Secondary vectors of malaria include those anopheline species that are known to play minor part in malaria transmission. Primary vectors of malaria in Africa are Anopheles gambiae s.s, Anopheles coluzzii, Anopheles arabiensis, Anopheles funestus, Anopheles moucheti and Anopheles nili, while Anopheles rivolorum, Anopheles pharoensis, Anopheles ziemanni, among others are secondary vectors. They are recognized for their importance in malaria transmission, as they may help to augment or extend the malaria transmission period and potentially sustain malaria transmission after the main indoor resting and indoor biting vectors have been reduced by vector control measures such as indoor residual spraying or Long-lasting insecticidal nets (LLINs). Thus, the terminology “secondary” versus “primary” vector is fluid and forged by ecological conditions and malaria control strategies. Most secondary vectors are outdoor resting and outdoor biting are thus, not taken care of in the current control methods. High use of insecticides for vector control in Africa, climate change, unprecedented land use changes in Africa are some of the factors that could influence the conversion of secondary vectors to become main vectors in Africa. This chapter examines the role of secondary vectors in malaria transmission and the possibility of them becoming main vectors in future.
- secondary vectors
- main vectors
- malaria elimination
- residual malaria transmission
Malaria is still a major public health problem in sub-Saharan Africa despite the massive investment in intervention measures that have been rolled out within the last decade and have produced a decline of 37% of malaria cases . Main interventions include the scaling up of vector control through long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) , as well as the introduction of ACT and improved malaria diagnostic . Malaria transmission dynamics within sub-Saharan African countries is highly variable. Transmission can occur throughout the year (in particular with areas that receive rainfall twice a year) or only during a few months in the year (in particular with areas that has only one transmission season) and even then heterogeneities in transmission are observed between years within the same area. Inoculation rates vary from 0 to over a 1000 infective bites per year. Some areas have sole vectors that are involved in transmission of parasites to the human population while others could have several vectors that will consist of main vectors and secondary vectors. Differences in ecological requirements, longevity and feeding behavior (e.g. anthropophily and endophily) account for the different roles played by main and secondary vectors in malaria transmission in Africa .
Secondary vectors of malaria include those anopheline species that are known to play or suspected of playing a minor part in malaria transmission. With over 140 species of anopheline species in sub-Saharan Africa, <20 of them are able to transmit malaria to humans . There are some six species that are considered to be major malaria vectors that are responsible for 95% of the total malaria transmission on the continent . These are
The current malaria vector intervention tools are all indoor and insecticide based. This is because the main malaria vectors in Africa are majorly endophagic and endophilic. Secondary vectors that could be exophagic and exophilic or could bite earlier indoors before people sleep under their LLINs and those that move between being zoophilic (tendency to bite animals only) and anthropophilic (tendency to bite humans only) are left out of the current control methods. However, a few secondary vectors have been known historically to flourish and take over malaria transmission after the main vector(s) have been suppressed . High use of insecticides for vector control in Africa, climate change, unprecedented land use and land cover changes that is ongoing in many parts of Africa are some of the factors that could influence the conversion of secondary vectors to become main vectors in sub-Saharan Africa.
Secondary vectors are species that frequently have relatively little contact with man and are perhaps less likely to be affected by house-spraying with residual insecticides and the use of insecticide impregnated bednets than are the primary vectors. This chapter emphasizes the importance of such secondary vectors. It examines the role of secondary vectors in malaria transmission and the possibility of them becoming main vectors in future, as many countries in sub-Saharan Africa drive towards the elimination of the disease. It highlights the overall malaria parasite transmission intensity by these secondary vectors in several sites across Africa. Historical evidence is presented in this chapter to underscore the possibility of secondary vectors becoming main vectors. For instance,
2. Contribution of secondary vectors to malaria transmission in different parts of sub-Saharan Africa
Secondary vectors just like the main vectors are distributed all over sub-Saharan Africa. From Senegal in the west of Africa through Cameroun to Ethiopia and down to Angola, each country has a few of them that could be either transmitting malaria or not and all of them contributes to 5% of malaria transmission on the continent. They are therefore of importance to the sustenance of malaria transmission. Some secondary vectors have historically been known to be transmitting sporozoites of malaria parasites, albeit, at a lower rate whilst some vectors have been known to bite man but have not been found carrying malaria parasites. For instance, the
2.1. Western Africa
Around the Senegal River delta,
In Gambia, presumed secondary vectors are
In Baukina Faso, 3/3385 of
2.2. Central Africa
In irrigated rice fields in Goulmoun in south western Chad, four vectors were identified with a different human biting rate:
Cameroun seems to be the country with most secondary vectors implicated in malaria transmission. In northwest of Cameroon,
2.3. Eastern Africa
2.4. Southern Africa
Similarly, studies from Mozambique displayed high anthropophilic behavior with early peaks in foraging activity with
All these shows that these secondary vectors do assume anthropophilic behaviors, could get infected with plasmodium infection and could potentially become the main vector of malaria. Figure 1 shows a map of the distribution of all the secondary vectors discussed here in this review from sub-Saharan Africa.
