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.

INTRODUCTION

Mosquitoes, particularly those from the genera Aedes, Culex, and Anopheles, continue to be organisms of utmost concern in global public health [15]. 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 [811]. 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 [8].

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 [12]. 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 [13]. 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 [12]. 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 [12]. 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 [1519].

It was not until the 1880s, when Plasmodium parasites were identified as the causative agent of malaria, that mosquitoes were recognized as disease vectors [20]. 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 [20]. 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 [15]. Active areas of research for novel methods of control include genetically engineered mosquitoes that limit populations through the production of sterile offspring [2224]. 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 [24, 30].

CASE EXAMINATION

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, 3436]. 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 [3739].

FIGURE 1.

Generalized mosquito life cycle. Adult female mosquitoes will take a blood meal from a host and subsequently lay her eggs in water. These eggs are triggered to hatch by hypoxic conditions in the water, signaling that there is high bacterial density in the water, which will act as food for larvae. Once hatched, the mosquitoes will grow and develop through four instars (successively larger stages) until pupation occurs. Pupae then attempt to minimize energy expenditure as they finish developing the physiological structures of an adult mosquito. The pupae will eclose (similar to metamorphose) into fully developed adult mosquitoes and continue on the life cycle [16, 31, 36, 39–43].

FIGURE 1.

Generalized mosquito life cycle. Adult female mosquitoes will take a blood meal from a host and subsequently lay her eggs in water. These eggs are triggered to hatch by hypoxic conditions in the water, signaling that there is high bacterial density in the water, which will act as food for larvae. Once hatched, the mosquitoes will grow and develop through four instars (successively larger stages) until pupation occurs. Pupae then attempt to minimize energy expenditure as they finish developing the physiological structures of an adult mosquito. The pupae will eclose (similar to metamorphose) into fully developed adult mosquitoes and continue on the life cycle [16, 31, 36, 39–43].

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, 4448]. 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 [49]. 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, 5254]. 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

Introduction

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 [57].

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, 5860]. 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 [6265]. 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, 6972]. Predation in isolated patches can limit the abundance of mosquito populations significantly [73]. 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, 7678]. 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) [15].

FIGURE 2.

Mosquito ecology — predation, competition, and control methods impacting mosquito populations and disease transmission potential. The circular bubbles represent the mosquito life cycles at different stages (adult and larval) and in two major types of larval habitats. These are partially flowing water sources, such as streams and ponds, and stagnant water sources, such as tree hollows and tires. The arrows demonstrate the factors that reduce the mosquito population at each of the various life stages.

FIGURE 2.

Mosquito ecology — predation, competition, and control methods impacting mosquito populations and disease transmission potential. The circular bubbles represent the mosquito life cycles at different stages (adult and larval) and in two major types of larval habitats. These are partially flowing water sources, such as streams and ponds, and stagnant water sources, such as tree hollows and tires. The arrows demonstrate the factors that reduce the mosquito population at each of the various life stages.

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 [13]. 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 [13]. Clothing barriers, such as wearing long pants, can also reduce this biting risk by presenting a physical barrier for mosquitoes [81]. 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 [15]. 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 [13]. 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, 8790]. 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 [74]. 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 [60].

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 [72]. 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 [9597]. 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 [101104]. 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 [105], 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.

CONCLUSION

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

  1. 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.

  2. 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

  • 3.

    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.

  • 4.

    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.

    • Develop a 1- to 2-page control plan that addresses mosquito population control and community involvement in decision making.

  • 5.

    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.

AUTHOR CONTRIBUTIONS

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.

FUNDING

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.

COMPETING INTERESTS

The authors have declared that no competing interests exist.

SUPPORTING INFORMATION

File S1. Case study teaching notes supplement. (PDF)

