Globally, mosquitoes have the propensity to severely impact public health by transmitting infectious agents that can lead to diseases, such as malaria, dengue fever, chikungunya, Zika fever, and West Nile fever. To develop appropriate control and mitigation measures for controlling the spread of mosquito-borne disease, we need to better understand ecological influences on mosquitoes, including competition, predation, and interactions with the environment. Building novel and environmentally conscious strategies has become increasingly important under the threat of potential range expansion with climate change and increased global connectivity. As a result of this case study and answering the corresponding questions, readers will be able to identify modern approaches to mosquito control based on an ecological understanding of these disease vectors. Readers will actively engage in scenarios where they will balance trade-offs between public health and environmental health, while considering the breadth of factors involved in global mosquito control efforts.
Mosquitoes, particularly those from the genera Aedes, Culex, and Anopheles, continue to be organisms of utmost concern in global public health [1–5]. Some mosquitoes are known as disease vectors or organisms that can transmit and spread infection from one organism to another without experiencing severe symptoms themselves [3, 6, 7]. Certain genera of mosquitoes can transmit malaria, Zika, chikungunya, dengue, and yellow fever, along with a multitude of other diseases [2, 5]. Globally, mosquito-borne diseases have a major impact on human social and economic systems including reduced fertility, early mortality, lowered productivity of workers, and a decrease in savings and investment from workers impacted by disease-related medical expenses [8–11]. A study by Sachs and Malaney found that countries with high rates of malaria have a gross domestic product (GDP) fivefold less than those without intensive malaria, signifying the wide-reaching effect that mosquito-borne diseases have beyond health impacts .
Vector-borne disease, which includes mosquito-borne disease, is an area of high interest in public health, as it accounts for nearly 17% of infectious disease annually . In 2016, for example, there were 212 million new cases of malaria around the world, resulting in 429,000 deaths, primarily in Africa and of children under the age of 5 years . Despite this, there has been an overall reduction in global malaria mortality by 29% between 2010 and 2015, indicating that current programs in mosquito control have made substantial progress [13, 14]. Limitations to further reduction of malaria include insecticide resistance, anti-malarial drug resistance, and economic constraints in resource-limited tropical areas [13, 15, 16]. Moreover, 3.8 billion people are at risk of contracting dengue hemorrhagic fever annually . Some mosquitoes can carry various other transmissible disease agents, leading to infection of human and wildlife hosts (such as birds) with Zika, West Nile, chikungunya, yellow fever, and Japanese encephalitis viruses . The variety of pathogens that mosquitoes can carry and spread to other organisms makes controlling mosquito populations a focal aspect in plans for reducing these diseases [15–19].
It was not until the 1880s, when Plasmodium parasites were identified as the causative agent of malaria, that mosquitoes were recognized as disease vectors . Many early mosquito control methods, implemented following World War I, focused on physical barriers to biting, such as wire screens on windows [20, 21]. Some other early methods included the use of crushed flowers and roots of plants that produced early versions of pyrethroid pesticides, the use of “Paris Green” (copper acetoarsenite) and the introduction of larval predators (fish) to mosquito habitats . While some of these methods are still widely used today, these fell out of favor for new, synthetic pesticides due to increased efficacy, and later, health, safety, and sometimes cost [15, 20]. Many pesticides used today for mosquito control were first developed approximately 50 years ago and have been periodically subjected to thorough safety and efficacy reevaluations in the United States . Active areas of research for novel methods of control include genetically engineered mosquitoes that limit populations through the production of sterile offspring [22–24]. Microbial manipulation, with microbes like Wolbachia that demonstrate some evidence of reducing fecundity and blocking transmission (or, the spread) of viruses in some species of mosquitoes, has shown promise as a new technique [25, 26].
Everything from environmental conditions to mosquito species and age to human blood type, carbon dioxide output, and host skin microbiome influences mosquito-borne pathogen transmission [27, 28]. The complexity of transmission dynamics makes mitigating disease quite difficult, even with diverse methods of control available [16, 29]. In this case study, we will provide background about mosquito disease vectors, as well as describe methods of mosquito control being implemented across the world to reduce mosquito-borne pathogen transmission. We will focus primarily on three genera of human disease vector mosquitoes that can be found globally: Aedes, Culex, and Anopheles [2–4, 30].