3. Impact of land use and land cover changes on mosquito species proliferation
Environmental change is driving the expansion of numerous vector species and the intensification of pathogen transmission in many places in the world  because vectors respond sharply to changes in the ecology of their breeding habitat. These ecological changes include land use and land cover changes [37–40] which can change the environment within which the vector prefers to breed or the microclimate of the area within which certain vectors would tolerate . Malaria vectors could therefore invade a new area when the land use and land cover changes . Land cover changes and human settlement subsequent to deforestation has prompted an increase in the human-biting rate of formerly zoophilic vectors in several parts of the tropics and the instigation of upsurges in malaria transmission and malaria epidemics [40, 42]. Human settlement can increase malaria transmission if there are malaria infected people in among the settlers. Mitigating against the impacts of environmental change on malaria transmission will be particularly difficult when public health goals conflict with economic development. Economic development in many places in Africa is associated with extension of agricultural practices such as rice and sugar cane that are associated with extensive water bodies that favor the establishment of breeding sites for malaria vectors. Economic development has also been associated with deforestation, where the forest is cut down for housing and agricultural purposes. For instance in Guiana, following the elimination of malaria in the Demerara River Estuary by DDT spraying, the human population grew rapidly and land use activities switched from livestock herding to more profitable rice farming. This caused the formerly zoophilic
In many areas of Africa, the type of land use activity and the ecological context created after deforestation, determines which species of mosquito are able to remain and adapt, which ones disappear, and which new species are able to invade the place, that find the new habitat congenial to their survival and proliferation . Deforestation could enhance the vectorial capacity of malaria transmitting mosquitoes, and there was 29–106% increase in vectorial capacity for
Environmental pressures and climate change may bring about malaria vectors dynamism, which leads to some malaria vectors becoming more efficient in transmitting malaria . Manga et al. , working in an area that has been deforested to build a new airport in Cameroon, observed that deforestation caused the introduction of
Outside of the continent of Africa, Conn
4. Proliferation of mosquito species to higher altitudes due to climate change and climate variability
The highlands of Africa, where malaria incidence is on the rise, represent an ecological zone of special concern . The high rate of deforestation leads to rise in temperatures in highland areas [39, 52, 53]. Global climate warming could potentially make the high-altitude areas which used to be unsuitable for mosquito proliferation suitable for these mosquitoes to increase in density. Each vector has its own ecological niche requirement, and an important limiting factor for vector spatial distribution range is climate. A typical case in point, in the highlands of western Kenya, Zhou et al.  reported that the population of
In the Amani hills of Tanzania, Matola et al.  reported that malaria vectors were scarce on the Amani hills until the late 1960s, and it was generally presumed that any cases of malaria transmission must have been contracted by people visiting surrounding lower altitudes where malaria is holoendemic. However,
Even though these vectors are main and not secondary vectors, the fact that the highlands became permissible to their proliferation leading to increases in malaria transmission suggest that this could happen with secondary vectors. Some of these secondary vectors already live in the highland areas [30, 57] and therefore when conditions such as land use changes, climate change and reduction in interspecific competition from main vectors as a result of elimination or reduction in their population could trigger their proliferation. Others could migrate into the highlands from surrounding lowland areas when conditions such as those already discussed become permissible to their survival. Malaria vectors and non-vectors could periodically extend their range beyond their normal area of distribution.