REFERENCES

REFERENCES
1.
Camargo S. History of Aedes aegypti Eradication in the Americas.
Bull Org mond Sante Bull Wld Hlth Org [Internet]
.
1967
[cited 9 Dec 2017];
36
:
602
603
. Available: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2476393/pdf/bullwho00598-0087.pdf.
2.
CDC.
Estimated range of Aedes aegypti and Aedes albopictus in the US | Zika virus | CDC [Internet]
.
Centers for Disease Control and Prevention
.
2017
[cited 29 Nov 2017]. Available: https://www.cdc.gov/zika/vector/range.html.
3.
Fonseca DM, Keyghobadi N, Malcolm CA et al. Emerging vectors in the Culex pipiens complex.
Science [Internet]
.
American Association for the Advancement of Science
;
2004
Mar 5 [cited 9 Dec 2017];
303
(
5663
):
1535
1538
. Available: http://www.ncbi.nlm.nih.gov/pubmed/15001783.
4.
Briegel H. Fecundity, metabolism, and body size in Anopheles (Diptera: Culicidae), Vectors of Malaria.
J Med Entomol [Internet]
.
Oxford University Press
;
1990
Sep 1 [cited 6 May 2018];
27
(
5
):
839
850
. Available: https://academic.oup.com/jme/article-lookup/doi/10.1093/jmedent/27.5.839.
5.
WHO.
Mosquito-Borne Diseases [Internet]
.
WHO
:
World Health Organization
;
2016
[cited 2 May 2018]. Available: http://www.who.int/neglected_diseases/vector_ecology/mosquito-borne-diseases/en/.
6.
Liu-Helmersson J, Stenlund H, Wilder-Smith A, Rocklöv J. Vectorial capacity of Aedes aegypti: effects of temperature and implications for global dengue epidemic potential. Moreira LA, editor.
PLoS One [Internet]
.
Public Library of Science
;
2014
Mar 6 [cited 15 Sep 2018];9(3): e89783. doi:.
7.
Adams B, Kapan DD.
Man bites mosquito: understanding the contribution of human movement to vector-borne disease dynamics
.
PLoS One
.
2009
;
4
(
8
):
e6763
.
8.
Sachs J, Malaney P. The economic and social burden of malaria.
Nature [Internet]
.
2002
Feb 7 [cited 7 May 2018];
415
(
6872
):
680
685
. Available: http://www.nature.com/articles/415680a.
9.
Montibeler EE, de Oliveira DR. Dengue endemic and its impact on the gross national product of the Brazilian economy.
Acta Trop [Internet]
.
2018
[cited 16 Dec 2017];
178
:
318
326
. Available: http://linkinghub.elsevier.com/retrieve/pii/S0001706X17307684.
10.
Ramaiah KD, Das PK, Michael E, Guyatt HL. The economic burden of lymphatic Filariasis in India.
Parasitol Today [Internet]
. Elsevier Current Trends;
2000
Jun 1 [cited 7 May 2018];
16
(
6
):
251
253
. Available: https://www.sciencedirect.com/science/article/pii/S0169475800016434.
11.
Steelman CD, White TW, Schilling PE. Effects of mosquitoes on the average daily gain of feedlot steers in Southern Louisiana.
J Econ Entomol [Internet]
.
Oxford University Press
;
1972
Apr 1 [cited 7 May 2018];
65
(
2
):
462
466
. Available: http://academic.oup.com/jee/article/65/2/462/2210714/Effects-of-Mosquitoes-on-the-Average-Daily-Gain-of.
12.
WHO | Vector-Borne Diseases
.
WHO [Internet]
.
World Health Organization
;
2017
[cited 9 Dec 2017]; Available: http://www.who.int/mediacentre/factsheets/fs387/en/.
13.
World Health Organization
.
World Malaria Report 2016 – English summary [Internet]
.
2017
[cited 14 Sep 2018]. Available: http://apps.who.int/bookorders.
14.
US Centers for Disease Control and Prevention
.
CDC – Malaria’s impact worldwide [Internet]
.
CDC
.
2018
[cited 2 Sep 2018]. Available: https://www.cdc.gov/malaria/malaria_worldwide/impact.html.
15.
Rose RI. Pesticides and public health: integrated methods of mosquito management.
Emerg Infect Dis [Internet]
.
Centers for Disease Control and Prevention
;
2001
[cited 28 Mar 2019];
7
(
1
):
17
23
. Available: http://www.ncbi.nlm.nih.gov/pubmed/11266290.
16.
Brady OJ, Godfray HCJ, Tatem AJ et al.
Adult vector control, mosquito ecology and malaria transmission
.
Int Health
.
2015
;
7
(
2
):
121
129
.
17.
Ng’habi K, Viana M, Matthiopoulos J, Lyimo I, Killeen G, Ferguson HM. Mesocosm experiments reveal the impact of mosquito control measures on malaria vector life history and population dynamics.
Sci Rep [Internet]
.
Nature Publishing Group
;
2018
Dec 17 [cited 20 Sep 2018];
8
(
1
):
13949
. Available: http://www.nature.com/articles/s41598-018-31805-8.
18.
Yakob L, Walker T. Zika virus outbreak in the Americas: the need for novel mosquito control methods.
Lancet Glob Heal [Internet]