Mosquito Life Cycle
Generalized Life Cycle
The life histories and developmental stages of mosquitoes determine the control methods to be used [15, 20, 31, 32]. Many mosquitoes lay their eggs in semi-stagnant water and hatching is triggered by hypoxic (low-oxygen) conditions upon bacterial consumption of oxygen in the water column. The type of habitat where eggs are laid and hatch depends largely on genus, as Culex tend to be fairly hardy in polluted, anoxic systems, whereas Anopheles require well-oxygenated water with lower bacterial density [4, 32, 33]. Once the eggs hatch, the mosquito larvae will then grow through four larval stages until they pupate and eclose (metamorphose) into adults. Adults feed on flower nectar and to aid in egg development, females will blood feed multiple times on vertebrate hosts and lay eggs (Figure 1) [31, 34–36]. This blood feeding stage is where female mosquitoes will potentially become infected with pathogens and parasites, which can then establish in the female mosquito and spread to the next host when the female blood feeds again, undergoing several rounds of reproduction within a lifespan [37–39].
Aedes and Culex: Container and Tree-Hole Breeders
Aedes and Culex mosquitoes lay their eggs in either natural or human-made containers, where bacteria aid in the hatching of eggs and act as food for larvae. Many of these mosquitoes live in close association with humans (with the exception of some species and sylvatic, or forest, ecotypes) and can act as disease vectors [1, 3, 36, 44–48]. Historically, Aedes aegypti, the yellow fever mosquitoes native to Africa are thought to have invaded new continents, including North America, sometime before 1650 via ships during the slave trade . Currently, A. aegypti is found across the world in tropical and subtropical regions, whereas Aedes albopictus, the Asian tiger mosquito, is invading new habitats globally through the introduction by the tire trade [46, 50]. While A. albopictus tends to be a poorer vector than A. aegypti for most viruses, it is still able to transmit viruses as its invasive geographic range expands to include naive hosts unfamiliar with the pathogens it carries [6, 45, 50, 51]. Culex pipiens (sub: pipiens or quinquefasciatus; the Northern House Mosquito) is a mosquito species found in all continents, which breeds in polluted and stagnant waters (or containers) in urban settings, and can transmit viruses from birds to mammals through blood feeding (including West Nile and eastern encephalitis) [3, 47].
Anopheles: Pool, Pond, and Stream Breeders
Anopheline mosquitoes lay their eggs in freshly formed rainwater pools, ponds, or slow-moving streams, where the eggs hatch a few days later and the resulting larvae live and feed on the water surface microlayer [4, 32, 52–54]. Anopheles mosquitoes tend to prefer cleaner water habitats than Aedes or Culex, and are more sensitive to changes in environmental conditions. Female Anopheles mosquitoes can become infected with the malaria parasite Plasmodium when they take a blood meal from an infected host, and then can spread the parasite to other hosts upon its next feeding. While not all species of Anopheles can carry and transmit Plasmodium, the species that have high contact rates with humans, namely the Anopheles gambiae species complex, typically do [4, 52, 55].
Understanding Mosquito Ecology for Planning Effective Control Strategies
Ecological concepts can help to guide appropriate mosquito control measures. Historical methods for mosquito control, such as the application of DDT or by petrolizing stagnant water, had adverse impacts on abiotic environmental health and on non-target species (e.g., fragile eggshells in bald eagles and other birds), ultimately leading to detrimental ecological consequences and the disuse of these methods [1, 20, 56], although approximately 14 countries still use DDT .