5. Impact of intensive use of insecticides for public health interventions
Insecticides are the primary weapon against malaria vectors in the current malaria intervention paradigm. However, their prolonged use have been associated with the development of resistance by malaria vectors. Their intensive application has evolutionary implications evident in the number, behavior and physiology of the vectors. For numeric responses to intensive insecticide use, mosquito populations typically decrease in density because their longevity is reduced very much [58, 59]. For instance, studies carried out in western Kenya showed that,
The reduction in one target vector may trigger a cascade of ecological effects that could impede or enhance transmission by another. A notable examples include the apparent replacement of the highly anthropophilic and endophagic
Again, in Kenya, the inception of rigorous malaria control in the early part of the 2000s using LLINs saw dramatic changes of vector species. There has been a marked decline in the population of
These scenarios demonstrate that secondary vectors have the potential to occupy the niche left by main vectors after the latter’s elimination through intensive vector control in sub-Saharan Africa that relies solely on insecticides with the use of IRS and LLINs.
Malaria transmission in Africa is a dynamic and complex system that is continuously changing. Despite the substantial amount of work done on malaria epidemiology and control in Africa, there remains gaps in our understanding of the ecology and biology of secondary vectors. Further knowledge is required to improve control of the disease especially as many countries embark on rigorous campaign to move from control to elimination phase of malaria transmission. Currently, much attention has been given to the main malaria vectors with the promotion of high LLIN use and IRS application which mainly tackle indoor transmitting vectors. However, a very big public health problem in recent years is residual malaria transmission. This has been reported to be increasing in many parts of sub-Saharan Africa [68, 70]. Most often studies on residual malaria transmission tend to focus on the main malaria vectors. However, the secondary vectors discussed here are mostly exophagic and exophilic and therefore would be more involved in residual transmission. The contribution of these secondary vectors should be seen much more in influencing residual malaria transmission. Moreso when there is currently no intervention in the vector control paradigm to take care of residual malaria transmitting vectors. Other measures such as larviciding or larval source reduction that could tackle secondary vectors and residual malaria transmission have not receive much attention. There is a great need to understand the bioecology of secondary vectors and their contribution to malaria epidemiology in order to program intervention for them.
From the above review, it was seen that
Why the population densities of these secondary vectors have not been as much as the main vectors has received little attention in the research world. It could be that interspecific competition with the main vectors has not favored the secondary vectors. If this is true, then when main vectors are eliminated or their densities brought down by intervention, secondary vectors could assume the role of main vectors since there would not be any competition. However, Gillies  asserted that most secondary vectors do have a short lifespan with natural mortalities estimated to be around 50–60% per gonotrophic cycle. This could explain to an extent, why their population sizes have not been high in many places. However, it has been shown in several areas in sub-Saharan Africa that the rigorous LLIN distribution and IRS application for malaria control within the last decade has led to
Human behavior is identified to drive residual malaria transmission. In areas where it is warmer in some months of the year, some residents would want to sit outside of their house instead of being indoors for several hours of the night or sleep outside the whole night as happens in the north of Ghana . In such areas, if the main vectors are eliminated, it is more likely that secondary vectors would replace them since blood meal will be available outdoors and possible pathogen transmission would be enhanced. It has also been suggested that since many secondary vectors are exophagic and exophilic, they could potentially sustain transmission of malaria after the main endophagic and endophilic vectors have been reduced by indoor control measures such as IRS and LLIN use [3, 8, 14].
However, it is worth noting that a possible reason why these vectors have not been able to actively transmit malaria might be that these secondary vectors may not be as refractory to the development of Plasmodium parasites as the main vectors are. If this is true, then no matter how abundant their population might be, they may not be able to assume the responsibility as main vectors and actively increase malaria transmission.
It is worth to note that the co-occurrence of primary and secondary vectors at the same sites may lead to an increased risk of malaria transmission. High infection rates in the secondary vectors could also arise as a result of high malaria transmission maintained by the primary vectors and increased density of humans who maybe carrying gametocytes .
The implementation of any successful vector-control measures requires knowledge of the biology of the anopheline species present in the area to be targeted. The scientific world needs to be concerned with the bionomics, morphology and genetics of these secondary vectors, to be ready when they also step up their game to become main vectors. In addition, malaria control measures needs to take into account secondary vectors most of whom are exophagic and exophilic.