Additionally unlike native African vector species, An. stephensi is highly adapted to urban environments (Mordecai et al. 2020). Consequently the concurrent impacts of climate change and increasing urbanization (Section 5.2) may drive the expansion of this highly efficient vector across urban settings in Africa
In addition to variation in climate responses between vector species, there can also be substantial intraspecific variation in environmental tolerances between populations. Several studies have documented associations between dessication resistance and chromosomal inversions within African vector species (Gray et al. 2009, Fouet et al. 2012). This inter- and intraspecific variation in mosquito adaptations means that malaria vector communities under future climate change scenarios in Africa are likely to be radically different from those at present.
Several modelling studies have attempted to predict how the species composition and distribution of malaria vectors will respond to climate change in Africa (e.g. (Drake and Beier 2014, Tonnang et al. 2014, Akpan et al. 2019, Olabimi et al. 2021). Key themes have been assessment of whether there will be a major shift towards more ‘dry’ or ‘higher temperature’ adapted species. For example, climate change has been hypothesized to favour An. arabiensis within the An. gambiae s.l group because it is the best adapted to dry conditions (Drake and Beier 2014). As this species is more exophagic and zoophilic than other members of the group (An. coluzzii and An gambiae; Lyimo and Ferguson 2009), a shift in this direction could reduce the suitability of indoor interventions such as ITN s and IRS. However, a study using ecological niche modelling predicted that climate change will significantly reduce the distribution of An. arabiensis by 2050 (Drake and Beier 2014). Thus An. arabiensis may not expand its range with climate change but could become an increasingly prominent vector within remaining foci of transmission. In contrast, a more localized modelling study suggested climate change will increase the range and density of both An. arabiensis and An. gambiae s.s. in Nigeria; primarily by facilitating increased expansion of Sahel and Sudan savannas within northern States (Akpan et al. 2019). It may not be possible to generalize about the predicted nature of shifts in African vector composition with climate change, as this likely depends on national and sub-national ecology and geography.
2.3 Implications of changes in malaria vector species composition for control
The nature and extent of climate-driven changes in malaria vector species composition could have significant impacts on the efficacy of interventions. Of particular concern is the potential for changes that favour vector species, genotypes and/or at behaviours with reduced susceptibility to interventions. There is evidence that the impact of the core indoor interventions of ITN s and IRS varies between African vector species (Sinka et al. 2016). In particular, there has been extensive analysis of differences in the impacts of ITN s between highly endophagic and anthrophilic species like An. gambiae and An. funestus compared to the more zoophagic and exophilic An. arabiensis (Kiware et al. 2012, Kiware et al. 2012, Killeen 2014, Killeen et al. 2014). Modelling indicates that the magnitude of transmission reduction expected from ITN s varies substantially between these species on account of differences in their innate host preference, the presence of alternative hosts (cattle), and degree of outdoor biting (e.g. (Killeen 2014)). Such impacts are complex; while more zoophagic species like An. arabiensis have lower vectorial capacity than highly anthrophilic species, they are also harder to suppress with indoor interventions like ITN and IRS because their behaviour means they come into contact with them less frequently. These theoretical predictions have been empirically supported by combined analysis of data from intervention trials; confirming that An. funestus is most heavily impacted by indoor insecticide-based interventions, followed by An. coluzzii/gambiae and then An. arabiensis (Sinka et al. 2016). Even if the geographic range of An. arabiensis decreases with climate change ((Drake and Beier 2014), its potential dominance within remaining transmission settings could pose a challenge for current core interventions.
Finally, the impact of current interventions could also be eroded if An. stephensi continues to emerge and expand across African cities (Sinka et al. 2020). Like An. arabiensis, this vector is quite exophilic and exophagic (Sinka et al. 2020, Balkew et al. 2021), and often bites early in the evening (e.g. before 10 pm, (Reisen and Aslamkhan 1978)). These behaviours will like reduce the impact of indoor interventions including ITN s. If climate change enhances the establishment of An. stephensi, there will be a need to expand the focus of control activities from rural to urban settings. The need to invest and implement in additional supplementary control measures will ultimately depend on which vector species are favoured under future climate scenarios.
3 Environmental dependency of vector control interventions
Climate change could directly affect control by modifying the efficacy and quality of interventions. Such effects could arise through environmental dependencies that are additional to those created by local vector ecology and insecticide resistance, and instead due to variation in product performance in different climates. Here we consider the potential for such effects with current WHO-recommended core (ITN and IRS) and supplementary (larviciding) vector control interventions.
3.1 Insecticide treated nets and indoor residual spraying
Both ITN s and IRS work by targeting adult mosquitoes with insecticides inside houses. ITN s target adult females during host seeking, and IRS the females and males that rest indoors. Until recently, pyrethroids were the only class of insecticides approved for use on ITN s. Products based on pyrethroids, organochlorines, organophosphates, carbamates and neonicotinoids have been approved for IRS (WHO 2022). Whilst ITN s and IRS are recommended as core general interventions, there is considerable heterogeneity in their impact between African settings. For example, in recent trials the IRS compound Actellic (pirimiphos-methyl) was associated with an 88% reduction of An. funestus in Kenya (Abong’o et al. 2020) but only 48% reduction of the same species in Mozambique (Wagman et al. 2021). Such differences may be due to variation in insecticide resistance and local vector ecology, but could also be due to local environmental conditions that impact product performance, durability and residual efficacy. Currently, the World Health Organization pre-qualifies vector control products including insecticides and treated nets on the basis of submission of evidence demonstrating impact on target vectors within environmental conditions of intended deployment settings (WHO 2021). Whether similar efficacy and durability would be maintained under altered climatic conditions is unknown; and may vary between products and intervention classes. Studies from agricultural entomology indicate that the immediate and residual efficacy of some insecticide classes vary with temperature (Arthur 2013, Arthur et al. 2019) and humidity conditions (Ranabhat and Wang 2020, Gerken et al. 2021). As reviewed by (Sibanda et al. 2011), the stability of compounds used in IRS also varies with temperature, ultraviolet light and other environmental variables. Consequently it is reasonable to expect that environmental conditions contribute to local heterogeneity in vector control product efficacy; however the nature and epidemiological relevance of such effects are unknown. The WHO has highlighted investigation of the environmental contribution to vector control impact as a key priority for research, particularly in the context of mosquito behaviour and outdoor transmission (WHO 2022).
Variation in insecticide performance could be linked to temperature. As reviewed by Glunt et al. the toxicity of insecticides used in vector control often depends on ambient temperature (Glunt et al. 2013). This is hypothesized to be a function of temperature impacts on mosquito metabolism and nervous system function (Glunt et al. 2013). It has been further suggested that the standard temperatures used in WHO insecticide bioassays (25±2 °C for ITN s, and 27±2 °C for IRS) may overestimate the temperatures at which mosquitoes are exposed to these interventions in the field (Glunt et al. 2013). The impact of temperature on toxicity appears to vary between insecticides classes (Glunt et al. 2013, Glunt et al. 2014, Glunt et al. 2018), with some potentially increasing with warming conditions and others falling or remaining stable. A recent systematic review supports a trend of decreasing toxicity at higher temperatures (Agyekum et al. 2021); which could lead to a deterioration of efficacy with climate change. As highlighted by (Glunt et al. 2013), more explicit consideration of the temperature profile of insecticide products and their fit to the environment of deployment could help mitigate against this. As discussed (Section 5.1), these potential impacts of temperature on insecticides may interact below with the willingness of people to use interventions like ITN s. This interplay between direct and indirect impacts on product efficacy and use will determine the impact of these interventions in warming conditions.
3.2 Larviciding
Larviciding is the regular application of microbial or chemical insecticides to water bodies or containers to kill the aquatic immature stages of mosquitoes (larvae and pupae). Larviciding is widely accepted as a supplement to the core interventions or ITN s and IRS. Several malaria endemic countries in Africa are now implementing larviciding; motivated by the need to incorporate additional approaches that also target exophilic, early biting and pyrethroid resistant vector populations (Tusting et al. 2013). Several larvicide products are non-chemically based (e.g. the bacteria Bacillus thurigenesis), and thus not impaired by pyrethroid resistance. Evidence on the effectiveness of ground larviciding application for malaria control is well-established (Tusting et al. 2013, Derua et al. 2019). Notable examples include the use of the chemical Paris Green to eliminate Anopheles gambiae in Brazil and Egypt in 1940 and 1945s respectively (Soper and Wilson 1943, Shousha 1948), and a 90% reduction in malaria prevalence following larviciding in Sri-Lanka (Tusting et al. 2013). Despite this rich evidence base in support of this intervention, there has been limited consideration of how climate change may impact its impact and feasibility.