While modern approaches attempt to minimize downstream impacts on the abiotic and biotic ecosystem, improper application or misuse of modern methods can still cause problems [15, 58–60]. Embracing ecological principles that influence mosquitoes can help us to better understand and control pathogen transmission, as well as develop novel methods for control. Two of the most impactful pressures on mosquitoes in nature are competition and predation, as these can shape distribution, abundance, dispersal, and other population- and community-level dynamics. By understanding how mosquito species interact with each other and with their environment, including climate and microbes, we can develop more environmentally friendly and simultaneously more effective ways of controlling vector mosquitoes.
Competition and Predation
Interspecific competition at the various stages of mosquito development can play a role in development and success later in life, as well as the overall structure of the local and regional mosquito community [33, 61, 62]. Resource limitations within larval habitats lead to competition between mosquitoes [62–65]. Competition between species in these small container habitats can be exceptionally intense and can vary spatially by depth [33, 64, 66, 67]. In Aedes spp. breeding habitats, A. albopictus larvae will intensely outcompete A. aegypti larvae to the point of exclusion (and on a broader regional scale, competitive replacement), where A. aegypti can only survive in containers where A. albopictus is absent, with high resource availability and low intraspecific competition [44, 61, 62, 64]. Interspecific competition can also influence the adult mosquitoes’ relative infection load (in terms of viral titers) when competitive stress is high [66, 68], leading to a potentially higher risk of anthropogenic viral transmission by affected mosquitoes [51, 66, 68].
While competition can structure mosquito communities and lead to changes in pathogen infection loads, predation pressure has the ability to limit the abundance and density of mosquitoes in the environment and is actively used as a method for mosquito population reduction at multiple life stages [19, 69–72]. Predation in isolated patches can limit the abundance of mosquito populations significantly . Mosquitoes are subjected to predation pressure from different sources at various points in their life cycle. As larvae, mosquitoes are heavily preyed upon by freshwater invertebrates, as well as amphibians and fish [70, 74]. As adults, mosquitoes can be preyed upon by multiple insectivores, but bats have been contentiously held as a major predator of adult mosquitoes [71, 75, 76]. Bats are an interesting focal predator for the pathogen-transmitting mosquitoes, as they act as a reservoir for several pathogens, such as rabies and Ebola viruses, though these diseases are not transmitted by mosquitoes [71, 76–78]. Bats and freshwater invertebrates should be of particular research interest in limiting mosquitoes that typically act as vectors for disease, as they have the potential to alter community dynamics between mosquito species and potentially decrease viral loads [66, 68, 75, 76].
Methods for Mosquito Control
Three major categories of classification for mosquito control are physical, chemical, and biological methods [5, 16, 60, 79, 80]. Each category has multitudes of sub-categories and can target the mosquito in terms of reducing population size or reducing disease transmission potential. These definitions are broad, but they help to break down major strategies being employed in integrated pest management plans — the synergistic use of multiple methods to create a more successful control outcome. The mosquito life cycle (Figure 1) also dictates that control methods should be used for optimal results, as larvicides and adulticides are specific to those life stages (Figure 2) .
Physical Control Methods
Physical mosquito control methods include barrier-style methods of vector bite prevention and physical acts to reduce the number of mosquitoes in a local population. One of the most effective methods of controlling the spread of the mosquito-borne disease has been the implementation of insecticide-treated bed nets, which physically cover sleeping individuals and present a barrier to limit the ability of mosquitoes to access a host . While the insecticides are a chemical deterrent, the physical barrier helps to prevent bites, and the increased implementation of these nets in areas of high mosquito-borne disease risk has helped to reduce global transmission rates . Clothing barriers, such as wearing long pants, can also reduce this biting risk by presenting a physical barrier for mosquitoes . Window screens are also very helpful in reducing the movement of mosquitoes from outside of the home into the home and help to reduce contact rates with humans. A more active form of physical control is dumping standing water where mosquito eggs and larvae can incubate, as well as filling in areas that typically flood during rainstorms (including tire tracks) to prevent the formation of favorable habitat for mosquitoes [5, 12, 13, 82]. Wetland draining and mosquito-ditching to remove standing water from areas experiencing high transmission rates of vector-borne diseases are also employed in control strategies, though current usage of this approach has decreased as it is often environmentally degrading and expensive [15, 20, 73].
