Impact of Human Activities on Disease-Spreading Mosquitoes in Urban Areas

Abstract

Abstract

Urbanization is one of the leading global trends of the twenty-first century that has a significant impact on health. Among health challenges caused by urbanization, the relationship of urbanization between emergence and the spread of mosquito-borne infectious diseases (MBIDs) is a great public health concern. Urbanization processes encompass social, economic, and environmental changes that directly impact the biology of mosquito species. In particular, urbanized areas experience higher temperatures and pollution levels than outlying areas but also favor the development of infrastructures and objects that are favorable to mosquito development. All these modifications may influence mosquito life history traits and their ability to transmit diseases. This review aimed to summarize the impact of urbanization on mosquito spreading in urban areas and the risk associated with the emergence of MBIDs. Moreover, mosquitoes are considered as holobionts, as evidenced by numerous studies highlighting the role of mosquito–microbiota interactions in mosquito biology. Taking into account this new paradigm, this review also represents an initial synthesis on how human-driven transformations impact microbial communities in larval habitats and further interfere with mosquito behavior and life cycle in urban areas.

Graphical Abstract

Introduction

According to the World Health Organization, by 2050, more than 70% of the world’s population will live in cities [1, 2]. Cities generate wealth but also concentrate poverty and inequality, as evidenced with the overcrowded slums in the developing world [3]. Meanwhile, anthropogenic activities are increasingly impacting life quality in cities. Through urbanization processes, urban areas encompass various modifications such as changes in population density, reinforcement of environmental stressors, and habitat modification and fragmentation [4–8]. Urban areas are also important contributors to global warming by generating carbon emissions, accounting for up to 76 % of global carbon dioxide (CO2) emissions. Undoubtedly, rapid urbanization around the world will result in more public health issues within urban areas. This has led to the new concept of “urban health” defined as the study of urban environment characteristics that can affect health and diseases [9].

Out of the 3500 mosquito species worldwide, only a few are able to transmit pathogens that can cause diseases for both humans and animals. However, this results in nearly 700 million people that contract infections each year. Among them, Malaria remains the most serious mosquito-borne infectious disease (MBID) with an at-risk population of around 3.4 billion and 409,000 deaths recorded worldwide in 2019 [10]. Arboviruses such as dengue virus (DENV), Zika virus (ZIKV), and chikungunya virus (CHIKV) are transmitted to humans through the highly competent mosquitoes Aedes aegypti and Aedes albopictus [11]. Several species of Culex mosquitoes are also involved in the transmission of pathogens such as West Nile virus (WNV), Japanese encephalitis virus (JEV), and St. Louis encephalitis virus (SLEV) as well as filarial nematodes that cause diseases in birds, humans, and other animals [12]. Notably, transmission of mosquito-borne infectious diseases has increased in urban areas in recent decades [13, 14]. Even though they are native from natural areas with little human-driven landscape transformation, many mosquito vector species had the ability to be introduced into urban areas [15]. Ecological disturbances produced by anthropogenic landscape transformation on vector mosquito species, growing urban population, migration of native populations at risk, poor waste management, or improper water management have greatly favored the spread of mosquito species vectors in urban areas causing health and economic issues [16–19]. In addition, urbanization processes create ideal habitats for many mosquito species that ultimately increase the risk associated with the occurrence of MBIDs [20]. This is particularly the case for the highly invasive and anthropophilic Asian tiger mosquito, Ae. albopictus, which prefers very dense urban areas [21, 22]. Interestingly, a recent study showed that the more urbanized a given area the fewer mosquito species were found, and those were primary vectors of arboviruses, Ae. aegypti and Cx. quinquefasciatus [23]. It seems that the genus Anopheles would be correlated with low levels of urbanization, while the genera Culex, Culiseta, and Aedes would be correlated with moderate or high urbanization levels [23–27]. More specifically, specific factors such as high population density, urban pollution, habitat modification, and temperature increase strongly influence interactions between mosquito vectors and human population but also select mosquito species that are more adapted and favor the diversification and/or the development of artificial mosquito habitats [28–33].