African malaria vectors spend between 7 to 27 days (Fillinger et al. 2003, Majambere et al. 2007, Ng’habi et al. 2010, Nartey et al. 2013, Ngowo et al. 2021) in aquatic habitats before transforming into terrestrial adults. During this period, larvae can be targeted by a range of methods including chemical insecticides, bacteria (e.g. Bacillus thuringiensis israelensis and bacillus sphaericus), surface oils and films, Spinosyns (metabolites extracted from the bacterium Saccharopolyspora spinosa) and insect growth regulators (e.g. novaluron and pyriproxyfen)(WHO 2013). These larvicides can be delivered through ground application (by hand or using conventional sprayers) or aerial application. Ground based larviciding is the most common delivery mechanism in sub Saharan Africa (Choi et al. 2019). The feasibility and impact of larviciding is highly environmentally dependent; and is recommended for use only in settings where larval habitats are ‘few’, ‘fixed’ and ‘findable’ (WHO 2022). There are several reasons why these criteria may be impacted by climate change. First, climate change will lead to heavy and prolonged precipitation and extensive flooding in some African settings. Ground delivery of larvicides may be hampered by extensive flooding which could limit access to aquatic habitats, dilute and wash away product (the latter may not be a concern if larvae are also washed out). Heavy precipitation and rainfall can also generate cryptic breeding habitats that are too numerous to treat. Additionally more frequent periods of heavy rainfall will necessitate repeated re-application of larvicides that is beyond the capacity of control programmes to deliver. The impact of larvicides in reducing malaria vector density is linearly correlated with coverage (Smith et al. 2013). Thus if larval populations are increasingly dispersed across a larger number of small and hard to reach habitats, the overall impact of larviciding will be compromised. This was observed in a programme in a flood zone in The Gambia, where larviciding had limited impact largely because ground teams were unable to reach and treat breeding habitats in a timely manner (Majambere et al. 2010). An explosion in the number of larval habitats due to prolonged precipitation will also make larviciding prohibitively expensive to implement at appropriate coverage.
In contrast to challenges posed by extreme rainfall, the prolonged drought conditions created in some parts of Africa due to climate changes may be advantageous for larviciding. Extreme drought would eliminate most small and ephemeral aquatic habitats; with mosquito populations being restricted only to a few remaining large and more stable habitats. These larger habitats fit more closely to the paradigm of ‘few, fixed and findable’, and will be easier to identify, access and treat. For example, a study by Charlwood et al. (2000) in the Kilombero Valley of Tanzania found that malaria vector larvae only persisted along the edge of river systems and larger permanent water bodies in the dry season. The concentration of larvae into these more limited and recognizable habitats as conditions become drier will make ground larviciding a more practical and cost effective intervention.
Another challenge for larviciding will be the increasing unpredictability of seasonal rains under climate change. The implementation of larviciding is easiest in the dry season when aquatic habitats are at their fewest. However, both the timing and duration of dry periods are less predictable as climate changes. For example, the monsoon season in parts of India may be lengthening with climate change (Karmakar and Pradhan 2020), thus decreasing the window over which larviciding is feasible.
Finally as with insecticides used for adult control, there is evidence that the efficacy of larvicides is influenced by the micro-climatic conditions under which they are deployed. Aedes vexans larvae collected from a field population in Germany were much more likely to be killed by Bti at warm (25 °C) than cooler temperatures (5–20 °C); (Becker et al. 1992). However, another study found that Bti had a lower impact on Ae. stimulans in cool temperatures; presumably because larval feeding rates and thus biocontrol uptake was reduced (Walker 1995). To our knowledge, the impact of high temperatures on the efficacy of larvicides used for African malaria control is not well known.
3.3 Novel vector control approaches
The efficacy of other novel vector control products currently in the development process could also be highly sensitive to local micro-climatic conditions, and thus vulnerable to change with climate. For example, the performance of spatial repellents is dependent on temperature, humidity and airflow conditions within the treated space (Ogoma et al. 2012). Studies in rural Tanzania (Ogoma et al. 2017) and Vietnam (Kawada et al. 2006) indicate spatial repellency is higher at warmer than cooler temperatures. This potential benefit of increased efficacy at higher temperatures could be offset off by faster evaporation and thus lower residual efficacy.
Attractive Target Sugar Baits (ATSB s) is another promising new vector control intervention whose efficacy is likely to be environmentally-dependent (Fraser et al. 2021). This intervention consists of device baited with an attractant lure and sugar source containing an insecticide. The effectiveness of this intervention likely depends on the attractiveness of ATSB s relative to other sugar sources fed on by mosquitoes in the environment (plants, flowers, etc.); with early work showing this intervention has high entomological impact in arid areas with limited vegetation (e.g. Mali (Traore et al. 2020); Israel (Beier et al. 2012)). Trials are currently underway to evaluate the epidemiological impact of ATSB s in differing eco-epidemiological settings (Eisele et al. 2022); and will show whether impact is reduced when deployed in more vegetation rich settings. If so, this intervention may have greater impact under warmer, drying conditions that may arise under climate change.
Several novel (endectocides) and existing (insecticide-treatment) interventions are targeted at exophagic vector species that feed on cattle (e.g. An. arabiensis and An. stephensi). An example is Ivermectin; an endectocide that can be used to treat helminths and other parasitic infections in humans and livestock, and also kills mosquitoes that feed on treated hosts (e.g. (Sylla et al. 2010). Mass drug administration of ivermectin to humans and/or cattle is being considered as a vector control tool. Preliminary trial results and modelling indicate this intervention will be most effective in areas of highly seasonal transmission (Slater et al. 2020). Climate-driven changes in malaria seasonality, and/or livestock husbandry and movement patterns could thus modify the likely coverage and feasibility of this strategy.
Climate change could also impact the effectiveness of existing and novel (e.g. eave tubes) housing-based vector control interventions. These interventions usually involve screening or closing of mosquito entry points such as the open eave space between the roof and wall. In the case of Eaves Tubes, the eave space is filled in and PVC ‘tubes’ coated with insecticidal netting are inserted as points of air flow between the inside and outside of the house. Odours from people sleeping inside the house disseminate out through the Eaves Tubes; causing mosquitoes to be lured towards them and killed when landing on their surface. A recent epidemiological trial in Cote d’Ivoire indicated this intervention reduced malaria infection risk in children by 38% (Sternberg et al. 2021). In some cases, these interventions may increase indoor temperatures by reducing indoor air flow. Under warming conditions, the discomfort due to even small reductions in indoor airflow may reduce the acceptability of these interventions. This could be mitigated through additional house design modifications to ensure the comfort of the indoor microclimate.
As shown using these representative examples, microclimatic and other environmental conditions within the settings where novel vector control interventions are deployed are likely to affect their performance. Greater understanding of how new and existing products for malaria vector control will perform under future climate scenarios is needed.
4 Mosquito resistance strategies
There is growing evidence that resistance strategies mounted by mosquitoes are environmentally dependent. Focussing on ITN s and IRS, mosquito vectors have developed a variety of physiological resistance (Black et al. 2021) and behavioural avoidance strategies including early and outdoor biting and resting (Sherrard-Smith et al. 2019). There is extensive evidence from agricultural entomology that the efficiency of physiological resistance to insecticides is temperature dependent; with the implications for future climate scenarios already well recognized (Pu et al. 2020). Notably, while some studies found physiological resistance in agricultural pests was impaired at high temperature, others reported an enhancement (Pu et al. 2020). This increased resistance at higher temperature was hypothesized to be due to pleiotropy or increased enzymatic activity in warmer conditions (Pu et al. 2020). In contrast, there has been relatively limited consideration of the impacts of temperature on insecticide resistance in malaria vectors. A recent systematic review suggested there may be a positive association between physiological resistance and temperature in Anopheles vectors (Agyekum, Botwe et al. 2021); suggesting mosquitoes will be less susceptible to insecticides in warmer climates. However, there is considerable heterogeneity in findings between studies. One laboratory study found that an insecticide resistant strain of An. arabiensis lived longer than a susceptible control line under high temperatures (Oliver and Brooke 2017); suggesting that climate could modify or even reverse the fitness cost of resistance mechanisms. However, another study showed that a resistant line of An. funestus exposed to Bendiocarb was more likely to die at high than intermediate temperatures, whilst deltamethrin was least likely to kill a resistant line of An. arabiensis at intermediate temperature than either hot or cold extremes (Glunt et al. 2018). The manner in which temperature impacts physiological resistance is thus complex, and may vary between mechanisms, species and insecticide classes.
In addition to physiological resistance, malaria vectors employ a range a behavioural avoidance strategies to evade indoor interventions. These can include a shift to biting earlier in the evening or in the morning when people are not protected by ITN s (Moiroux et al. 2014), increased zoophily and outdoor resting (Kreppel et al. 2020), and outdoor biting (Govella and Ferguson 2012; Reddy et al. 2011, Russell et al. 2011). Similar to physiological resistance, these behavioural adaptations may be shaped by local environmental and microclimatic conditions. Recent work has shown that outdoor biting and resting can vary seasonally and in response to temperature. For example, An. arabiensis in Tanzania became more exophilic when temperatures indoors became warmer relative to outdoors (Ngowo et al. 2017), during the hot season (Kulkarni et al. 2006, Kreppel et al. 2019), and An. gambiae sl in Burkina Faso are more likely to rest indoors during the wet than dry season (Sanou 2020). Should such seasonal variation reflects how African malaria vectors could adapt their behaviour to warming conditions, suggesting there may be an increased need for outdoor interventions under future climate change scenarios.
