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

Background

Climate change affects the survival and transmission of arthropod vectors as well as the development rates of vector-borne pathogens. Increased international travel is also an important factor in the spread of vector-borne diseases (VBDs) such as dengue, West Nile, yellow fever, chikungunya, and malaria. Dengue is the most important vector-borne viral disease. An estimated 2.5 billion people are at risk of infection in the world and there are approximately 50 million dengue infections and an estimated 500,000 individuals are hospitalized with dengue haemorrhagic fever annually. The Asian tiger mosquito (Aedes albopictus) is one of the vectors of dengue virus, and populations already exist on Jeju Island, South Korea. Currently, colder winter temperatures kill off Asian tiger mosquito populations and there is no evidence of the mosquitos being vectors for the dengue virus in this location. However, dengue virus-bearing mosquito vectors can inflow to Jeju Island from endemic area such as Vietnam by increased international travel, and this mosquito vector''s survival during colder winter months will likely occur due to the effects of climate change.

Methods and Results

In this section, we show the geographical distribution of medically important mosquito vectors such as Ae. albopictus, a vector of both dengue and chikungunya viruses; Culex pipiens, a vector of West Nile virus; and Anopheles sinensis, a vector of Plasmodium vivax, within Jeju Island, South Korea. We found a significant association between the mean temperature, amount of precipitation, and density of mosquitoes. The phylogenetic analyses show that an Ae. albopictus, collected in southern area of Jeju Island, was identical to specimens found in Ho Chi Minh, Vietnam, and not Nagasaki, Japan.

Conclusion

Our results suggest that mosquito vectors or virus-bearing vectors can transmit from epidemic regions of Southeast Asia to Jeju Island and can survive during colder winter months. Therefore, Jeju Island is no longer safe from vector borne diseases (VBDs) due to the effects of globalization and climate change, and we should immediately monitor regional climate change to identify newly emerging VBDs.     

Decoupling of active and passive reasons for the invasion dynamics of Aedes albopictus Skuse (Diptera: Culicidae): Comparisons of dispersal history in the Apennine and Florida peninsulas

Aedes albopictus is an important vector of several diseases including dengue‐ and Chikungunya fever and is a potential vector of Zika‐fever. The invasion dynamics of Aedes albopictus was reconsidered by comparing the temperature‐related development of the mosquito with the observed real geographical distribution in Florida and in Italy. The potential number of generations and the annual dispersal distances of the mosquito were calculated for the estimates. The estimated total dispersals are 3.6–4.6 km/year/generation in Italy and 4.6–5.3 km/year/generation in Florida, values that are at least five to six times higher than those derived from release and recapture studies and from the previously measured flying distances of female Asian tiger mosquitoes. Subtracting the calculated dispersal distances with the known active dispersal of female Ae. albopictus, the passive dispersal component of the total dispersal distances was found to be 2.8–4.1 km/year/generation in Italy and 3.8–4.8 km/year/generation in Florida. Our results confirm that the active dispersal of female mosquitoes plays a secondary role in determining the rate of areal expansion and, in contrast, passive factors may play a primary role. It was concluded, based on similar average values of the passive dispersal distances of the mosquito in Florida and Italy, that at large spatial scales the anthropogenic component can be well estimated.     

Climate Change and Range Expansion of the Asian Tiger Mosquito (Aedes albopictus) in Northeastern USA: Implications for Public Health Practitioners