In this context, the aim of this review is to summarize the impact of urbanization on mosquito spreading in urban areas and thus the risk of development and emergence of MBIDs. In particular, this study emphasizes the following issues: (i) the influence of certain types of infrastructures and objects in urban areas on mosquito life cycle; (ii) the impact of temperature increase on mosquito life history traits, behavior and vector competence; and (iii) the impact of urban pollution on mosquito bio-ecology. Because of the importance of the microbiota in mosquito biology, this review also aims to assess consequences of urbanization on mosquito-associated microbiota and its contribution to mosquito spreading in urban areas.

Methods

Searches were conducted on Google Scholar from February to March 2023. Briefly, we searched for empirical research form reviewed or peer-reviewed articles with no time restrictions that investigated mosquitoes in relation to any urbanization process. After a previous screen, we decided to focus on specific search terms in line to urban mosquito, temperature, fertilizer, pesticide, bisphenol, microplastic, heavy metal, glyphosate, and light pollution. We limited our search to terms appearing in the title of articles only. We also consulted forward/backward citation tracking of the included articles to select other appropriate articles including those related to mosquito microbiota and urban contaminants. Duplicate studies were removed, and the remaining studies were then screened for inclusion. Articles were included if the research topic involved laboratory experiments or field experiments performed in urban areas only. We excluded studies dealing with predictive models, urban biodiversity, mosquito-borne diseases, and mosquito control only that are not in the scope of our review and our primary objectives. We also excluded studies such as commentaries and studies written in languages other than English.

Results

The PRISMA flowchart depicts the results of our review process (Fig. 1). Our search yielded a total of 670 studies. After title/abstract review and remove of duplicates, we found 76 studies that matched our inclusion criteria.

Fig. 1.

PRISMA chart for the identification and selection of articles

Impact of Infrastructures and Objects on the Abundance and Diversity of Urban Mosquitoes

A great variety of infrastructures and objects exist in the urban space and often hosts artificial sites that are favorable to mosquito development and breeding. Some of them such as buildings and construction sites create artificial recipients suitable for mosquito habitats [34]. Artificial breeding sites are often related to small-volume containers of standing water, which are more colonized than larger ones [35]. This has led anthropophilic mosquito species such as Ae. aegypti and Ae. albopictus to become better adapted to artificial habitats than natural habitats [36]. A great diversity of Aedes manmade container habitats, in which garden water and/or rainwater is naturally accumulated, was identified as the most productive mosquito aquatic habitats in many residential areas of metropolitan areas worldwide (i.e., buckets, ornamental bromeliads and flower pots, drains, discarded receptacles, ornamental containers, gully traps, canvas/plastic sheet, and gutters) [34, 37, 38]. They are widely present in urban areas and difficult to manage in order to limit mosquito proliferation. Previous studies also showed that Ae. aegypti and Cx. quinquefasciatus develop in high numbers in construction sites frequently equipped with elevator shafts, jersey plastic barriers, flooded floors, and stair shafts and are almost exclusively the only species present [39, 40]. Moreover, Ae. albopictus, Ae. aegypti, and Cx. quinquefasciatus were shown to successfully colonize water habitats in the cemeteries [36].

Meanwhile, the integration of urban green infrastructure is increasing in cities. Urban vegetation provides undeniable benefits to urban climate, health, thermal comfort, and environmental quality of cities [41]. However, management of standing water is difficult in urban green infrastructure and these areas or installations represent potential habitats and breeding sites for mosquitoes [42]. One of the most striking examples of the impact of urban greening on mosquitoes is illustrated by the excessive mosquito proliferation on vegetated exterior facades of buildings described as a “vertical forest” in Chengdu, capital of the Sichuan province in western China. This uncontrolled phenomenon led the inhabitants to leave their apartments (unpublished data).

While many studies evidenced the diversity of artificial breeding sites in urban areas, studies focused on urban infrastructures and objects in the development of mosquito habitats are still scarce, and more studies would be necessary to integrate the emergence of MBIDs as a risk factor in subsequent urban planning.