5 Indirect impacts of climate change on vector control
In addition to the potential direct impacts described above, there are multiple ways through which the ability to implement vector control will be indirectly impacted by the wider social, ecological, economic and political consequences of climate change. Such indirect effects will be widespread and complex, and may have a larger impact on intervention strategy and efficacy than any of the more direct impacts outlined above. Here we highlight a few factors that may have the greatest bearing on malaria vector control.
5.1 Human behaviour and use of interventions
Climate change could impact vector control efficacy by changing the human behavioural factors that influence intervention coverage and uptake. For example, the degree of protection obtained from ITN s is crucially dependent on usage. The decision to use an ITN is associated with micro-climatic conditions (Pulford et al. 2011, von Seidlein et al. 2012, Ahorlu et al. 2019). Specifically, users perceive ITN s to be less comfortable under warmer indoor temperatures and higher humidity (von Seidlein et al. 2012). ITN usage may fall during hotter periods of the year when people prefer to sleep outside where it is cooler (Guglielmo et al. 2021). Similar effects could lead to a reduction in ITN usage with the warmer conditions brought by climate change.
In addition to influencing the decision of whether to use an ITN or not, climate change may influence the amount of time people are likely to spend under a net. Exposure to malaria vectors in outdoor settings in Africa happens in evening hours (e.g. <10 pm, before people go indoors to sleep); when people are engaged in outdoor activities such as cooking, eating or socializing (Finda et al. 2019, Monroe et al. 2019). Prolonged exposure longer into the night can also happen when people are engaged in specific types of outdoor work or socio-cultural events (Monroe et al. 2019). The total time spent outdoors in the evening and late night period is also influenced by microclimatic conditions. One study showed that residents of rural communities in Burkina Faso went indoors to sleep at later hours during the hotter period of the year (Guglielmo et al. 2021). By delaying the time of night at which users first go under an ITN, warming conditions could reduce the total amount of protection received from it. Improved understanding of the environmental factors that influence human behaviours and decisions on ITN use (Monroe et al. 2021) are needed.
5.2 Land use and urbanization
One of the largest expected impacts of climate change is on land use (IPCC 2020). Climate change is predicted to lead to large changes in land quality and use across the globe; including erosion and degradation in some coastal areas, and expansion of drylands with increasing desertification. Drying conditions combined with shorter more intense rainfall and extreme flooding events will increase erosion and diminish soil quality (IPCC 2020). Changes to land type and soil quality will fundamentally impact patterns of land use and human activities; with several consequences for vector control strategies.
Most directly, these changes will impact agriculture and food security. It is estimated that ~90% of agriculture in sub-Saharan Africa is dependent on rain and managed by small holders (Abraham 2018). Staple crops such as maize and wheat have already been negatively affected by recent climate change (IPCC 2020); with yields at further risk in the future. Additionally, reductions in water availability and distribution will impact livestock husbandry. This is in turn could impact the efficacy and feasibility of livestock-based vector control methods such as zooprophylaxis and endectocides (Donnelly et al. 2015) Adaptations such as crop diversification and irrigation will be required to mitigate against the most negative consequences of these changes (Abraham 2018). However, these strategies could also influence the efficacy and feasibility of vector control. For example, irrigation schemes and dams are known to have complex associations with malaria risk in Africa (Ijumba and Lindsay 2001, Keiser et al. 2005, Kibret et al. 2017, Kibret, McCartney et al. 2021) Analysis of the literature indicates that dams may lead to increased transmission in highland or semi-arid areas of unstable transmission, but may be less important in areas of endemic transmission (Kibret et al. 2017). The creation of large irrigated areas may increase mosquito breeding sites, and make larval control more difficult (Karch et al. 1992).
Another mitigation response to diminishing crop yields arising from unpredictable weather conditions is heavier pesticide use. For example, small scale farmers in Rwanda reported increased use of pesticides as one of several common responses to mitigate the adverse impacts of increased drought and floods on their crops (Helwig et al. 2020). Pesticides used in agriculture are a major source of selection for insecticide resistance in malaria vectors (Nkya et al. 2013, Nkya et al. 2014, Chouaibou et al. 2016); thus their intensified use in response to climate change could erode the efficacy of ITN s and other insecticide-based approaches. Such an interplay will increase the already great need for stronger intersectoral collaboration between agriculture and public health under future climate scenarios.
Diminishing returns from small scale agriculture as a result of climate change have been linked to increasing migration to urban centres in several areas of Africa (Henderson et al. 2014, 2017, Serdeczny et al. 2017). Currently urbanization is happening faster in Africa than anywhere else in the world; with up to 2/3 of the total population expected to live in urban areas by 2050 (OECD et al. 2020). Climate change poses specific risks to urban populations, particularly those living in informal settlements that are at increased risk of flood damage, socioeconomically deprived, and poorly connected to electricity and water infrastructure (Abraham 2018). These housing conditions could generate increased exposure to malaria and other vector-borne diseases (Mordecai et al. 2020). For example, rapid urbanization in Soweto led to more people living in flood plain areas (Abraham 2018); with these being ideal habitats for mosquito vectors. Urban dwellers, and particularly those living in peri-urban and informal settlements may increasingly turn to market gardening to enhance food security (Eigenbrod and Gruda 2015). This could increase malaria exposure in those living close to market gardens (e.g.(Yadouleton et al. 2010)); possibly due to the generation of larval breeding sites through agricultural activities.
Poor housing conditions in informal urban settlements may not only increase malaria risk (Tusting et al. 2015), but may make it more difficult to implement standard vector control measures including installation of ITN s and IRS. Some interventions such as larviciding may be more feasible and cost effective to implement in urban settings (Worrall and Fillinger 2011), whilst others like ITN s and IRS have lower usage in urban than rural settings (Ministry of Health, (Zanzibar) et al. 2018). As described in Section 2, the recent invasion of An. stephensi in East Africa poses an additional risk for malaria control in urban African settings (Sinka et al. 2020). Unlike native African vector species, An. stephensi is highly adapted to urban environments (Mordecai et al. 2020). The unique ecology and behaviour of this vector, combined with it higher transmission efficiency, could require more tailored vector control interventions in urban settings. Sustaining vector control under future climate scenarios will require adapting current approaches to socio-economically disadvantaged populations in urban environments.
5.3 Economic and political factors
The ability to finance and implement large scale vector surveillance is fundamentally dependent on strong political will, governance infrastructure and economic security. As illustrated by the recent overwhelming resurgence of vector-borne diseases in Venezuela, even countries with a long and successful history of vector control can see rapid reversals during socio-economic and humanitarian crises (Grillet et al. 2019). Climate change is likely to increase vulnerability to such socio-economic shocks and lead to corresponding constraints on health systems and vector control programmes. These constraints may be further exacerbated by increased conflict (Freeman 2017, Adaawen et al. 2019), migration and increases in other infectious (Ahmed et al. 2018, Adekiya et al. 2020, Bryson et al. 2020, Charnley et al. 2022) and non-communicable diseases (Amegah et al. 2016).
The United Nations High Commission on Refugees estimates that 21.5 million people have been forcibly displaced each year since 2008 due to extreme weather events including floods, storms, wildlife and extreme temperature (Bilak et al. 2016). This number is expected to increase with climate change; with as many as 86 million internal climate migrants expected in sub Saharan Africa by 2050 (Clement et al. 2021). Refugees often face a considerably higher risk of malaria exposure and severe outcomes due to a myriad of factors including poor and insecure housing, infrastructure and limited access to prevention and treatment (e.g. (Hauser et al. 2023 Anderson et al. 2011, Charchuk et al. 2016)). There is some evidence that migration can lead to malaria spillover across border areas and local upsurges in areas where transmission was under control (e.g. (Rodriguez-Morales et al. 2019). Thus in the absence of access to healthcare including diagnosis and treatment, climate refugees may increasingly strain malaria control and compromise elimination activities. Development and implementation of more tailored diagnostics, treatments and vector control interventions for emergency contexts will be needed to sustain progress under climate change.
Sustaining and expanding malaria vector control under these more complex and economically constrained circumstances will be challenging. Already funding for malaria control is substantially below the level needed to meet global elimination targets, and has largely plateaued since 2012 (Lindsay et al. 2021). If health systems become even more stretched as climate changes, vector control programmes will increasingly be asked to deliver more effective interventions with less funding. Mass distribution of efficacious but relatively higher cost interventions that are recommended for use now (e.g. some Next Generation Nets) may become increasingly unaffordable. Clearly, maintaining malaria vector control will require the adaptation of current approaches and development of new ones that are both effective and affordable under future climate scenarios.