.
Elsevier
;
2016
Mar 1 [cited 28 Mar 2019];
4
(
3
):
e148
e149
. Available: https://linkinghub.elsevier.com/retrieve/pii/S2214109X16000486.
19.
Baldacchino F, Bussola F, Arnoldi D et al. An integrated pest control strategy against the Asian tiger mosquito in northern Italy: a case study.
Pest Manage Sci [Internet]
.
John Wiley & Sons, Ltd
;
2017
Jan 1 [cited 28 Mar 2019];
73
(
1
):
87
93
. doi:.
20.
Gachelin G, Garner P, Ferroni E, Verhave JP, Opinel A. Evidence and strategies for malaria prevention and control: a historical analysis.
Malar J [Internet]
.
BioMed Central
;
2018
Feb 27 [cited 28 Mar 2019];
17
(
1
):
96
. Available: http://www.ncbi.nlm.nih.gov/pubmed/29482556.
22.
Wang S, Dos-Santos ALA, Huang W et al. Driving mosquito refractoriness to Plasmodium falciparum with engineered symbiotic bacteria.
Science [Internet]
.
American Association for the Advancement of Science
;
2017
Sep 29 [cited 9 Dec 2017];
357
(
6358
):
1399
1402
. Available: http://www.ncbi.nlm.nih.gov/pubmed/28963255.
23.
Pike A, Dong Y, Dizaji NB, Gacita A, Mongodin EF, Dimopoulos G.
Changes in the microbiota cause genetically modified Anopheles to spread in a population
.
Science
.
2017
;
357
(
6358
):
1396
1399
.
24.
Meghani Z, Boëte C. Genetically engineered mosquitoes, Zika and other arboviruses, community engagement, costs, and patents: ethical issues. Pimenta P, editor.
PLoS Negl Trop Dis [Internet]
.
Public Library of Science
;
2018
Jul 26 [cited 28 Mar 2019];
12
(
7
):
e0006501
. doi:.
25.
McMeniman CJ, Lane R V, Cass BN et al. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti.
Science [Internet]
.
American Association for the Advancement of Science
;
2009
Jan 2 [cited 9 Dec 2017];
323
(
5910
):
141
144
. Available: http://www.ncbi.nlm.nih.gov/pubmed/19119237.
26.
Hoffmann AA, Montgomery BL, Popovici J et al.
Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission
.
Nature
.
2011
;
476
(
7361
):
454
.
27.
Emami SN, Ranford-Cartwright LC, Ferguson HM. The transmission potential of malaria-infected mosquitoes (An. gambiae-Keele, An. arabiensis-Ifakara) is altered by the vertebrate blood type they consume during parasite development.
Sci Rep [Internet]
.
Nature Publishing Group
;
2017
Jan 17 [cited 7 May 2018];
7
:
40520
. Available: http://www.nature.com/articles/srep40520.
28.
Verhulst NO, Qiu YT, Beijleveld H et al. Composition of human skin microbiota affects attractiveness to malaria mosquitoes. Schneider BS, editor.
PLoS One [Internet]
.
Public Library of Science
;
2011
Dec 28 [cited 7 May 2018];
6
(
12
):
e28991
. doi:.
29.
Li C, Lu Y, Liu J, Wu X. Climate change and dengue fever transmission in China: evidences and challenges.
Sci Total Environ [Internet]
.
2017
Dec 5 [cited 15 Dec 2017];
622–623
:
493
501
. Available: http://www.ncbi.nlm.nih.gov/pubmed/29220773.
30.
Rochlin I, Ninivaggi DV., Hutchinson ML, Farajollahi A. Climate change and range expansion of the Asian Tiger mosquito (Aedes albopictus) in Northeastern USA: implications for Public Health Practitioners. Oliveira PL, editor.
PLoS One [Internet]
.
Public Library of Science
;
2013
Apr 2 [cited 9 Dec 2017];
8
(
4
):
e60874
. doi:.
31.
Crans WJ. A classification system for mosquito life cycles: life cycle types for mosquitoes of the northeastern United States.
2004
[cited 13 Dec 2017]; Available: https://pdfs.semanticscholar.org/0a2d/3db372987ef00d954a52ca42ae0ed94002e5.pdf.
32.
Moller-Jacobs LL, Murdock CC, Thomas MB. Capacity of mosquitoes to transmit malaria depends on larval environment.
Parasit Vectors [Internet]
.
BioMed Central
;
2014
Dec 14 [cited 7 May 2018];
7
(
1
):
593
. http://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-014-0593-4.
33.
Briegel H. Physiological bases of mosquito ecology.
J Vector Ecol [Internet]
.
2003
;
28
(
1
):
1
11
. Available: http://sove.org/Journal/Entries/2003/6/1_Volume_28,_Number_1_files/Briegel.pdf.
34.
Gjullin CM, Hegarty CP, Bollen WB. The necessity of a low oxygen concentration for the hatching of Aedes mosquito eggs.
J Cell Comp Physiol [Internet]
.
The Wistar Institute of Anatomy and Biology
;
1941
Apr 1 [cited 13 Dec 2017];
17
(
2
):
193
202
. doi:.
35.
Judson CL. The physiology of hatching of Aedine mosquito eggs: hatching stimulus.