The Asian tiger mosquito, Aedes albopictus (Skuse), is an invasive species with substantial biting activity, high disease vector potential, and a global distribution that continues to expand. New Jersey, southern New York, and Pennsylvania are currently the northernmost boundary of established Ae. albopictus populations in the eastern United States. Using positive geographic locations from these areas, we modeled the potential future range expansion of Ae. albopictus in northeastern USA under two climate change scenarios. The land area with environmental conditions suitable for Ae. albopictus populations is expected to increase from the current 5% to 16% in the next two decades and to 43%–49% by the end of the century. Presently, about one-third of the total human population of 55 million in northeastern USA reside in urban areas where Ae. albopictus is present. This number is predicted to double to about 60% by the end of the century, encompassing all major urban centers and placing over 30 million people under the threat of dense Ae. albopictus infestations. This mosquito species presents unique challenges to public health agencies and has already strained the resources available to mosquito control programs within its current range. As it continues to expand into areas with fewer resources and limited organized mosquito control, these challenges will be further exacerbated. Anticipating areas of potential establishment, while planning ahead and gathering sufficient resources will be the key for successful public health campaigns. A broad effort in community sanitation and education at all levels of government and the private sector will be required until new control techniques are developed that can be applied efficiently and effectively at reasonable cost to very large areas.     

Is Switzerland Suitable for the Invasion of Aedes albopictus?

Background

Over the last 30 years, the Asian tiger mosquito, Aedes albopictus, has rapidly spread around the world. The European distribution comprises the Mediterranean basin with a first appearance in Switzerland in 2003. Early identification of the most suitable areas in Switzerland allowing progressive invasion by this species is considered crucial to suggest adequate surveillance and control plans.

Methodology/Principal Findings

We identified the most suitable areas for invasion and establishment of Ae. albopictus in Switzerland. The potential distribution areas linked to the current climatic suitability were assessed using remotely sensed land surface temperature data recorded by the MODIS satellite sensors. Suitable areas for adult survival and overwintering of diapausing eggs were also identified for future climatic conditions, considering two different climate change scenarios (A1B, A2) for the periods 2020–2049 and 2045–2074. At present, the areas around Lake Geneva in western Switzerland provide suitable climatic conditions for Ae. albopictus. In northern Switzerland, parts of the Rhine valley, around Lake Constance, as well as the surroundings of Lake Neuchâtel, appear to be suitable for the survival at least of adult Ae. albopictus. However, these areas are characterized by winters currently being too cold for survival and development of diapausing eggs. In southern Switzerland, Ae. albopictus is already well-established, especially in the Canton of Ticino. For the years 2020–2049, the predicted possible spread of the tiger mosquito does not differ significantly from its potential current distribution. However, important expansions are obtained if the period is extended to the years 2045–2074, when Ae. albopictus may invade large new areas.

Conclusions/Significance

Several parts of Switzerland provide suitable climatic conditions for invasion and establishment of Ae. albopictus. The current distribution and rapid spread in other European countries suggest that the tiger mosquito will colonize new areas in Switzerland in the near future.     

Forest canopy,water level,and biopesticide interact to determine oviposition habitat selection in Aedes albopictus

Understanding how interacting abiotic and biotic factors influence colonization rates into different habitat types is critical for both conserving and controlling species. For example, the rapid global spread of Asian tiger mosquitoes, Aedes albopictus, has reduced native species abundances and produced disease outbreaks. Fortunately, bacterial endospores of two Bacillus species (biospesticide) are highly lethal to Ae. albopictus larvae and have been commercially developed to reduce populations. Oviposition habitat selection is the first defense Ae. albopictus females possess against any control substance added to breeding sites, and considerable variation exists in their response to biopesticides. In a field experiment, I crossed the presence/absence of biopesticides, with two canopy (open, closed) and water (high, low) levels at 64 breeding sites, to examine if these interacted to influence oviposition site choice. Avoidance of biopesticide was most pronounced in closed canopy sites and those with low water levels, as all main effects and two‐way interactions influenced oviposition. Oviposition habitat selection represents a possible mechanism of resistance to biopesticides and other methods used to kill mosquito larvae. Future experiments examining how larval density and mortality modify these results should allow for more effective control of this highly invasive species.     