6 Conclusions and recommendations
Consideration of the potential impacts of climate change on vector-borne diseases has so far focussed almost exclusively on assessment of the environmental determinants of transmission. Such analyses provide an essential foundation to understand how the area at ‘risk’ of transmission may expand or contract; but on their own are insufficient to predict the nature of public health impacts. An equally important yet largely neglected question is how well our current and prospective control measures will function under altered climates; and how our ability to implement and sustain these approaches will be shaped by shifts in wider socio-environmental, economic and political factors that accompany this change. Within the context of malaria vector control in Africa; we have highlighted several routes through which the efficacy of interventions could be modified by the types of climate change predicted. A key theme is that climate change will have diverse and complex impacts across different regions of Africa, so that there may be no universal impact in all settings. Through synthesis of the varied biological and indirect impacts considered here, it is clear that climate change could have wide-ranging impacts on the implementation, feasibility and efficacy of vector control interventions in Africa. The overall impact of these changes on malaria control will depend on to what extent conditions for the ‘worst’ vs ‘best’ case scenarios are realized, as exemplified by the representative example in Box 1. At one end of the spectrum, climate change may enhance vector control through causing malaria vector populations to contract and reduce in abundance, and increasing the efficacy of some control methods. Alternatively, climate change could substantially erode vector control through favouring vector species and phenotypes that are harder to tackle with existing interventions, enhancing capacity for resistance, reducing the acceptability and use of interventions, and generating economic constraints that make it harder to deliver control programmes. The degree to which potential challenges can be offset by such advantages will fundamentally depend on the robustness of public health and other socioeconomic infrastructure. Clearly, there is a need to ‘future-proof’ vector control strategies through more anticipation and integration of potential climate impacts into future planning. This will require going beyond modifications and tailoring of existing and currently developing interventions, to more ‘blue sky’ and integrated approaches that are able to mitigate the impacts of climate change on malaria and other environmental hazards at the same time. Just as there has been extensive consideration of adaptation of agricultural systems to climate change, similar forethought is required for adaptation of vector control strategies. In particular, the addition of new control strategies that may be less sensitive to the environmental conditions of deployment (e.g. malaria vaccines) could greatly supplement and bolster control. While we focus on malaria in Africa, many of the issues raised here apply to the control of other mosquito-borne diseases that are controlled through use of similar interventions (e.g. Aedes vectors of arboviruses). To better prepare and mitigate against the most negative impacts, we advocate for consideration of climate change impacts to be built into future vector control and public health planning.
Box 1: Speculative ‘best’ and ‘worst’ case examples of how climate change may impact malaria vector control interventions in Africa, based on information reviewed in this chapter
Acknowledgements
NJG and HMF were supported by joint funding from the UK Medical Research Council (MRC, MR/T008873/1) and the UK Foreign, Commonwealth & Development Office (FCDO) under the MRC/FCDO Concordat agreement which is also part of the EDCTP2 programme supported by the European Union.
References
Abong’o B, Gimnig JE, Torr SJ, Longman B, Omoke D, Muchoki M, ter Kuile F, Ochomo E, Munga S, Samuels AM, Njagi K, Maas J, Perry RT, Fornadel C, Donnelly MJ and Oxborough RM (2020 ) Impact of indoor residual spraying with pirimiphos-methyl (Actellic 300CS) on entomological indicators of transmission and malaria case burden in Migori County, western Kenya. Sci Rep 10. https://doi.org/10.1038/s41598-020-61350-2.
Abraham EM (2018) Understanding climate change adaptation in Africa: key considerations. Management of Environmental Quality 29: 165–179. https://doi.org/10.1108/meq-01-2017-0001.
Adaawen S, Rademacher-Schulz C, Schraven B and Segadlo N (2019) Drought, migration, and conflict in sub-Saharan Africa: what are the links and policy options? In: Mapedza E, Tsegai D, Bruntrup M and McLeman R eds., Drought Challenges: Policy Options for Developing Countries, Current Directions in Water Scarcity Research, pp. 15–31. https://doi.org/10.1016/b978-0-12-814820-4.00002-x.
Adekiya TA, Aruleba RT, Oyinloye BE, Okosun KO and Kappo AP (2020) The Effect of climate change and the snail-schistosome cycle in transmission and bio-control of schistosomiasis in Sub-Saharan Africa. International Journal of Environmental Research and Public Health 17. https://doi.org/10.3390/ijerph17010181.
Adhikari U, Nejadhashemi AP and Herman MR (2015) A review of climate change impacts on water resources in East Africa. Transactions of the ASABE58: 1493–1507.
Agyekum TP, Arko-Mensah J, Botwe PK, Hogarh JN, Issah I, Dwomoh D, Billah MK, Dadzie SK, Robins TG and Fobil JN (2022) Effects of elevated temperatures on the development of immature stages of Anopheles gambiae (s.l.) mosquitoes. Tropical Medicine & International Health 27(4): 338–346. https://doi.org/10.1111/tmi.13732.
Agyekum TP, Botwe PK, Arko-Mensah J, Issah I, Acquah AA, Hogarh JN, Dwomoh D, Robins TG and Fobil JN (2021) A systematic review of the effects of temperature on Anopheles mosquito development and survival: implications for malaria control in a future warmer climate. International Journal of Environmental Research and Public Health 18. https://doi.org/10.3390/ijerph18147255.
Ahmed SA, Florez MG and Karanis P (2018) The impact of water crises and climate changes on the transmission of protozoan parasites in Africa. Pathogens and Global Health 112: 281–293. https://doi.org/10.1080/20477724.2018.1523778.
Ahorlu CS, Adongo P, Koenker H, Zigirumugabe S, Sika-Bright S, Koka E, Tabong PTN, Piccinini D, Segbaya S, Olapeju B and Monroe A (2019) Understanding the gap between access and use: a qualitative study on barriers and facilitators to insecticide-treated net use in Ghana. Malaria Journal 18. https://doi.org/10.1186/s12936-019-3051-0.
Akpan GE, Adepoju KA and Oladosu OR (2019) Potential distribution of dominant malaria vector species in tropical region under climate change scenarios. PLoS One 14. https://doi.org/10.1371/journal.pone.0218523.
Akurut M, Willems P and Niwagaba CB (2014) Potential Impacts of Climate Change on Precipitation over Lake Victoria, East Africa, in the 21st Century. Water 6: 2634–2659. https://doi.org/10.3390/w6092634.
Alonso D, Bouma MJ and Pascual M (2011) Epidemic malaria and warmer temperatures in recent decades in an East African highland. Proceedings of the Royal Society B-Biological Sciences 278: 1661–1669. https://doi.org/10.1098/rspb.2010.2020.
Amegah AK, Rezza G and Jaakkola JJK (2016) Temperature-related morbidity and mortality in Sub-Saharan Africa: a systematic review of the empirical evidence. Environment International 91: 133–149. https://doi.org/10.1016/j.envint.2016.02.027.
Anderson J, Doocy S, Haskew C, Spiegel P and Moss WJ (2011) The burden of malaria in post-emergency refugee sites: a retrospective study. Conflict and Health 5: (19 September 2011).
Arthur FH (2013) Dosage rate, temperature, and food source provisioning affect susceptibility of Tribolium castaneum and Tribolium confusum to chlorfenapyr. Journal of Pest Science 86: 507–513. https://doi.org/10.1007/s10340-013-0495-9.
Arthur FH, Starkus LA and McKay T (2019) Degradation and residual efficacy of beta- cyfluthrin as a surface treatment for control of Tribolium castaneum Herbst: Effects of temperature and environment. Journal of Stored Products Research 84. https://doi.org/10.1016/j.jspr.2019.101514.
Bayoh MN and Lindsay SW (2003) Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera : Culicidae). Bulletin of Entomological Research 93: 375–381.
Bayoh MN and Lindsay SW (2004) Temperature-related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory. Medical and Veterinary Entomology 18: 174–179. https://doi.org/10.1111/j.0269-283X.2004.00495.x.
Becker N, Zgomba M, Ludwig M, Petric D and Rettich F (1992) Factors influencing the activity of Bacillus-thuringiensis var israelensis treatments. Journal of the American Mosquito Control Association 8: 285–289.
Beier JC (1998) Malaria parasite development in mosquitoes. Annual Review of Entomology 43: 519–543.
Beier JC, Muller GC, Gu WD, Arheart KL and Schlein Y (2012) Attractive toxic sugar bait (ATSB) methods decimate populations of Anopheles malaria vectors in arid environments regardless of the local availability of favoured sugar-source blossoms. Malaria Journal 11. https://doi.org/10.1186/1475-2875-11-31.
Ben Mohamed A (2011) Climate change risks in Sahelian Africa. Regional Environmental Change 11: S109–S117. https://doi.org/10.1007/s10113-010-0172-y.
Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, Battle KE, Moyes CL, Henry A, Eckhoff PA, Wenger EA, Briet O, Penny MA, Smith TA, Bennett A, Yukich J, Eisele TP, Griffin JT, Fergus CA, Lynch M, Lindgren F, Cohen JM, Murray CL, Smith DL, Hay SI, Cibulskis RE and Gething PW (2015) The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526: 207–211. https://doi.org/10.1038/nature15535.
Bilak A, Cardona-Fox G, Ginnett J, Rushing EJ, Scherer, I, Swain M, Walicki N and Yonetani M (2016) Grid 2016: Global Report on Internal Displacement, Internal Displacement Monitoring Centre.
Black WC, Snell TK, Saavedra-Rodriguez K, Kading RC and Campbell CL (2021) From global to local-new insights into features of pyrethroid detoxification in vector mosquitoes. Insects 12: 19. https://doi.org/10.3390/insects12040276.
Boyce R, Reyes R, Matte M, Ntaro M, Mulogo E, Metlay JP, Band L and Siedner MJ (2016) Severe flooding and malaria transmission in the Western Ugandan Highlands: implications for disease control in an era of global climate change. Journal of Infectious Diseases 214: 1403–1410. https://doi.org/10.1093/infdis/jiw363.