Impact of Temperature Increase on Mosquito Life Cycle

It is a well-established fact that urban areas are associated with increased surface temperatures, also called urban heat islands (UHI) [43, 44], and the ongoing climate change seems to reinforce this phenomena [45]. Cities are often 2 to 3 °C hotter than their rural surroundings [46]. However, mosquitoes are poikilotherms, i.e., the body temperature corresponds closely to the external temperature. Therefore, the temperature strongly influences their physiological functions as well as their ecology and dispersion [47, 48]. This means that increases in temperature are expected to have major impacts on geographical dispersion, life history traits, behavior, and vectorial capacity of urban mosquitoes (Table 1).

Table 1.

Influence of temperature on mosquitoes and mosquito-borne infectious disease risks

Conditions	Mosquito genus	Mosquito species	Temperatures	Results	References
Field	Aedes	Ae. albopictus	15.6, 26°C	Decreased larval and adult mortality at the highest temperature Decreased adult body size at the highest temperature Decreased growth rate at the highest temperature	[69]	Murdock et al., 2017
	Aedes/Culex/Anopheles	Ae. aegypti/Ae. albopictus/Ae. vexans/Cx. quinquefasciatus/Cx. pipiens	15, 20, 25°C	Ae. aegypti and Ae. albopictus optimal air temperatures is around 25°C compared to 20°C for Ae. Vexans, Cx. quinquefasciatus and Cx. Pipiens	[65]	Blagrove et al., 2017
	Culex/Mansonia/Ochlerotatus/Psorophora/Aedes/Uranotaenia	23 species	[4–10.9°C], [11–18.9°C], [19–25.9°C], [26–32.9°C]	Differential effects of temperature increase on flight activity according to mosquito species	[78]	Freire et Schweigmann, 2009
	Culex	Cx. pipiens	Field temperatures	Higher density of larvae at 24.82°C Higher fecundity rate at 24.82°C Optimal temperature for mosquito development is 21.66–22.22 °C	[63]	Nagy et al., 2022
		Cx. pipiens/Cx. restuans	Field temperatures	Wolbachia abundance decreases with higher temperature	[70]	Novakova et al., 2017
Laboratory	Aedes	Ae. aegypti	10, 15, 18, 21, 27, 32, 35°C	The optimal temperature for flight was 21°C Flight performance was greater below 27°C	[76]	Rowley et Graham, 1968
			Prediction based on peer-reviewed literature	Dengue epidemic potential was higher at 29.3°C Biting rates increased linearly with temperature	[81]	Liu-Helmersson et al., 2014
			25, 30, and 35 °C	The fecundity is reduced as temperature increased Egg production, oviposition time, and patterns are reduced as temperature increased	[83]	Costa et al., 2010
			8, 21, 26, and 30°C	Higher transmission competence of CHIKV at the highest temperature	[92]	Winokur et al., 2020
		Ae. albopictus	18, 23, 28, and 32°C (constant) and 28, 23, 18°C (fluctuating)	Higher transmission competence of DENV at the highest temperature	[89]	Liu et al., 2017
			18, 28°C	Higher transmission competence of CHIKV at the highest temperature	[91]	Wimalasiri-Yapa et al., 2019
			20, 28°C	Higher transmission competence of CHIKV at the highest temperature	[94]	Zouache et al., 2014
			20, 28°C	Increased competence to transmit DENV at the highest temperature nor CHIKV	[95]	Mercier et al., 2022
			5, 10, 15, 20, 25, 30, 35, 40°C	The optimal temperature for larval development was 29.7°C The shortest gonotrophic cycle was 30°C	[60]	Delatte et al., 2009
			21, 27, 34 °C	The highest temperature decreased larval development time The highest temperature increased larval and adult mortality	[62]	Ezeakacha et Yee, 2019
		An. dirus/An. sawadwongporni	23, 30°C	Larger body size at 23°C Decreased development time at the highest temperature No temperature effect on sex ratio and egg hatching rate	[75]	Phasomkusolsil et al., 2011
	Anopheles	An. gambiae	Temperature increase by 2°C from 10 to 40°C	Decreased larval development time as temperature increased (optimal temperature 28 to 32°C) Optimal adult development between 28 and 32°C Higher adult emergence between 22 and 26°C No adult emergence below 18°C or above 34°C	[55]	Bayoh et Lindsay, 2003
			23, 27, 31, 35 °C	Decreased larval development time as temperature increased Increased larval and adult mortality as temperature increased Highest number of eggs laid at 27°C and lowest at 31°C No influence on blood meal as temperature increased	[61]	Christiansen-Jucht et al., 2015
		An. pseudopunctipennis	15, 20, 22, 25, 27, 30, 33, 35, 37°C	Increased mosquito mortality as temperature increased Decreased gonotrophic cycle time as temperature increased	[85]	Lardeux et al., 2008
		An. stephensi	18, 26, 32°C	Increased pre-blood meal period at lower temperature	[66]	Paaijmans et al., 2013
			21, 24, 27, 30, 32, 34°C	Increased larval and adult mortality as temperature increased Increased biting rates as temperature increased Decreased gonotrophic cycle time as temperature increased The optimal temperature for malaria transmission was 29°C	[68]	Shapiro et al., 2017
			Prediction based on peer-reviewed literature	Malaria transmission decreased between 25 and 28°C	[93]	Mordecai et al., 2013
		NA	16, 20, 24, 28, 32°C	Decreased larval development time from 29 days to 9 days as temperature increased (16°C to 28°C) Decreased longevity as temperature increased Increased larval and adult mortality as temperature increased Increased blood feeding as temperature increased Reduced the fecundity as temperature increased	[59]	Ciota et al., 2014
	Culex	Cx. pipiens	16, 20, 24, 27, 31, 35°C	Decreased larval development time as temperature increased Increased larval and adult mortality as temperature increased	[67]	Ruybal et al., 2016
			7, 10, 15, 20, 25, 30, 33°C	The highest survival was found at 25°C Wing length decreased as temperature increased	[58]	Loetti et al., 2011
			18, 20, 26, 30°C	Higher transmission competence of CHIKV at 30°C	[90]	Dohm et al., 2002
		Cx. quinquefasciatus	35, 37, 38, 39, 40, 41 °C	Increased insecticide resistance as temperature increased	[100]	Swain et al., 2009
	Culiseta	C. incidens	20, 25, 30°C	The higher biting rates are observed at 20°C The peak blood feeding is observed at 25°C	[82]	Su et Mulla, 2001