Multiple introductions and overwintering shape the progressive invasion of Aedes albopictus beyond the Alps

Aedes albopictus originates from Southeast Asia and is considered one of the most invasive species globally. This mosquito is a nuisance and a disease vector of significant public health relevance. In Europe, Ae. albopictus is firmly established and widespread south of the Alps, a mountain range that forms a formidable biogeographic barrier to many organisms. Recent reports of Ae. albopictus north of the Alps raise questions of (1) the origins of its recent invasion, and (2) if this mosquito has established overwintering populations north of the Alps. To answer these questions, we analyzed population genomic data from >4000 genome‐wide SNPs obtained through double‐digest restriction site‐associated DNA sequencing. We collected SNP data from specimens from six sites in Switzerland, north and south of the Alps, and analyzed them together with specimens from other 33 European sites, five from the Americas, and five from its Asian native range. At a global level, we detected four genetic clusters with specimens from Indonesia, Brazil, and Japan as the most differentiated, whereas specimens from Europe, Hong Kong, and USA largely overlapped. Across the Alps, we detected a weak genetic structure and high levels of genetic admixture, supporting a scenario of rapid and human‐aided dispersal along transportation routes. While the genetic pattern suggests frequent re‐introductions into Switzerland from Italian sources, the recovery of a pair of full siblings in two consecutive years in Strasbourg, France, suggests the presence of an overwintering population north of the Alps. The suggestion of overwintering populations of Ae. albopictus north of the Alps and the expansion patterns identified points to an increased risk of further northward expansion and the need for increased surveillance of mosquito populations in Northern Europe.     

Crouching Tiger,Hidden Trouble: Urban Sources of Aedes albopictus (Diptera: Culicidae) Refractory to Source-Reduction

Our ultimate objective is to design cost-effective control strategies for Aedes albopictus, the Asian tiger mosquito, an important urban nuisance and disease vector that expanded worldwide during the last 40 years.  We conducted mosquito larval surveys from May through October 2009 in the City of Trenton, New Jersey, USA, while performing intensive monthly source-reduction campaigns that involved removing, emptying, or treating all accessible containers with larvicides and pupicides. We examined patterns of occurrence of Ae. albopictus and Culex pipiens, another urban mosquito, among different container types by comparing observed and expected number of positive containers of each type. Expected use was based on the relative frequency of each container type in the environment. Aedes albopictus larvae and pupae were found significantly more often than expected in medium volumes of water in buckets and plant saucers but were rarely collected in small volumes of water found in trash items such as discarded cups and cans. They were also absent from large volumes of water such as in abandoned swimming pools and catch basins, although we consistently collected Cx. pipiens from those habitats. The frequency of Ae. albopictus in tires indicated rapid and extensive use of these ubiquitous urban containers. Standard larval-based indices did not correlate with adult catches in BG-Sentinel traps, but when based only on Ae. albopictus key containers (buckets, plant saucers, equipment with pockets of water, and tires) they did. Although we found that only 1.2% of the 20,039 water-holding containers examined contained immature Ae. albopictus (5.3% if only key containers were counted), adult populations were still above nuisance action thresholds six times during the 2009 mosquito season. We conclude that in urban New Jersey, effective source reduction for Ae. albopictus control will require scrupulous and repeated cleaning or treatment of everyday use containers and extensive homeowner collaboration.     

Evidence of Habitat Structuring Aedes albopictus Populations in Réunion Island

Arbovirus vector dynamics and spread are influenced by climatic, environmental and geographic factors. Major Chikungunya and Dengue fever outbreaks occurring the last 10 years have coincided with the expansion of the mosquito vector Aedes albopictus to nearly all the continents. We characterized the ecological (larval development sites, population dynamics, insemination and daily survival rates) and genetic (diversity, gene flow, population structure) features of two Aedes albopictus populations from distinct environments (rural and urban) on Réunion Island, in the South-West Indian Ocean. Microsatellite analysis suggests population sub-structuring Ae. albopictus populations. Two genetic clusters were identified that were significantly linked to natural versus urban habitats with a mixed population in both areas. Ae. albopictus individuals prefer urban areas for mating and immature development, where hosts and containers that serve as larval development sites are readily available and support high population densities, whereas natural environments appear to serve as reservoirs for the mosquito.     