Ann Entomol Soc Am [Internet]
.
Oxford University Press
;
1960
Sep 1 [cited 13 Dec 2017];
53
(
5
):
688
691
. Available: https://academic.oup.com/aesa/article-lookup/doi/10.1093/aesa/53.5.688.
36.
Ponnusamy L, Böröczky K, Wesson DM, Schal C, Apperson CS. Bacteria stimulate hatching of yellow fever mosquito eggs. Leulier F, editor.
PLoS One [Internet]
.
Public Library of Science
;
2011
Sep 6 [cited 14 Sep 2018];
6
(
9
):
e24409
. doi:.
37.
Hillyer JF. Insect immunology and hematopoiesis.
Dev Comp Immunol [Internet]
.
2016
[cited 27 Apr 2018];
58
:
102
118
. Available: https://ac.els-cdn.com/S0145305X15300896/1-s2.0-S0145305X15300896-main.pdf?_tid=150457e0-0521-4cf3-9d2d-66d15821c2ea&acdnat=1524851452_3a4375e5a2d199a52f5d0d6f4345520b
38.
Dennison NJ, Jupatanakul N, Dimopoulos G. The mosquito microbiota influences vector competence for human pathogens.
Curr Opin Insect Sci [Internet]
.
NIH Public Access
;
2014
Sep 1 [cited 29 Mar 2018];
3
:
6
13
. Available: http://www.ncbi.nlm.nih.gov/pubmed/25584199.
39.
League GP, Hillyer JF. Functional integration of the circulatory, immune, and respiratory systems in mosquito larvae: pathogen killing in the hemocyte-rich tracheal tufts.
BMC Biol [Internet]
.
BioMed Central
;
2016
Dec 19 [cited 27 April 2018];
14
(
1
):
78
. Available: http://bmcbiol.biomedcentral.com/articles/10.1186/s12915-016-0305-y.
40.
7th Son Studio
. Close up mosquito pupae and larvae underwater – image [Internet].
Shutterstock
; n.d. Available: https://www.shutterstock.com/image-photo/close-mosquito-pupae-larvae-underwater-134180195.
41.
7th Son Studio
. Close up mosquito eggs hatch in water – image [Internet].
Shutterstock
; n.d. Available: https://www.shutterstock.com/image-photo/close-mosquito-eggs-hatch-water-134182007.
42.
7th Son Studio
. Mosquito larva – image [Internet].
Shutterstock
; n.d. Available: https://www.shutterstock.com/image-photo/mosquito-larva-582013186.
43.
Oteera. Culex mosquito bite and sucking human blood. macro shot. – image [Internet].
Shutterstock
; n.d. Available: https://www.shutterstock.com/image-photo/culex-mosquito-bite-sucking-human-blood-1006706152.
44.
Braks MAH, Hon Rio NA, Lounibos LP, Lourenç R, De-Oliveira O, Juliano SA.
Interspecific competition between two invasive species of container mosquitoes, Aedes aegypti and Aedes albopictus (Diptera: Culicidae), in Brazil
.
Ann Entomol Soc Am
.
2004
;
97
(
1
):
130
139
.
45.
Lee SH, Nam KW, Jeong JY et al. The effects of climate change and globalization on mosquito vectors: evidence from Jeju Island, South Korea on the potential for Asian Tiger mosquito (Aedes albopictus) influxes and survival from Vietnam rather than Japan. Schnell MJ, editor.
PLoS One [Internet]
.
Public Library of Science
;
2013
Jul 24 [cited 11 Dec 2017];
8
(
7
):
e68512
. doi:.
46.
Hawley W, Reiter P, Copeland R, Pumpuni C, Craig G.
Aedes albopictus in North America: probable introduction in used tires from northern Asia
.
Science
.
1987
;
236
(
4805
):
1114
1116
.
47.
Novakova E, Woodhams DC, Rodríguez-Ruano SM et al.
Mosquito microbiome dynamics, a background for prevalence and seasonality of West Nile virus
.
Front Microbiol
.
2017
;
8
(
Apr
):
526
.
48.
Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M. Fighting malaria with engineered symbiotic bacteria from vector mosquitoes.
PNAS [Internet]
.
2012
[cited 29 Mar 2018];
109
(
31
):
1734
1739
. Available: http://www.pnas.org/content/pnas/109/31/12734.full.pdf.
49.
D’Antonio M, Spielman A.
Mosquito: A Natural History of Our Most Persistent and Deadly Foe
. 1st ed.
New York
:
Hyperion
;
2001
.
50.
Benedict MQ, Levine RS, Hawley WA, Lounibos LP. Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus.
Vector Borne Zoonotic Dis [Internet]
.
NIH Public Access
;
2007
[cited 9 Dec 2017];
7
(
1
):
76
85
. Available: http://www.ncbi.nlm.nih.gov/pubmed/17417960.
51.
Alto BW, Lounibos LP. Vector Competence for Arboviruses in Relation to the Larval Environment of Mosquitoes. In:
Ecology of Parasite-Vector Interactions [Internet]
.
Wageningen
:
Wageningen Academic Publishers
;
2013
[cited 7 May 2018]. pp.
81
101
. Available: http://link.springer.com/10.3920/978-90-8686-744-8_4.
52.
US Centers for Disease Control and Prevention. CDC – Malaria – Anopheles mosquitoes [Internet].