Temperature and Life History Traits

Sensitivity of mosquitoes to temperature differs from species to species [49, 50] and has differential consequences in term of performance of larval and adult stages. Temperature of larval breeding sites is mainly influenced by the ambient temperature which itself depends on weather variations [51]. To a lesser extent, other factors such as types of containers (geometry, matter, or colors), biotic composition, turbidity, and type of land covers can also modulate the water temperature of larval habitats [51–54]. Previous studies reported that the average optimal water temperature of larval habitats is around 25–30°C [55–58]. However, many studies conducted in laboratory conditions highlighted differential impacts of the water temperature on the duration of larval development according to mosquito species. Ciota et al. (2014) found that larval development time decreased with rise in water temperature for Culex species, ranging from 29 days at 16°C to 9 days at 28°C [59]. Similar observations were reported for An. gambiae and Ae. albopictus mosquitoes [56, 60, 61] even though some variations occur along development time. For example, raise in water temperature increased the developmental rates of first instar larvae and pupae of An. gambiae but decreased the developmental rates of fourth instar larvae [61]. Interestingly, some authors observed carry-over effects and significant interactions between larval density and temperature in Ae. albopictus [62, 63]. The smallest females took the longest to develop in the highest temperature, and this effect was accentuated with density. As for immature stages, many studies evaluated the correlation between increasing temperature and longevity of adult mosquitoes, with contrasted effects depending on the mosquito species [64]. For instance, Ae. albopictus and Culex sp. live longer at 15°C compared to 30°C [59]. Ae. aegypti optimal air temperature is between 24 and 25°C compared to 20°C for Ae. vexans and Cx. pipiens [65]. Regarding survival rates, higher temperature significantly increases mosquito larval and adult mortality [59, 61, 66–68]. For instance, Murdock et al. (2017) conducted a field experiment and demonstrated a significant decrease in survival of Ae. albopictus larvae in urban areas characterized by warmer microclimate compared to suburban and rural [69]. Similarly, the development rate and survival of An. stephensi larvae were significantly reduced at higher temperature [49, 66].