Duration and dose-dependency of female sexual receptivity responses to seminal fluid proteins in Aedes albopictus and Ae. aegypti mosquitoes

Male mosquitoes transfer seminal fluid proteins (hereafter ‘SFPs’) during mating. These proteins can have profound effects on female behavior in the yellow fever mosquito Aedes aegypti and the Asian tiger mosquito Aedes albopictus. SFPs are thought to be responsible for female refractoriness to mating in both species. However, only limited information is available about the duration of induced refractoriness or the quantity of SFPs required to be effective in Ae. albopictus. Here, we tested the duration of the effect of SFPs on female refractory behavior for both Aedes species. Additionally, we determined the lowest SFP dose required to induce female refractory behavior in Ae. aegypti. Virgin females were injected intra-thoracically with doses ranging from 0.25 to 0.008 equivalents of one male’s SFP amount. Our results demonstrate high sensitivity of female Ae. aegypti and Ae. albopictus to SFPs of their own species, with the majority of females becoming refractory at doses ? 0.031 male-equivalents after injection into the hemocoel. This effect was long-lasting in both species; none of the injected females were inseminated when presented with males of their own species 30 to 34 days post-injection, whereas most saline-injected control females mated at this time point. These results will aid future work to characterize individual SFPs involved in post-mating refractoriness in these two species. Moreover, they show that as is the situation in the mosquito Anopheles gambiae, and unlike Drosophila melanogaster, sperm are not required for the maintenance of a sexual refractoriness response in Ae. aegypti and Ae. albopictus.     

Female-specific flightless (fsRIDL) phenotype for control of Aedes albopictus

Background

Aedes albopictus, the Asian tiger mosquito, is a vector of several arboviruses including dengue and chikungunya, and is also a significant nuisance mosquito. It is one of the most invasive of mosquitoes with a relentlessly increasing geographic distribution. Conventional control methods have so far failed to control Ae. albopictus adequately. Novel genetics-based strategies offer a promising alternative or aid towards efficient control of this mosquito.

Methodology/Principal Findings

We describe here the isolation, characterisation and use of the Ae. albopictus Actin-4 gene to drive a dominant lethal gene in the indirect flight muscles of Ae. albopictus, thus inducing a conditional female-specific late-acting flightless phenotype. We also show that in this context, the Actin-4 regulatory regions from both Ae. albopictus and Ae. aegypti can be used to provide conditional female-specific flightlessness in either species.

Conclusion/Significance

With the disease-transmitting females incapacitated, the female flightless phenotype encompasses a genetic sexing mechanism and would be suitable for controlling Ae. albopictus using a male-only release approach as part of an integrated pest management strategy.     

The role of priority effects in limiting the success of the invasive tiger mosquito,Aedes albopictus

Priority effects (PE), wherein species colonizing a habitat early have a negative impact on later colonizers, can have profound and legacy effects on community organization. In temperate zones, larval mosquito habitats are emptied each year in the winter and recolonized in the spring. There are phenological differences among common species but the role of PE in these communities is largely unexplored. Aedes albopictus, the invasive tiger mosquito, is considered a superior competitor to resident species during the larval phase when conditions are initiated with same-staged heterospecific larvae. However in nature, Ae. albopictus hatches, and resumes activity, later in the spring than other species, suggesting it encounters larger later developed individuals, and denser populations, of species such as Aedes triseriatus. Additionally, despite their competitive inferiority, these species often coexist with Ae. albopictus in larval habitats, with Ae. albopictus often occurring at relatively low abundances in sylvan habitats. Using lab and near field experiments, we tested the hypothesis that PE with early hatching species reduces survivorship and population growth for the invasive Ae. albopictus. When Ae. albopictus larvae encountered larger, later developed heterospecific larvae at greater densities, under controlled lab conditions and in artificial and natural mesocosms, they experienced significant reductions in survival and estimated finite rate of population increase. Additionally, we found that intraguild predation of Ae. triseriatus on Ae. albopictus may be an important mechanism through which PE works. We conclude that PE is a potential mechanism for coexistence between invasive and resident mosquitoes and should be further explored.