2015
[cited 5 Jul 2018]. Available: https://www.cdc.gov/malaria/about/biology/mosquitoes/index.html#.
53.
Bayoh MN, Lindsay SW. Temperature-related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory.
Med Vet Entomol [Internet]
.
Wiley/Blackwell
(10.1111);
2004
Jun 1 [cited 15 Sep 2018];
18
(
2
):
174
179
. doi:.
54.
Paaijmans KP, Imbahale SS, Thomas MB, Takken W. Relevant microclimate for determining the development rate of malaria mosquitoes and possible implications of climate change.
Malar J [Internet]
.
BioMed Central
;
2010
Jul 9 [cited 9 Dec 2017];
9
(
1
):
196
. Available: http://malariajournal.biomedcentral.com/articles/10.1186/1475-2875-9-196.
55.
Wang Y, Gilbreath TM, Kukutla P, Yan G, Xu J. Dynamic Gut Microbiome across Life History of the Malaria Mosquito Anopheles gambiae in Kenya. Leulier F, editor.
PLoS One [Internet]
.
Public Library of Science
;
2011
Sep 21 [cited 29 Mar 2018];
6
(
9
):
e24767
. doi:.
56.
57.
van den Berg H. Global status of DDT and its alternatives for use in vector control to prevent disease.
Environ Health Perspect [Internet]
.
National Institute of Environmental Health Science
;
2009
Nov [cited 30 March 2019];
117
(
11
):
1656
1663
. Available: http://www.ncbi.nlm.nih.gov/pubmed/20049114.
58.
Milam D, Farris J, Wilhide J. Evaluating mosquito control pesticides for effect on target and nontarget organisms.
Arch Environ Contam Toxicol [Internet]
.
Springer-Verlag
;
2000
Sep 1 [cited 9 Dec 2017];
39
(
3
):
324
328
. Available: http://link.springer.com/10.1007/s002440010111.
59.
Wilson C, Tisdell C.
Why farmers continue to use pesticides despite environmental, health and sustainability costs
.
Ecol Econ
.
2001
;
39
(
3
):
449
462
.
60.
Williamson S, Ball A, Pretty J. Trends in pesticide use and drivers for safer pest management in four African countries.
Crop Prot [Internet]
.
Elsevier
;
2008
Oct 1 [cited 31 March 2018];
27
(
10
):
1327
1334
. Available: https://www.sciencedirect.com/science/article/pii/S0261219408000884.
61.
Juliano SA, Philip Lounibos L.
Ecology of invasive mosquitoes: effects on resident species and on human health
.
Ecol Lett
.
2005
;
8
(
5
):
558
574
.
62.
Livdahl TP. Competition within and between hatching chorots of a treehole mosquito.
Ecology [Internet]
.
Ecological Society of America
;
1982
Dec 1 [cited 13 December 2017];
63
(
6
):
1751
. Available: http://www.jstor.org/stable/1940117?origin=crossref.
63.
Braks MAH, Honório NA, Lounibos LP, Lourenço-De-Oliveira R, Juliano SA. Interspecific competition between two invasive species of container mosquitoes, Aedes aegypti and Aedes albopictus (Diptera: Culicidae), in Brazil. doi: [Internet].
2009
Jan 24 [cited 9 December 2017]; Available from: http://www.bioone.org/doi/abs/10.1603/0013-8746%282004%29097%5B0130%3AICBTIS%5D2.0.CO%3B2?journalCode=esaa.
64.
Juliano SA. Species introduction and replacement among mosquitoes: interspecific resource competition or apparent competition?
Source Ecol [Internet]
.
1998
;
79
(
1
):
255
268
. Available: http://www.jstor.org/stable/176880.
65.
Merritt R, Dadd R, Walker E. Feeding behavior, natural food, and nutritional relationships of larval mosquitoes.
Annu Rev Entomol [Internet]
.
1992
[cited 5 December 2017];
37
(
1
):
349
376
. Available: https://www.researchgate.net/profile/Edward_Walker2/publication/21808918_Merritt_RW_Dadd_RH_Walker_ED_Feeding_behavior_natural_food_and_nutritional_relationships_of_larval_mosquitoes_Annu_Rev_Entomol_37_349-376/links/0046352ff3d7a30930000000/Merritt-RW-Da.
66.
Alto BW, Lounibos LP, Mores CN, Reiskind MH. Larval competition alters susceptibility of adult Aedes mosquitoes to dengue infection.
Proceedings Biol Sci [Internet]
.
The Royal Society
;
2008
Feb 22 [cited 9 December 2017];
275
(
1633
):
463
471
. Available: http://www.ncbi.nlm.nih.gov/pubmed/18077250.
67.
Edgerly JS, Willey MS, Livdahl TP. The community ecology of Aedes egg hatching: implications for a mosquito invasion.
Ecol Entomol [Internet]
.
Blackwell Publishing
Ltd;
1993
May 1 [cited 9 December 2017];
18
(
2
):
123
128
. doi:.
68.
Alto BW, Lounibos LP, Higgs S, Juliano SA. Larval competition differentially affects arbovirus infection in Aedes mosquitoes.
Ecology [Internet]
.
NIH Public Access