Chemical Control Methods
Chemical mosquito control methods include application of pesticides intended to reduce populations of vectors or deter them from biting. Organophosphates and pyrethroids are classes of pesticides utilized for mosquito control, specifically as adulticides, which can be applied over large areas and near homes to reduce mosquito populations . However, the widespread use of these pesticides has also led to widespread resistance, which lowers their efficacy when they are applied [15, 83, 84]. Switching from pyrethroid pesticides to newer (and frequently more costly) pesticides has led to a decrease in indoor residual spraying (IRS), which potentially leaves people at risk of bites and infection with pathogens . Common personal pesticides, such as DEET and picaridin, are fairly effective in repelling most species of mosquito and can greatly reduce the risk of bites [81, 85]. While there are claims that some other types of natural mosquito deterrents are effective, most of these have not shown equivalent efficacy in laboratory trials [85, 86].
One major issue with several types of chemical mosquito control is the potential for downstream human health and environmental health impacts, such as the increase in cancer rates among professional pesticide appliers and indirect effects on non-target species of arthropods [58, 60, 87–90]. Salamanders and other potential predators of mosquito larvae can also be adversely impacted by application of these substances to habitats, such as the increased mortality seen in salamanders subjected to low levels of picaridin in a recent study . Despite these risks, chemical control of mosquitoes remains one of our greatest tools in battling the mosquito-borne disease, particularly when these risks are minimized through integrated pest management plans .
Biological Control Methods
Biological mosquito control methods include ecological manipulation (i.e., introduction of predators), microbial-based larvicides, or direct or semi-direct vector or pathogen manipulation. The introduction or promotion of mosquito predators, such as bats, amphibians, mosquitofish, or dragonflies, can be an effective way of reducing mosquito-borne disease through population reduction [71, 72, 74, 91, 92]. While supporting habitat and other ecological needs of mosquito predators already in a system can be an excellent way to promote control, introducing new predators risks ecological consequences downstream and can create problems in the trophic cascade of an ecosystem . Biological larvicides are a method of mosquito control that have been employed globally and are effective at reducing larval populations of mosquitoes [93, 94]. These biological larvicides consist of bacteria, such as Bacillus thuringiensis israelensis or Lysinibacillus sphaericus, which can be applied directly or are lysed and have their endotoxins applied to corncob pieces and are applied to larval mosquito habitats. When the mosquito larvae consume the bacteria or the endotoxin, they form crystals in their guts that lead to mortality [95–97]. Another emerging method of mosquito control is creating and releasing genetically modified male mosquitoes that ultimately lead to a reduction in mosquito populations due to non-viable offspring being produced [22, 24, 48, 98]. Recent research on gene drives may also lead to large scale reductions in mosquito populations [99, 100]. Another experimental method of control is the introduction of Wolbachia, an intracellular bacterium found in arthropods that can reduce mosquito populations by interfering with reproduction and can interfere with pathogens that would otherwise infect the mosquito [101–104]. While we are still early in the development and implementation of many of these biological methods of control, many of them seem to hold promise when utilized in an integrated management strategy.
Considerations for Control Plans
With increasing globalization through trade and travel , mosquito-borne diseases pose a mounting threat to human populations and an increasingly complex mitigation challenge [9, 45, 106]. With increased global connectivity and potential range expansion under climate change regimes [45, 54, 106, 107], understanding how these mosquitoes function within their environment can give us insights about how to better control the spread of mosquito-borne diseases. Other major considerations for selecting an appropriate form of mosquito control are safety, efficacy, cost, evolution of resistance, and public perception [15, 24, 60, 108]. For example, pesticides have improved most control agents, have moved away from using DDT, petrolization, and Paris Green as these had adverse effects on non-target organisms, including birds and humans [15, 20, 56, 57]. Novel and sometimes improved strategies can be costly to bring to market and maintain use over time, such as in the case of genetically engineered mosquitoes being released to reduce viable offspring in Brazil [24, 25]. Most currently used strategies were created 50 or more years ago (with limited data on efficacy and safety in some cases), so new strategies will continue to be necessary despite the cost and economic difficulty to commercialize, due to improving safety standards and emergent resistance issues [15, 20, 24]. Costs associated with control strategies include direct costs (purchasing, developing, and implementing) to places that use them, but also indirect costs, such as removal of mosquito predators and loss of invertebrate biodiversity [17, 74, 109]. Financial costs and issues with health inequity, especially in economically disadvantaged countries, are factors that need to be considered when developing appropriate control measures [24, 89, 90, 110, 111]. Control methods that do not account for these factors will likely be ineffective. Understanding mosquito ecology and current control methods will aid in the development of novel or improved control mechanisms and tools for implementing them efficiently.