     

Climate,environmental and socio-economic change: weighing up the balance in vector-borne disease transmission

Arguably one of the most important effects of climate change is the potential impact on human health. While this is likely to take many forms, the implications for future transmission of vector-borne diseases (VBDs), given their ongoing contribution to global disease burden, are both extremely important and highly uncertain. In part, this is owing not only to data limitations and methodological challenges when integrating climate-driven VBD models and climate change projections, but also, perhaps most crucially, to the multitude of epidemiological, ecological and socio-economic factors that drive VBD transmission, and this complexity has generated considerable debate over the past 10–15 years. In this review, we seek to elucidate current knowledge around this topic, identify key themes and uncertainties, evaluate ongoing challenges and open research questions and, crucially, offer some solutions for the field. Although many of these challenges are ubiquitous across multiple VBDs, more specific issues also arise in different vector–pathogen systems.     

Electrophysiological and behavioural response of Aedes albopictus to n‐heinecosane,an ovipositional pheromone of Aedes aegypti

Aedes aegypti (L.) and Aedes albopictus (Skuse) (Diptera: Culicidae) are highly anthropophilic mosquito species and potential vectors of dengue and yellow fever. The location of suitable sites for oviposition requires a set of visual, tactile, and olfactory cues that influence females before they lay their eggs. In this study, the effect of n‐heneicosane, a recognized oviposition pheromone of Ae. aegypti, on the olfactory receptors of the antennae of Ae. aegypti and Ae. albopictus was studied using electroantennographic detection coupled to gas chromatography (GC‐EAD). A significant electroantennographic response to n‐heneicosane in adult females of both mosquito species was observed. In addition, gravid Ae. albopictus females laid more eggs in substrate treated with n‐heneicosane at 0.1, 1, or 10 p.p.m. than in the control, denoting oviposition attractancy. Conversely, at 30, 50, 100, and 200 p.p.m., more eggs were laid in the control substrate, indicating oviposition repellency. Analysis of the larval cuticle by GC and mass spectrometry confirmed the presence of n‐heneicosane in the cuticles of Ae. albopictus larvae. The species‐specific role of n‐heneicosane as an oviposition pheromone in Ae. aegypti and its significance as a behaviour modifier of Ae. albopictus in breeding sites is discussed.     

Temporal Patterns of Abundance of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) and Mitochondrial DNA Analysis of Ae. albopictus in the Central African Republic

The invasive Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) was first reported in central Africa in 2000, in Cameroon, with the indigenous mosquito species Ae. aegypti (Diptera: Culicidae). Today, this invasive species is present in almost all countries of the region, including the Central African Republic (CAR), where it was first recorded in 2009. As invasive species of mosquitoes can affect the distribution of native species, resulting in new patterns of vectors and concomitant risk for disease, we undertook a comparative study early and late in the wet season in the capital and the main cities of CAR to document infestation and the ecological preferences of the two species. In addition, we determined the probable geographical origin of invasive populations of Ae. albopictus with two mitochondrial DNA genes, COI and ND5. Analysis revealed that Ae. aegypti was more abundant earlier in the wet season and Ae. albopictus in the late wet season. Used tyres were the most heavily colonized productive larval habitats for both species in both seasons. The invasive species Ae. albopictus predominated over the resident species at all sites in which the two species were sympatric. Mitochondrial DNA analysis revealed broad low genetic diversity, confirming recent introduction of Ae. albopictus in CAR. Phylogeographical analysis based on COI polymorphism indicated that the Ae. albopictus haplotype in the CAR population segregated into two lineages, suggesting multiple sources of Ae. albopictus. These data may have important implications for vector control strategies in central Africa.     