;
2005
Dec [cited 9 December 2017];
86
(
12
):
3279
3288
. Available: http://www.ncbi.nlm.nih.gov/pubmed/19096729.
69.
Reiskind MH, Wund MA. Experimental assessment of the impacts of Northern long-eared bats on Ovipositing Culex (Diptera: Culicidae) mosquitoes.
J Med Entomol [Internet]
.
2009
[cited 1 December 2017];
46
(
5
):
1037
1044
. Available: https://watermark.silverchair.com/jmedent46-1037.pdf?token=AQECAHi208BE49Ooan9kkhW_Ercy7Dm3ZL_9Cf3qfKAc485ysgAAAaswggGnBgkqhkiG9w0BBwagggGYMIIBlAIBADCCAY0GCSqGSIb3DQEHATAeBglghkgBZQMEAS4wEQQMlNkUcJ751NiXm0yhAgEQgIIBXn-A5eCYUUMNomWrGILNEYJ8RgUoiZI8PU4FOZDm.
70.
Saha N, Aditya G, Saha GK, Hampton SE.
Opportunistic foraging by heteropteran mosquito predators
.
Aquat Ecol
.
2010
;
44
:
167
176
.
71.
Wetzler G, Boyles J. The energetics of mosquito feeding by insectivorous bats.
Can J Zool [Internet]
.
2017
Dec 2 [cited 15 December 2017];cjz-2017-0162. Available: http://www.nrcresearchpress.com/doi/10.1139/cjz-2017-0162.
72.
Carlson J, Keating J, Mbogo CM, Kahindi S, Beier JC. Ecological limitations on aquatic mosquito predator colonization in the urban environment.
J Vector Ecol [Internet]
.
NIH Public Access
;
2004
Dec [cited 15 September 2018];
29
(
2
):
331
339
. Available: http://www.ncbi.nlm.nih.gov/pubmed/15707292.
73.
Chase JM, Shulman RS. Wetland isolation facilitates larval mosquito density through the reduction of predators.
Ecol Entomol [Internet]
.
Blackwell Publishing Ltd
;
2009
Dec 1 [cited 9 December 2017];
34
(
6
):
741
747
. doi:.
74.
Almeida RM, Han BA, Reisinger AJ, Kagemann C, Rosi EJ. High mortality in aquatic predators of mosquito larvae caused by exposure to insect repellent.
Biol Lett [Internet]
.
2018
[cited 28 March 2019];
14
:
1
5
. Available: https://royalsocietypublishing.org/doi/pdf/10.1098/rsbl.2018.0526?casa_token=dAqDdFxmF5oAAAAA:8×3HqgglaWiYMVK5C7IZQ-xwL-mzdDq8td5YMMgC9XnmptbhLJfMiqdBX3IywzhvED_tCabaRdWFnp4
75.
Storer TI. Bats, bat towers, and mosquitoes.
J Mammology [Internet]
.
1926
[cited 9 December 2017];
7
(
2
):
85
90
. Available: http://www.jstor.org/stable/pdf/1373673.pdf.
76.
Wong S, Lau S, Woo P, Yuen K-Y. Bats as a continuing source of emerging infections in humans.
Rev Med Virol [Internet]
.
John Wiley & Sons
, Ltd.;
2007
Mar 1 [cited 9 December 2017];
17
(
2
):
67
91
. doi:.
77.
Pourrut X, Souris M, Towner JS et al. Large serological survey showing cocirculation of Ebola and Marburg viruses in Gabonese bat populations, and a high seroprevalence of both viruses in Rousettus aegyptiacus.
BMC Infect Dis [Internet]
.
BioMed Central
;
2009
Dec 28 [cited 15 September 2018];
9
(
1
):
159
. Available: http://bmcinfectdis.biomedcentral.com/articles/10.1186/1471-2334-9-159.
78.
Leendertz SAJ, Gogarten JF, Düx A, Calvignac-Spencer S, Leendertz FH.
Assessing the evidence supporting fruit bats as the primary reservoirs for Ebola viruses. Ecohealth [Internet]
.
Springer
US;
2016
Mar 13 [cited 15 September 2018];
13
(
1
):
18
25
. Available: http://link.springer.com/10.1007/s10393-015-1053-0.
79.
Milam CD, Farris JL, Wilhide JD. Evaluating mosquito control pesticides for effect on target and nontarget organisms.
Arch Environ Contam Toxicol [Internet]
.
Springer-Verlag
;
2000
Sep 1 [cited 29 March 2018];
39
(
3
):
324
328
. Available: http://link.springer.com/10.1007/s002440010111.
80.
Lacey LA, Undeen AH. Microbial control of black flies and mosquitoes. [cited
2018
May 9]; Available: https://www.annual reviews.org/doi/pdf/10.1146/annurev.en.31.010186.001405.
81.
US Centers for Disease Control and Prevention
. Avoid bug bites | Travelers’ Health | CDC [Internet].
2016
[cited 18 September 2017]. Available: https://wwwnc.cdc.gov/travel/page/avoid-bug-bites.
82.
Ferguson NM, Cucunubá ZM, Dorigatti I et al. Countering the Zika epidemic in Latin America.
Science [Internet]
.
American Association for the Advancement of Science
;
2016
Jul 22 [cited 13 December 2017];
353
(
6297
):
353
354
. Available: http://www.ncbi.nlm.nih.gov/pubmed/27417493.
83.
Mouchès C, Pasteur N, Bergé JB et al. Amplification of an esterase gene is responsible for insecticide resistance in a California Culex mosquito.
Science [Internet]
.
American Association for the Advancement of Science
;
1986
Aug 15 [cited 28 March 2019];