Bryson JM, Bishop-Williams KE, Berrang-Ford L, Nunez EC, Lwasa S, Namanya DB, Harper SL and Indigenous Hlth Adaptation C (2020) Neglected tropical diseases in the context of climate change in East Africa: a systematic scoping review. American Journal of Tropical Medicine and Hygiene 102: 1443–1454. https://doi.org/10.4269/ajtmh.19-0380.
Caminade C, Kovats S, Rocklov J, Tompkins AM, Morse AP, Colon-Gonzalez FJ, Stenlund H, Martens P and Lloyd SJ (2014) Impact of climate change on global malaria distribution. Proceedings of the National Academy of Sciences of the United States of America 111: 3286–3291. https://doi.org/10.1073/pnas.1302089111.
Charchuk R, Paul MKJ, Claude KM, Houston S and Hawkes MT (2016) Burden of malaria is higher among children in an internal displacement camp compared to a neighbouring village in the Democratic Republic of the Congo. Malaria Journal 15. https://doi.org/10.1186/s12936-016-1479-z.
Charlwood JD, Vij R and Billingsley PF (2000) Dry season refugia of malaria-transmitting mosquitoes in a dry savannah zone of east Africa. Am J Trop Med Hyg 62: 726–732.
Charnley GEC, Kelman I and Murray KA (2022) Drought-related cholera outbreaks in Africa and the implications for climate change: a narrative review. Pathogens and Global Health 116: 3–12. https://doi.org/10.1080/20477724.2021.1981716.
Chersich MF, Wright CY, Venter F, Rees H, Scorgie F and Erasmus B (2018) Impacts of climate change on health and wellbeing in South Africa. International Journal of Environmental Research and Public Health 15. https://doi.org/10.3390/ijerph15091884.
Choi L, Majambere S and Wilson AL (2019) Larviciding to prevent malaria transmission (Review). Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD012736.pub2.
Chou SC, Lyra AdA, Gomes JL, Rodriguez DA, Martins MA, Resende NC, Tavares PDS, Dereczynski CP, Pilotto IL, Martins AM, Alves de Carvalho LF, Lima Onofre JL, Major I, Penhor M and Santana A (2020) Downscaling projections of climate change in Sao Tome and Principe Islands, Africa. Climate Dynamics 54: 4021–4042. https://doi.org/10.1007/s00382-020-05212-7.
Chouaibou MS, Fodjo BK, Fokou G, Allassane OF, Koudou BG, David JP, Antonio-Nkondjio C, Ranson H and Bonfoh B (2016) Influence of the agrochemicals used for rice and vegetable cultivation on insecticide resistance in malaria vectors in southern Cote d’Ivoire. Malaria Journal 15: (24 August 2016)–(2024 August 2016).
Christiansen-Jucht CD, Parham PE, Saddler A, Koella JC and Basanez MG (2015) Larval and adult environmental temperatures influence the adult reproductive traits of Anopheles gambiae s.s. Parasites & Vectors 8. https://doi.org/10.1186/s13071-015-1053-5.
Clement V, Rigaud K, A dS, Jones B, S A, J S, N S and Shabahat E (2021) Groundswell Part 2: Acting on Internal Climate Migration. World Bank, Washington, DC. https://openknowledge.worldbank.org/handle/10986/36248.
Connolly-Boutin L and Smit B (2016) Climate change, food security, and livelihoods in sub-Saharan Africa. Regional Environmental Change 16: 385–399. https://doi.org/10.1007/s10113-015-0761-x.
Derua YA, Kweka EJ, Kisinza W, Githeko AK and Mosha FW (2019) Bacterial larvicides used for malaria vector control in sub‑Saharan Africa: review of their effectiveness and operational feasibility. Parasit Vectors 12: 426.
Diouf I, Adeola AM, Abiodun GJ, Lennard C, Shirinde JM, Yaka P, Ndione J-A and Gbobaniyi EO (2021) Impact of future climate change on malaria in West Africa. Theoretical and Applied Climatology. https://doi.org/10.1007/s00704-021-03807-6.
Donnelly B, Berrang-Ford L, Ross NA and Michel P (2015) A systematic, realist review of zooprophylaxis for malaria control. Malaria Journal 14. https://doi.org/10.1186/s12936-015-0822-0.
Drake JM and Beier JC (2014) Ecological niche and potential distribution of Anopheles arabiensis in Africa in 2050. Malaria Journal 13: (3 June 2014).
Du Plessis JA and Kalima SG (2021) Modelling the impact of climate change on the flow of the Eerste River in South Africa. Physics and Chemistry of the Earth 124. https://doi.org/10.1016/j.pce.2021.103025.
Egbendewe-Mondzozo A, Musumba M, McCarl BA and Wu X (2011) Climate change and vector-borne diseases: an economic impact analysis of malaria in Africa. International Journal of Environmental Research and Public Health 8: 913–930. https://doi.org/10.3390/ijerph8030913.
Eigenbrod C and Gruda N (2015) Urban vegetable for food security in cities. A review. Agronomy for Sustainable Development 35: 483–498. https://doi.org/10.1007/s13593-014-0273-y.
Eisele TP, Kleinschmidt I, Sarrassat S, TerKuile F, Miller J, Chanda J, Silumbe K, Samuels A, Janssen J, Ogwang C, Bradley J, Orange E, Yukich J, Ashton R, Kyomuhangi I, Harris AF, Doumbia S, Toure M, Moumine M, Majambere S, Mburu MM, Mwaanga G, Simubali L, Simulundu E, Bennett A, Slutsker L, Muller G, Ochomo E, Gimnig J, Johnson PCD, Wagman J, Litrell M and Attractive Targeted Sugar Bait P (2022) Attractive targeted sugar bait phase III trials in Kenya, Mali, and Zambia. Trials 23. https://doi.org/10.1186/s13063-022-06555-8.
Ermert V, Fink AH and Paeth H (2013) The potential effects of climate change on malaria transmission in Africa using bias-corrected regionalised climate projections and a simple malaria seasonality model. Climatic Change 120: 741–754. https://doi.org/10.1007/s10584-013-0851-z.
Fall P, Diouf I, Deme A and Sene D (2022) Assessment of Climate-Driven Variations in Malaria Transmission in Senegal Using the VECTRI Model. Atmosphere 13. https://doi.org/10.3390/atmos13030418.
Fillinger U, Knols BGJ and Becker N (2003) Efficacy and efficiency of new Bacillus thuringiensis var. israelensis and Bacillus sphaericus formulations against Afrotropical anophelines in Western Kenya. Trop Med Int Health 8: 37–47. https://doi.org/10.1046/j.1365-3156.2003.00979.x.
Finda MF, Moshi IR, Monroe A, Limwagu AJ, Nyoni AP, Swai JK, Ngowo HS, Minja EG, Toe LP, Kaindoa EW, Coetzee M, Manderson L and Okumu FO (2019) Linking human behaviours and malaria vector biting risk in south-eastern Tanzania. PLoS One 14. https://doi.org/10.1371/journal.pone.0217414.
Fouet C, Gray E, Besansky NJ and Costantini C (2012) Adaptation to Aridity in the Malaria Mosquito Anopheles gambiae: Chromosomal Inversion Polymorphism and Body Size Influence Resistance to Desiccation. PLoS One 7. https://doi.org/10.1371/journal.pone.0034841.
Fraser KJ, Mwandigha L, Traore SF, Traore MM, Doumbia S, Junnila A, Revay E, Beier JC, Marshall JM, Ghani AC and Muller G (2021) Estimating the potential impact of Attractive Targeted Sugar Baits (ATSBs) as a new vector control tool for Plasmodium falciparum malaria. Malaria Journal 20. https://doi.org/10.1186/s12936-021-03684-4.
Freeman L (2017) Environmental Change, Migration, and Conflict in Africa: A Critical Examination of the Interconnections. Journal of Environment & Development 26: 351–374. https://doi.org/10.1177/1070496517727325.
Gerken AR, Scully ED, Campbell JF and Morrison WR, III (2021) Effectiveness of long-lasting insecticide netting on Tribolium castaneum is modulated by multiple exposures, biotic, and abiotic factors. Pest Management Science 77: 1235–1244. https://doi.org/10.1002/ps.6134.
Gething PW, Smith DL, Patil AP, Tatem AJ, Snow RW and Hay SI (2010a) Climate change and the global malaria recession. Nature 465: 342–U394. https://doi.org/10.1038/nature09098.
Gething PW, Smith DL, Patil AP, Tatem AJ, Snow RW and Hay SI (2010b) Climate change and the global malaria recession. Nature 465: 342–345. https://doi.org/10.1038/nature09098.
Glunt KD, Blanford JI and Paaijmans KP (2013) Chemicals, Climate, and Control: Increasing the Effectiveness of Malaria Vector Control Tools by Considering Relevant Temperatures. Plos Pathogens 9: e1003602. https://doi.org/10.1371/journal.ppat.1003602
Glunt KD, Oliver SV, Hunt RH and Paaijmans KP (2018) The impact of temperature on insecticide toxicity against the malaria vectors Anopheles arabiensis and Anopheles funestus. Malaria Journal 17. https://doi.org/10.1186/s12936-018-2250-4.