An effective entomopathogenic fungus Metarhizium anisopliae for the simultaneous control of Aedes albopictus and Culex pipiens mosquito adults

The purpose of this study was to select the most effective Metarhizium anisopliae isolates for the simultaneous control of Aedes albopictus and Culex pipiens mosquito adults. The selection was performed using 65 isolates of M. anisopliae, an entomopathogenic fungus isolated from Korean soils. The selection process was carried out through evaluations of conidial thermotolerance, UV-B tolerance, pathogenicity and virulence against adults of two mosquito species and conidial production on grain medium. The thermotolerance of 65 M. anisopliae isolates ranged from 0% to 99%, and their UV-B tolerance ranged from 7.1% to 94.8%. Among them, 30 isolates with high thermotolerance were selected for evaluation of their pathogenicity and virulence against adults of the two mosquito species. Metarhizium anisopliae isolates were more susceptible to Cx. pipiens adults than Ae. albopictus adults because 11 isolates were pathogenic to Ae. albopictus and 21 isolates were pathogenic to Cx. pipiens. Virulence and conidial production were evaluated using 6 isolates with similar pathogenicity against the two species of mosquito. As a result, the accumulated mortality was 74–100% for Ae. albopictus and 78–100% for Cx. pipiens. LT₅₀ values ranged from 2.3 to 5.2 days for Ae. albopictus and from 3.2 − 4.7 days for Cx. pipiens. Comparison of conidial production using three kinds of grain media showed various results according to isolate and medium. Based on the above results, M. anisopliae CN6S1W1 was finally selected as the most effective fungal isolate for the simultaneous control of Ae. albopictus and Cx. pipiens mosquito adults.     

Assessment of geraniol-incorporated polymers to control Aedes albopictus (Diptera: culicidae)

Effective control of mosquito borne diseases has proven extremely difficult with both vector and pathogen remaining entrenched and expanding in many disease endemic areas. When lacking an effective vaccine, vector control methods targeting both larval habitats and adult mosquito populations remain the primary strategy for reducing risk. Aedes albopictus from Thailand was used as a reference baseline for evaluation of natural insecticides incorporated in polymer disks and pellets and tested both in laboratory and field conditions. In laboratory and field tests, the highest larval mortality was obtained with disks or pellets containing IKHC (Insect Killer Highly Concentrate) from Fulltec AG Company. This product is reputed to contain geraniol as an active ingredient. With pellets, high mortality of Ae. albopictus larvae (92%) was observed in presence of 1 g of pellets per 500 ml of water at day 1st, and the mortality was 100% at day 1st for larvae in presence of 5 or 10 g of pellets. Fulltec AG Company has not accepted to give us the exact composition of their IKHC product. Therefore, we cannot recommend it, but the principle of using monoterpenes like geraniol, incorporated into polymer disks or pellets as natural larvicide needs more attention as it could be considered as a powerful alternative in mosquito vector control.     

Piperonyl butoxide synergizes the larvicidal activity of Origanum vulgare essential oil and its major constituents against the larvae of Aedes albopictus and Culex pipiens quinquefasciatus

Mosquitoes bite human beings and transmit many diseases, such as malaria, dengue fever, and Zika virus. Vector control of mosquitoes is an effective strategy for reducing the spread of disease. However, extensive use of insecticides (e.g. pyrethroids and organophosphorus) has caused resistance in mosquitoes, which weakens the effectiveness of mosquito control. Phytochemicals have been considered an alternative approach to mosquito control. Essential oil (EO) was obtained from the leaves and flowers of Origanum vulgare, and its synergistic activity with piperonyl butoxide (PBO) was tested against Aedes albopictus and Culex pipiens quinquefasciatus larvae. Thirty-seven compounds were identified, among which carvacrol and thymol were two major constituents (30.73 % and 18.81 %, respectively). O. vulgare EO had a significant toxic effect against fourth-stage larvae of Cx. p. quinquefasciatus and Ae. albopictus, with LC₅₀ values of 17.51 and 75.90 mg/L. Carvacrol and thymol also each appeared to be more effective against Cx. p. quinquefasciatus (LC₅₀ = 19.30 and 11.56 mg/L, respectively) than Ae. albopictus (LC₅₀ = 26.62 and 26.66 mg/L, respectively). PBO interacted synergistically with O. vulgare EO, carvacrol and thymol with 2.60–6.26 times as much of the active compound needed without PBO as against Cx. p. quinquefasciatus and Ae. albopictus larvae. Overall, our results contribute to the development of new natural mosquito insecticides.