233
(
4765
):
778
780
. Available: http://www.ncbi.nlm.nih.gov/pubmed/3755546.
84.
Smith LB, Kasai S, Scott JG. Pyrethroid resistance in Aedes aegypti and Aedes albopictus: important mosquito vectors of human diseases.
Pestic Biochem Physiol [Internet]
.
Academic Press
;
2016
Oct 1 [cited 28 March 2019];
133
:
1
12
. Available: https://www.sciencedirect.com/science/article/abs/pii/S0048357516300220.
85.
Fradin MS, Day JF. Comparative efficacy of insect repellents against mosquito bites.
N Engl J Med [Internet]
.
Massachusetts Medical Society
;
2002
Jul 4 [cited 15 September 2018];
347
(
1
):
13
18
. doi:.
86.
Barnard DR, Xue R-D. Laboratory evaluation of mosquito repellents against Aedes albopictus, Culex nigripalpus, and Ochlerotatus triseriatus (Diptera: Culicidae).
J Med Entomol [Internet]
.
Oxford University Press
;
2004
Jul 1 [cited 15 September 2018];
41
(
4
):
726
730
. Available: https://academic.oup.com/jme/article-lookup/doi/10.1603/0022-2585-41.4.726.
87.
Kamel F, Engel LS, Gladen BC, Hoppin JA, Alavanja MCR, Sandler DP. Neurologic symptoms in licensed private pesticide applicators in the agricultural health study.
Environ Health Perspect [Internet]
.
National Institute of Environmental Health Science
;
2005
Jul [cited 31 March 2018];
113
(
7
):
877
882
. Available: http://www.ncbi.nlm.nih.gov/pubmed/16002376.
88.
Pimentel D, Acquay H, Biltonen M et al. Environmental and economic costs of pesticide use.
Bioscience [Internet]
.
Oxford University Press American Institute of Biological Sciences
;
1992
Nov [cited 31 March 2018];
42
(
10
):
750
760
. Available: https://academic.oup.com/bioscience/article-lookup/doi/10.23 07/1311994.
89.
Garry VF, Danzl TJ, Tarone R, Griffith J, Cervenka J, Krueger L, et al. Chromosome rearrangements in fumigant appliers: possible relationship to non-Hodgkin’s lymphoma risk.
Cancer Epidemiol Biomarkers Prev [Internet]
.
American Association for Cancer Research
;
2004
Apr 1 [cited 31 March 2018];
1
(
4
):
287
291
. Available: http://www.ncbi.nlm.nih.gov/pubmed/1303128.
90.
Cassidy RA, Natarajan S, Vaughan GM. The link between the insecticide heptachlor epoxide, estradiol, and breast cancer.
Breast Cancer Res Treat [Internet]
.
Kluwer Academic Publishers
;
2005
Mar [cited 28 March 2019];
90
(
1
):
55
64
. Available: http://link.springer.com/10.1007/s10549-004-2755-0.
91.
Goodsell JA, Kats LB. Effect of introduced mosquitofish on Pacific treefrogs and the role of alternative prey.
Conserv Biol [Internet]
.
Wiley/Blackwell
(10.1111);
1999
Aug 1 [cited 15 September 2018];
13
(
4
):
921
924
. doi:.
92.
Toohey MK, Goettel MS, Takagi M, Ram RC, Prakash G, Pillai JS. Field studies on the introduction of the mosquito predator Toxorhynchites Amboinensis (Diptera: Culicidae) into FIJI1.
J Med Entomol [Internet]
.
Oxford University Press
;
1985
Jan 18 [cited 15 September 2018];
22
(
1
):
102
110
. Available: https://academic.oup.com/jme/article-lookup/doi/10.1093/jmedent/22.1.102.
93.
Ingabire CM, Hakizimana E, Rulisa A et al. Community-based biological control of malaria mosquitoes using Bacillus thuringiensis var. israelensis (Bti) in Rwanda: community awareness, acceptance and participation.
Malar J [Internet]
.
BioMed Central
;
2017
Dec 3 [cited 7 February 2018];
16
(
1
):
399
. Available: http://malariajournal.biomedcentral.com/articles/10.1186/s12936-017-2046-y.
94.
Becker N. The use of Bacillus Thuringiensis Subsp. Israelensis (Bti) against mosquitoes, with special emphasis on ecological impact.
Isr J Entomol [Internet]
.
1998
[cited 29 March 2018];
XXXH
:
63
69
. Available: http://www.entomology.org.il/sites/default/files/pdfs/IJE-1998.Becker.pdf.
95.
Guidi V, Lehner A, Lüthy P, Tonolla M. Dynamics of Bacillus thuringiensis var. israelensis and Lysinibacillus sphaericus Spores in Urban Catch Basins after Simultaneous Application against Mosquito Larvae. Bourtzis K, editor.
PLoS One [Internet]
.
Public Library of Science
;
2013
Feb 4 [cited 16 December 2017];
8
(
2
):
e55658
. doi:.
96.
Baumann P, Clark MA, Baumann L, Broadwell AH. Bacillus sphaericus as a mosquito pathogen: properties of the organism and its toxins.
Microbiol Rev [Internet]
.
1991
Sep [cited 9 May 2018];
55
(
3
):
425
436