Mosquito-borne disease has a major impact on public health and socioeconomic systems worldwide. The three major disease vector genera are Aedes, Culex, and Anopheles. Aedes and Culex primarily transmit viruses, while Anopheles primarily spreads Plasmodium spp., which are the parasites that cause malaria. In addition, modern mosquito control methods consist of three major classes: physical control, chemical control, and biological control. There are a multitude of methods for controlling both mosquito populations and the transmission of pathogens that they carry among these three major classes of control. While there is no perfect “silver bullet” for mosquito control, integrated pest management plans can help to make these methods work in tandem to lead to more successful outcomes around the world.
CASE STUDY QUESTIONS
Is one of the major categories of mosquito control more effective than the others? Does one of the major categories of control have a greater environmental impact than the others? Support your conclusions.
If mosquito-borne disease could be reduced by half globally, what do you see as some potential health, social, and/or economic outcomes? Do you think that these outcomes would differ by region or country? Why or why not?
Using books, newspapers, academic papers, or reputable websites (such as CDC.gov), look up and consider mosquito-borne pathogen risks specific to your geographic area. Consider why these risks may be relevant to your region.
At times, it can be challenging to develop a new control plan. Of the control methods discussed here, what combination of two or three methods do you think would be a good integrated pest management strategy for where you live? Why?
Scenarios for Applied Learning
Scenario 1: You are an academic expert that has been asked to develop a series of suggestions for controlling an outbreak of malaria in a resource-limited, rural, subtropical area. You must be conscious of cost limitations and try to minimize the number and expense of efforts that you would recommend implementing.
Develop a 1- to 2-page control plan that addresses mosquito population control and community involvement in decision making.
Scenario 2: You are a governmental official deciding which mosquito control methods to implement for an annual control plan that will expand over the next 10 years. The public in the area that you are recommending control measures for tends to hold natural systems in high esteem and are concerned about how these measures will affect migratory birds and other native fauna in the area that are a big tourist attraction and thus contribute significantly to the local economy.
Scenario 3: You are a mosquito control expert and have just seen reports that A. albopictus has been detected and confirmed in your area for the first time. You have to develop a series of suggestions for the public in mitigating the risks of contracting mosquito-borne disease from this species.
Develop a 1- to 2-page control plan that addresses mosquito contact prevention and recommendations for the public.
AT-P was responsible for the conceptualization, literature review, and preparation of this manuscript. DW revised and prepared portions of the manuscript. IT and AC developed the figures and helped to review the manuscript.
We would like to thank Megan Fung and Ross Whetstone for their feedback on this manuscript. We would also like to thank the reviewers of this manuscript for their helpful comments and suggestions.
AT-P was supported by National Science Foundation grant DGE 1249946, Integrative Graduate Education and Research Traineeship (IGERT): Coasts and Communities — Natural and Human Systems in Urbanizing Environments, the University of Massachusetts Sanofi-Genzyme Doctoral Fellowship, the Craig R. Bollinger Memorial Research Grant, the Nancy Goranson Endowment Fund, and the University of Massachusetts Global Programs Office Seed Grant Fund. DW was supported by the UMass Boston Proposal Development Grant Program.
The authors have declared that no competing interests exist.
File S1. Case study teaching notes supplement. (PDF)