Glunt KD, Paaijmans KP, Read AF and Thomas MB (2014) Environmental temperatures significantly change the impact of insecticides measured using WHOPES protocols. Malaria Journal 13. https://doi.org/10.1186/1475-2875-13-350.
Gray EM and Bradley TJ (2005) Physiology of desiccation resistance in Anopheles gambiae and Anopheles arabiensis. American Journal of Tropical Medicine and Hygiene 73: 553–559. https://doi.org/10.4269/ajtmh.2005.73.553.
Gray EM, Rocca KAC, Costantini C and Besansky NJ (2009) Inversion 2La is associated with enhanced desiccation resistance in Anopheles gambiae. Malaria Journal 8. https://doi.org/10.1186/1475-2875-8-215.
Grillet ME, Hernandez-Villena JV, Llewellyn MS, Paniz-Mondolfi AE, Tami A, Vincenti-Gonzalez MF, Marquez M, Mogollon-Mendoza AC, Hernandez-Pereira CE, Plaza-Morr JD, Blohm G, Grijalva MJ, Costales JA, Ferguson HM, Schwabl P, Hernandez-Castro LE, Lamberton PHL, Streicker DG, Haydon DT, Miles MA, Acosta-Serrano A, Acquattela H, Basanez MG, Benaim G, Colmenares LA, Conn JE, Espinoza R, Freilij H, Graterol-Gil MC, Hotez PJ, Kato H, Lednicky JA, Martinez CE, Mas-Coma S, Morris JG, Navarro JC, Ramirez JL, Rodriguez M, Urbina JA, Villegas L, Segovia MJ, Carrasco HJ, Crainey JL, Luz SLB, Moreno JD, Gonzalez OON, Ramirez JD and Alarcon-de Noya B (2019) Venezuela’s humanitarian crisis, resurgence of vector-borne diseases, and implications for spillover in the region. Lancet Infect Dis 19: E149–E161. https://doi.org/10.1016/s1473-3099(18)30757-6.
Guglielmo F, Ranson H, Sagnon N and Jones C (2021) The issue is not ‘compliance’: exploring exposure to malaria vector bites through social dynamics in Burkina Faso. Anthropol Med 28: 508–525. https://doi.org/10.1080/13648470.2021.1884185.
Hauser M, Kabuya JBB, Mantus M, Kamavu LK, Sichivula JL, Matende WM, Fritschi N, Shields T, Curriero F, Kvit A, Chongwe G, Moss WJ, Ritz N and Ippolito MM (2023) Malaria in Refugee Children Resettled to a Holoendemic Area of Sub-Saharan Africa. Clinical Infectious Diseases 76(3): e1104–e1113 https://doi.org/10.1093/cid/ciac417.
Helwig K, C H-OC, Mikulewicz M, Mugiraneza P and E C (2020) The Role of Microfinance in Climate Change Adaptation: Evidence from Rural Rwanda, Glasgow Caledonian University Glasgow.
Henderson JV, Storeygard A and Deichmann U (2014) 50 Years of urbanization in Africa: examining the role of climate change. Policy Research Working Paper – World Bank: 42 pp.
Henderson JV, Storeygard A and Deichmann U (2017) Has climate change driven urbanization in Africa? J Dev Econ 124: 60–82. https://doi.org/10.1016/j.jdeveco.2016.09.001.
Ijumba JN and Lindsay SW (2001) Impact of irrigation on malaria in Africa: paddies paradox. Medical and Veterinary Entomology 15: 1–11. https://doi.org/10.1046/j.1365-2915.2001.00279.x.
IPCC (2020) Climate Change and Land, Geneva.
Kahamba NF, Finda M, Ngowo HS, Msugupakulya BJ, Baldini F, Koekemoer LL, Ferguson HM and Okumu FO (2022) Using ecological observations to improve malaria control in areas where Anopheles funestus is the dominant vector. Malaria Journal 21. https://doi.org/10.1186/s12936-022-04198-3.
Karch S, Asidi N, Manzambi ZM and Salaun JJ (1992) Efficacy of Bacillus-sphaericus against the malaria vector Anopheles-gambiae and other mosquitos in swamps and rice fields in Zaire. Journal of the American Mosquito Control Association 8: 376–380.
Karmakar M and Pradhan MM (2020) Climate change and public health: a study of vector-borne diseases in Odisha, India. Nat Hazards 102: 659–671. https://doi.org/10.1007/s11069-019-03594-4.
Kawada H, Iwasaki T, Luu Le L, Tran Khanh T, Nguyen Thi Nhu M, Shono Y, Katayama Y and Takagi M (2006) Field evaluation of spatial repellency of metofluthrin-impregnated latticework plastic strips against Aedes aegypti (L.) and analysis of environmental factors affecting its efficacy in My Tho City, Tien Giang, Vietnam. American Journal of Tropical Medicine and Hygiene 75: 1153–1157. https://doi.org/10.4269/ajtmh.2006.75.1153.
Keiser J, De Castro MC, Maltese MF, Bos R, Tanner M, Singer BH and Utzinger J (2005) Effect of irrigation and large dams on the burden of malaria on a global and regional scale. American Journal of Tropical Medicine and Hygiene 72: 392–406. https://doi.org/10.4269/ajtmh.2005.72.392
Kelly-Hope L and Thomson MC (2005) Climate and infectious diseases. In: Climate, Climatic Change and Human Health Workshop, Sep 12–14, Wengen, Switzerland, Advances in Global Change Research.
Kibret S, McCartney M, Lautze J, Nhamo L and Yan GY (2021) The impact of large and small dams on malaria transmission in four basins in Africa. Sci Rep 11. https://doi.org/10.1038/s41598-021-92924-3.
Kibret S, Wilson GG, Ryder D, Tekie H and Petros B (2017) The Influence of Dams on Malaria Transmission in Sub-Saharan Africa. EcoHealth 14: 408–419. https://doi.org/10.1007/s10393-015-1029-0.
Killeen GF (2014) Characterizing, controlling and eliminating residual malaria transmission. Malar J 13. https://doi.org/10.1186/1475-2875-13-330.
Killeen GF, Kiware SS, Seyoum A, Gimnig JE, Corliss GF, Stevenson J, Drakeley CJ and Chitnis N (2014) Comparative assessment of diverse strategies for malaria vector population control based on measured rates at which mosquitoes utilize targeted resource subsets. Malar J 13: 338. https://doi.org/10.1186/1475-2875-13-338.
Kirby MJ and Lindsay SW (2004) Responses of adult mosquitoes of two sibling species, Anopheles arabiensis and A. gambiae s.s. (Diptera: Culicidae) to high temperatures. Bull Entomol Res 94: 441–448.
Kirby MJ and Lindsay SW (2009) Effect of temperature and inter-specific competition on the development and survival of Anopheles gambiae sensu stricto and An. arabiensis larvae. Acta Tropica 109: 118–123.
Kiware SS, Chitnis N, Devine GJ, Moore SJ, Majambere S and Killeen GF (2012a) Biologically meaningful coverage indicators for eliminating malaria transmission. Biol Lett 8: 874–877. https://doi.org/10.1098/rsbl.2012.0352.
Kiware SS, Chitnis N, Moore SJ, Devine GJ, Majambere S, Merrill S and Killeen GF (2012b) Simplified models of vector control impact upon malaria transmission by zoophagic mosquitoes. PLoS One 7: e37661. https://doi.org/10.1371/journal.pone.0037661.
Kreppel K, Caminade C, Govella N, Morse AP, Ferguson HM and Baylis M (2019) Impact of ENSO 2016–17 on regional climate and malaria vector dynamics in Tanzania. Environmental Research Letters 14. https://doi.org/10.1088/1748-9326/ab26c7.
Kulkarni MA, Kweka E, Nyale E, Lyatuu E, Mosha FW, Chandramohan D, Rau ME and Drakeley C (2006) Entomological evalution of malaria vectors at different altitudes in Hal District, Northeastern Tanzania. Journal of Medical Entomology 43: 580–588.
Lafferty KD (2009) The ecology of climate change and infectious diseases. Ecology 90: 888–900. https://doi.org/10.1890/08-0079.1.
Lee Y, Meneses CR, Fofana A and Lanzaro GC (2009) Desiccation resistance among subpopulations of Anopheles gambiae s.s. from Selinkenyi, Mali. Journal of Medical Entomology 46: 316–320. https://doi.org/10.1603/033.046.0216.
Leedale J, Tompkins AM, Caminade C, Jones AE, Nikulin G and Morse AP (2016) Projecting malaria hazard from climate change in eastern Africa using large ensembles to estimate uncertainty. Geospatial Health 11: 102–114. https://doi.org/10.4081/gh.2016.393.
Lindsay SW, Parson L and Thomas CJ (1998) Mapping the ranges and relative abundance of the two principal African malaria vectors, Anopheles gambiae sensu stricto and An. arabiensis, using climate data. Proc Biol Sci 265: 847–854.
Lindsay SW, Thomas MB and Kleinschmidt I (2021) Threats to the effectiveness of insecticide-treated bednets for malaria control: thinking beyond insecticide resistance. Lancet Global Health 9: E1325–E1331. https://doi.org/10.1016/s2214-109x(21)00216-3.