. Available: http://www.ncbi.nlm.nih.gov/pubmed/1682792.
97.
Goldberg LJ, Margalit J. A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univitattus, Aedes aegypti, and Culex pipiens.
Mosq News [Internet]
.
1977
[cited 12 November 2017];
37
(
3
):
355
358
. Available: https://www.biodiversitylibrary.org/content/part/JAMCA/MN_V37_N3_P355-358.pdf.
98.
Ernst KC, Haenchen S, Dickinson K et al. Awareness and support of release of genetically modified “sterile” mosquitoes, Key West, Florida, USA.
Emerg Infect Dis [Internet]
.
Centers for Disease Control and Prevention
;
2015
Feb [cited 16 December 2017];
21
(
2
):
320
324
. Available: http://www.ncbi.nlm.nih.gov/pubmed/25625795.
99.
Sinkins SP, Gould F. Gene drive systems for insect disease vectors.
Nat Rev Genet [Internet]
.
Nature Publishing Group
;
2006
Jun 9 [cited 15 September 2018];
7
(
6
):
427
435
. Available: http://www.nature.com/doifinder/10.1038/nrg1870.
100.
Hammond A, Galizi R, Kyrou K et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae.
Nat Biotechnol [Internet]
.
Nature Publishing Group
;
2016
Jan 7 [cited 15 September 2018];
34
(
1
):
78
83
. Available: http://www.nature.com/articles/nbt.3439.
101.
McMeniman CJ, Lane R V, Cass BN et al. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti.
Science [Internet]
.
American Association for the Advancement of Science
;
2009
Jan 2 [cited 17 May 2018];
323
(
5910
):
141
144
. Available: http://www.ncbi.nlm.nih.gov/pubmed/19119237.
102.
Murray J V, Jansen CC, De Barro P. Risk associated with the release of Wolbachia-infected Aedes aegypti mosquitoes into the environment in an effort to control dengue.
Front public Heal [Internet]
.
Frontiers Media SA
;
2016
[cited 16 December 2017];
4
:
43
. Available: http://www.ncbi.nlm.nih.gov/pubmed/27047911.
103.
Bian G, Joshi D, Dong Y et al. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection.
Science [Internet]
.
American Association for the Advancement of Science
;
2013
May 10 [cited 6 May 2018];
340
(
6133
):
748
751
. Available: http://www.ncbi.nlm.nih.gov/pubmed/23661760.
104.
Hoffmann AA, Montgomery BL, Popovici J et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission.
2011
[cited 29 March 2018]; Available: http://web.uvic.ca/~starzom/Hoffmann_etal_2011.pdf.
105.
Krugman P, Venables AJ. Globalization and the inequality of nations.
Q J Econ [Internet]
.
Oxford University Press
;
1995
Nov 1 [cited 11 December 2017];
110
(
4
):
857
880
. Available: https://academic.oup.com/qje/article-lookup/doi/10.2307/2946642.
106.
Gubler Daniel J. Dengue, urbanization, and globalization: the unholy trinity of the 21st Century.
Trop Med Health [Internet]
.
2011
[cited 11 December 2017];
39
(
4
):
3
11
. Available: https://www.jstage.jst.go.jp/article/tmh/39/4SUPPLEMENT/39_2011-S05/_pdf.
107.
Epstein PR, Diaz HF, Elias S et al. Biological and physical signs of climate change: focus on mosquito-borne diseases.
Bull Am Meteorol Soc [Internet]
.
1998
Mar 1 [cited 9 December 2017];
79
(
3
):
409
417
. Available: http://journals.ametsoc.org/doi/abs/10.1175/1520-0477%281998%29079%3C0409%3ABAPSOC%3E2.0.CO%3B2.
108.
Gildenhard M, Rono EK, Diarra A et al. Mosquito microevolution drives Plasmodium falciparum dynamics.
Nat Microbiol [Internet]
.
Nature Publishing Group
;
2019
Mar 25 [cited 31 March 2019];1. Available: http://www.nature.com/articles/s41564-019-0414-9.
109.
Beketov MA, Kefford BJ, Schäfer RB, Liess M. Pesticides reduce regional biodiversity of stream invertebrates.
PNAS [Internet]
.
2013
[cited 30 March 2019];
110
(
27
):
11039
11043
. doi:.
110.
Purdue MP, Hoppin JA, Blair A, Dosemeci M, Alavanja MCR. Occupational exposure to organochlorine insecticides and cancer incidence in the Agricultural Health Study.
Int J Cancer [Internet]
.
John Wiley & Sons, Ltd
;
2007
Feb 1 [cited 28 March 2019];
120
(
3
):
642
649
. doi:.
111.
Cole DC, Orozco FA, Ibrahim S, Wanigaratne S. Community and household socioeconomic factors associated with pesticide-using, small farm household members’ health: a multi-level, longitudinal analysis.
Int J Equity Health [Internet]
.
BioMed Central
;
2011
Nov 17 [cited 30 March 2019];
10
(
1
):
54
. Available from: http://equityhealthj.biomedcentral.com/articles/10.1186/1475-9276-10-54.

Supplementary data