Lyimo IN and Ferguson HM (2009) Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends in Parasitology 25: 189–196.
Lyons CL, Coetzee M, Terblanche JS and Chown SL (2012) Thermal limits of wild and laboratory strains of two African malaria vector species, Anopheles arabiensis and Anopheles funestus. Malaria Journal 11: (6 July 2012).
Lyons CL, Coetzee M, Terblanche JS and Chown SL (2014) Desiccation tolerance as a function of age, sex, humidity and temperature in adults of the African malaria vectors Anopheles arabiensis and Anopheles funestus. Journal of Experimental Biology 217: 3823–3833. https://doi.org/10.1242/jeb.104638.
Mabaso MLH, Craig M, Ross A and Smith T (2007) Environmental predictors of the seasonality of malaria transmission in Africa: The challenge. American Journal of Tropical Medicine and Hygiene 76: 33–38. https://doi.org/10.4269/ajtmh.2007.76.33.
Majambere S, Lindsay SW, Green C, Kandeh B and Fillinger U (2007) Microbial larvicides for malaria control in The Gambia. Malaria Journal 6: 76. https://doi.org/10.1186/1475-2875-6-76.
Majambere S, Pinder M, Fillinger U, Ameh D, Conway DJ, Green C, Jeffries D, Jawara M, Milligan PJ, Hutchinson R and Lindsay SW (2010) Is Mosquito Larval Source Management Appropriate for Reducing Malaria in Areas of Extensive Flooding in The Gambia? A Cross-over Intervention Trial. Am J Trop Med Hyg 82: 176–184.
Martens P, Kovats RS, Nijhof S, de Vries P, Livermore MTJ, Bradley DJ, Cox J and McMichael AJ (1999) Climate change and future populations at risk of malaria. Global Environmental Change-Human and Policy Dimensions 9: S89–S107. https://doi.org/10.1016/s0959-3780(99)00020-5.
McMichael AJ (2013) Globalization, Climate Change, and Human Health REPLY. New England Journal of Medicine 369: 96–96.
Ministry of Health CD, Gender, Elderly and Children (Tanzania), (Zanzibar) MoH, (Tanzania) NBoS, Statistician OotCG and ICF (2018) Tanzania Malaria Indicator Survey 2017, Dar es Salaam.
Monroe A, Moore S, Koenker H, Lynch M and Ricotta E (2019) Measuring and characterizing night time human behaviour as it relates to residual malaria transmission in sub-Saharan Africa: a review of the published literature. Malaria Journal 18. https://doi.org/10.1186/s12936-019-2638-9.
Monroe A, Moore S, Olapeju B, Merritt AP and Okumu F (2021) Unlocking the human factor to increase effectiveness and sustainability of malaria vector control. Malaria Journal 20. https://doi.org/10.1186/s12936-021-03943-4.
Mordecai EA, Ryan SJ, Caldwell JM, Shah MM and LaBeaud AD (2020) Climate change could shift disease burden from malaria to arboviruses in Africa. Lancet Planetary Health 4: E416–E423.
Murdock CC, Sternberg ED and Thomas MB (2016) Malaria transmission potential could be reduced with current and future climate change. Sci Rep 6. https://doi.org/10.1038/srep27771.
Nartey R, Owusu-Dabo E, Kruppa T, Baffour-Awuah S, Annan A, Oppong S, Becker N and Obiri-Danso K (2013) Use of Bacillus thuringiensis var israelensis as a viable option in an Integrated Malaria Vector Control Programme in the Kumasi Metropolis, Ghana. Parasites & Vectors 6: 1–10.
Ndhlovu GZ and Woyessa YE (2021) Evaluation of Streamflow under Climate Change in the Zambezi River Basin of Southern Africa. Water 13. https://doi.org/10.3390/w13213114.
Ng’habi KR, Mwasheshi D, Knols BG and Ferguson HM (2010) Establishment of a self- propagating population of the African malaria vector Anopheles arabiensis under semi-field conditions. Malar J 9: 356. https://doi.org/10.1186/1475-2875-9-356.
Ngowo HS, Hape EE, Matthiopoulos J, Ferguson HM and Okumu FO (2021) Fitness characteristics of the malaria vector Anopheles funestus during an attempted laboratory colonization. Malaria Journal 20. https://doi.org/10.1186/s12936-021-03677-3.
Ngowo HS, Kaindoa EW, Matthiopoulos J, Ferguson HM and Okumu FO (2017) Variations in household microclimate affect outdoor-biting behaviour of malaria vectors. Wellcome open research 2: 102. https://doi.org/10.12688/wellcomeopenres.12928.1.
Nkya TE, Akhouayri I, Kisinza W and David J-P (2013) Impact of environment on mosquito response to pyrethroid insecticides: Facts, evidences and prospects. Insect Biochemistry and Molecular Biology 43: 407–416. https://doi.org/10.1016/j.ibmb.2012.10.006.
Nkya TE, Poupardin R, Laporte F, Akhouayri I, Mosha F, Magesa S, Kisinza W and David J-P (2014) Impact of agriculture on the selection of insecticide resistance in the malaria vector Anopheles gambiae: a multigenerational study in controlled conditions. Parasites & Vectors 7. https://doi.org/10.1186/s13071-014-0480-z.
Noor AM and Alonso PL (2022) The message on malaria is clear: progress has stalled. Lancet 399: 1777–1777. https://doi.org/10.1016/s0140-6736(22)00732-2.
OECD, Sahel and Club WA (2020) Africa's Urbanisation Dynamics 2020. https://doi.org/doi:https://doi.org/10.1787/b6bccb81-en.
Ogoma SB, Mmando AS, Swai JK, Horstmann S, Malone D and Killeen GF (2017) A low technology emanator treated with the volatile pyrethroid transfluthrin confers long term protection against outdoor biting vectors of lymphatic filariasis, arboviruses and malaria. PLoS Negl Trop Dis 11: e0005455.
Ogoma SB, Moore SJ and Maia MF (2012) A systematic review of mosquito coils and passive emanators: defining recommendations for spatial repellency testing methodologies. Parasites & Vectors 5. https://doi.org/10.1186/1756-3305-5-287.
Ohm JR, Baldini F, Barreaux P, Lefevre T, Lynch PA, Suh E, Whitehead SA and Thomas MB (2018) Rethinking the extrinsic incubation period of malaria parasites. Parasites & Vectors 11. https://doi.org/10.1186/s13071-018-2761-4.
Olabimi IO, Ileke KD, Adu BW and Arotolu TE (2021) Potential distribution of the primary malaria vector Anopheles gambiae Giles Diptera: Culicidae in Southwest Nigeria under current and future climatic conditions. Journal of Basic and Applied Zoology 82. https://doi.org/10.1186/s41936-021-00261-8.
Oliver SV and Brooke BD (2017) The effect of elevated temperatures on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). Malaria Journal 16. https://doi.org/10.1186/s12936-017-1720-4.
Paaijmans KP, Heinig RL, Seliga RA, Blanford JI, Blanford S, Murdock CC and Thomas MB (2013) Temperature variation makes ectotherms more sensitive to climate change. Global Change Biology 19: 2373–2380. https://doi.org/10.1111/gcb.12240.
Parham PE, Pople D, Christiansen-Jucht C, Lindsay S, Hinsley W and Michael E (2012) Modeling the role of environmental variables on the population dynamics of the malaria vector Anopheles gambiae sensu stricto. Malaria Journal 11. https://doi.org/10.1186/1475-2875-11-271.
Pu J, Wang Z and Chung H (2020) Climate change and the genetics of insecticide resistance. Pest Management Science 76: 846–852. https://doi.org/10.1002/ps.5700.
Pulford J, Hetzel MW, Bryant M, Siba PM and Mueller I (2011) Reported reasons for not using a mosquito net when one is available: a review of the published literature. Malaria Journal 10. https://doi.org/10.1186/1475-2875-10-83.
Ranabhat S and Wang C (2020) Effect of moisture on efficacy of selected insecticide dusts against the common bed bug, Cimex lectularius (Hemiptera: Cimicidae). Journal of Economic Entomology 113: 1933–1939. https://doi.org/10.1093/jee/toaa122.
Reiner RC, Geary M, Atkinson PM, Smith DL and Gething PW (2015) Seasonality of Plasmodium falciparum transmission: a systematic review. Malaria Journal 14. https://doi.org/10.1186/s12936-015-849-2.
Rodriguez-Morales AJ, Suarez JA, Risquez A, Villamil-Gomez WE and Paniz-Mondolfi A (2019) Consequences of Venezuela’s massive migration crisis on imported malaria in Colombia, 2016–2018. Travel Med Infect Dis 28: 98–99. https://doi.org/10.1016/j.tmaid.2019.02.004.
Sanou A (2020) The ecology and behaviour of insecticide resistant malaria vectors and implications for control in Burkina Faso, University of Glasgow.
Serdeczny O, Adams S, Baarsch F, Coumou D, Robinson A, Hare W, Schaeffer M, Perrette M and Reinhardt J (2017) Climate change impacts in Sub-Saharan Africa: from physical changes to their social repercussions. Regional Environmental Change 17: 1585–1600. https://doi.org/10.1007/s10113-015-0910-2.
Seyfarth M, Khaireh BA, Abdi AA, Bouh SM and Faulde MK (2019) Five years following first detection of Anopheles stephensi (Diptera: Culicidae) in Djibouti, Horn of Africa: populations established malaria emerging. Parasitology Research 118: 725–732. https://doi.org/10.1007/s00436-019-06213-0.
Shapiro LLM, Whitehead SA and Thomas MB (2017) Quantifying the effects of temperature on mosquito and parasite traits that determine the transmission potential of human malaria. Plos Biology 15. https://doi.org/10.1371/journal.pbio.2003489.
Sherrard-Smith E, Skarp JE, Beale AD, Fornadel C, Norris LC, Moore SJ, Mihreteab S, Charlwood JD, Bhatt S, Winskill P, Griffin JT and Churcher TS (2019) Mosquito feeding behavior and how it influences residual malaria transmission across Africa. Proceedings of the National Academy of Sciences of the United States of America 116: 15086–15095. https://doi.org/10.1073/pnas.1820646116.
Shousha AT (1948) Species-eradication. the eradication of Anopheles gambiae from Upper Egypt, 1942–1945. Bull World Health Organ 1: 309–353.
Sibanda MM, Focke WW, Labuschagne FJWJ, Moyo L, Nhlapo NS, Maity A, Muiambo H, Massinga P, Jr., Crowther NAS, Coetzee M and Brindley GWA (2011) Degradation of insecticides used for indoor spraying in malaria control and possible solutions. Malaria Journal 10. https://doi.org/10.1186/1475-2875-10-307.
Sinka ME, Golding N, Massey NC, Wiebe A, Huang Z, Hay SI and Moyes CL (2016) Modelling the relative abundance of the primary African vectors of malaria before and after the implementation of indoor, insecticide-based vector control. Malaria Journal 15. https://doi.org/10.1186/s12936-016-1187-8.
Sinka ME, Pironon S, Massey NC, Longbottom J, Hemingway J, Moyes CL and Willis KJ (2020) A new malaria vector in Africa: Predicting the expansion range of Anopheles stephensi and identifying the urban populations at risk. Proceedings of the National Academy of Sciences of the United States of America 117: 24900–24908. https://doi.org/10.1073/pnas.2003976117.
Slater HC, Foy BD, Kobylinski K, Chaccour C, Watson OJ, Hellewell J, Aljayyoussi G, Bousema T, Burrows J, D’Alessandro U, Alout H, Ter Kuile FO, Walker PGT, Ghani AC and Smit MR (2020) Ivermectin as a novel complementary malaria control tool to reduce incidence and prevalence: a modelling study. Lancet Infect Dis 20: 498–508. https://doi.org/10.1016/s1473-3099(19)30633-4.
Smith DL, Perkins TA, Tusting LS, Scott TW and Lindsay S (2013) Mosquito population regulation and larval source management in heterogeneous environments. PLoS One 8: e71247.
Soper FL and Wilson DB (1943) Anopheles gambiae in Brazil: 1930 to 1940. New York, The Rockefeller Foundation, 262 pp.
Sternberg ED, Cook J, Alou LPA, Assi SB, Koffi AA, Doudou DT, Aoura CJ, Wolie RZ, Oumbouke WA, Worrall E, Kleinschmidt I, N’Guessan R and Thomas MB (2021) Impact and cost-effectiveness of a lethal house lure against malaria transmission in central Cote d’Ivoire: a two-arm, cluster-randomised controlled trial. Lancet 397: 805–815. https://doi.org/10.1016/s0140-6736(21)00250-6.
Stopard IJ, Churcher TS and Lambert B (2021) Estimating the extrinsic incubation period of malaria using a mechanistic model of sporogony. Plos Computational Biology 17. https://doi.org/10.1371/journal.pcbi.1008658.
Sylla M, Kobylinski KC, Gray M, Chapman PL, Sarr MD, Rasgon JL and Foy BD (2010) Mass drug administration of ivermectin in south-eastern Senegal reduces the survivorship of wild-caught, blood fed malaria vectors. Malaria Journal 9. https://doi.org/10.1186/1475-2875-9-365.
Tanser FC, Sharp B and le Sueur D (2003) Potential effect of climate change on malaria transmission in Africa. Lancet 362: 1792–1798. https://doi.org/10.1016/s0140-6736(03)14898-2.
Thomas C (2004) Malaria – A changed climate in Africa? Nature 427: 690–691. https://doi.org/10.1038/427690b.
Thomas CJ, Davies G and Dunn CE (2004) Mixed picture for changes in stable malaria distribution with future climate in Africa. Trends in Parasitology 20: 216–220.
Tonnang HEZ, Tchouassi DP, Juarez HS, Igweta LK and Djouaka RF (2014) Zoom in at African country level: potential climate induced changes in areas of suitability for survival of malaria vectors. International Journal of Health Geographics 13: (20 May 2014).
Traore MM, Junnila A, Traore SF, Doumbia S, Revay EE, Kravchenko VD, Schlein Y, Arheart KL, Gergely P, Xue RD, Hausmann A, Beck R, Prozorov A, Diarra RA, Kone AS, Majambere S, Bradley J, Vontas J, Beier JC and Muller GC (2020) Large-scale field trial of attractive toxic sugar baits (ATSB) for the control of malaria vector mosquitoes in Mali, West Africa. Malaria Journal 19. https://doi.org/10.1186/s12936-020-3132-0.
Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD and Lindsay SW (2015) The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malaria Journal 14. https://doi.org/10.1186/S12936-015-0724-1.
Tusting LS, Thwing J, Sinclair D, Fillinger U, Gimnig JE, Bonner KE, Bottomley C and Lindsay S (2013) Mosquito larval source management for controlling malaria. Cochrane Database of Sytematic Reviews CD008923.
UNHCR (2022) Climate Risks Profile: Sahel, UN Refugee Agency.
Villena OC, Ryan SJ, Murdock CC and Johnson LB (2022) Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi. Ecology 103: e3685. https://doi.org/10.1002/ecy.3685.
von Seidlein L, Ikonomidis K, Bruun R, Jawara M, Pinder M, Knols BGJ and Knudsen JB (2012) Airflow attenuation and bed net utilization: observations from Africa and Asia. Malaria Journal 11. https://doi.org/10.1186/1475-2875-11-200.
Wagman JM, Varela K, Zulliger R, Saifodine A, Muthoni R, Magesa S, Chaccour C, Gogue C, Tynuv K, Seyoum A, Dengela D, Saute F, Richardson JH, Fornadel C, Linton YM, Slutsker L, Candrinho B and Robertson M (2021) Reduced exposure to malaria vectors following indoor residual spraying of pirimiphos-methyl in a high-burden district of rural Mozambique with high ownership of long-lasting insecticidal nets: entomological surveillance results from a cluster-randomized trial. Malaria Journal 20. https://doi.org/10.1186/s12936-021-03583-8.
Walker ED (1995) Effect of low-temperature on feeding rate of Aedes stimulans larvae and efficacy of Bacillus-thuringiensis var israelensis (H-14). Journal of the American Mosquito Control Association 11: 107–110.
Weiss DJ, Bertozzi-Villa A, Rumisha SF, Amratia P, Arambepola R, Battle KE, Cameron E, Chestnutt E, Gibson HS, Harris J, Keddie S, Millar JJ, Rozier J, Symons TL, Vargas-Ruiz C, Hay SI, Smith DL, Alonso PL, Noor AM, Bhatt S and Gething PW (2021) Indirect effects of the COVID-19 pandemic on malaria intervention coverage, morbidity, and mortality in Africa: a geospatial modelling analysis. Lancet Infect Dis 21: 59–69. https://doi.org/10.1016/s1473-099(20)30700-3.
WHO (2013) Larva source management: a supplementary measure for malaria vector control, WHO, Geneva.
WHO (2018) World Malaria Report, World Health Organization, Geneva.
WHO (2021a) Overview of the WHO Prequalification of Vector Control Products, Geneva.
WHO (2021b) World Malaria Report, 978-92-4-004049-6 Geneva.
WHO (2022) WHO Guidelines for Malaria, Geneva.
Worrall E and Fillinger U (2011) Large-scale use of mosquito larval source management for malaria control in Africa: a cost analysis. Malaria Journal 10. https://doi.org/10.1186/1475-2875-10-338.
Yadouleton A, N’Guessan R, Allagbe H, Asidi A, Boko M, Osse R, Padonou G, Kinde G and Akogbeto M (2010) The impact of the expansion of urban vegetable farming on malaria transmission in major cities of Benin. Parasites & Vectors 3. https://doi.org/10.1186/1756-3305-3-118.
Yamana TK, Bomblies A and Eltahir EAB (2016) Climate change unlikely to increase malaria burden in West Africa. Nature Climate Change 6: 1009-+. https://doi.org/10.1038/nclimate3085.
Yamana TK and Eltahir EAB (2013) Projected Impacts of Climate Change on Environmental Suitability for Malaria Transmission in West Africa. Environmental Health Perspectives 121: 1179–1186. https://doi.org/10.1289/ehp.1206174.