To our knowledge, only two studies have investigated the impact of temperature increase on microbial communities associated with larval habitats and mosquitoes. It was shown that higher temperatures led to a reduction of Wolbachia abundance in Cx. pipiens/restuans mosquitoes, which in turn, resulted in higher susceptibility to WNV in the subsequent mosquito generations [70]. In addition, increase in temperature of 2 °C for Ae. aegypti in the field was shown to favor specific bacterial taxa in the gut microbiota that could alter mosquito fitness, adaptation, and vector–pathogen interactions [71, 72]. Another study showed that microbial richness increased with warmer temperatures (30-32°C) [73].

Altogether, these results tend to show that temperature increase reduces the time duration of larval development as well as larval and adult survival rates. Even though warmer temperature would accelerate the larval cycle, it would also increase mortality of larvae and adults leading to counterbalancing effects on mosquito proliferation. Mortality increase could be explained by an acceleration of diverse metabolic processes or lead to the overproduction of reactive oxygen species that in turn could impact key metabolic pathways.

Temperature and Mosquito Behavior

Temperature also influences different traits of mosquito behavior including flight activity and biting rates as well as reproduction. Wing length is used as a proxy for the mosquito’s body size and is positively correlated with flight activity and dispersion [74]. Many studies showed that increasing temperatures reduce body size [49, 57, 58, 74]. For instance, An. dirus and An. sawadwongporni exhibited higher body size when rearing at 23°C compared to 30°C [75]. In Ae. aegypti, both males and females exhibit increased flight activity at 30°C compared to 20°C [76, 77]. Freire et al. (2009) characterized the flight activity of different mosquito species in relation to the average daily temperature in Buenos Aires (Argentina) and identified two groups [78]. The first one consisted of four species (Cx. eduardoi, Cx. chidesteri, Cx. pipiens, Oc. albifasciatus) that were active throughout the year in all thermal range (4–30.8°C), while the second group (Ae. aegypti, Ochlerotatus crinifer, and Cx. renatoi) displayed a seasonal activity pattern with no activity below 11°C. It was previously shown that the seasonal component may affect whole-organism metabolic rate which explains why some mosquito species reduce their metabolic rate to allow them to survive during the dry or cold season [79]. As temperature increases, the rate of metabolism increases and then rapidly declines at higher temperature [49]. Interestingly, higher metabolic rates were also shown to increase mosquito flight duration [80]. In addition, temperature may also have a significant effect on mosquito biting rates. It was shown that the biting rates of laboratory-reared An. stephensi and Ae. aegypti almost doubled and increased by 25% with increasing temperature from 21 to 32°C, respectively [68, 81]. Blood feeding habits also include the duration of the blood meal. For instance, it was shown that Aedes sp. females fed faster between 26 and 35°C than at lower temperature [77]. Su et al. (2001) found that Culiseta incidens exhibited peak blood feeding at 25°C [82]. In Cx. pipiens, the cumulative feeding rates were significantly higher at 28°C and 32°C compared to lower temperatures [59]. On the opposite, many studies highlighted the negative impact of increasing temperatures on mosquito reproductive traits. In Ae. aegypti, Costa et al. (2010) demonstrated a reduction of egg production and oviposition time as well as changing in oviposition patterns with increased temperatures [83]. Similarly, the fecundity, i.e., numbers of eggs, of other mosquito species such as Ae. krombeini, Cx. Pipiens, Cx. quinquefasciatus, An. dirus, An. stephensi, and An. sawadwongporni was reduced with increasing temperatures [59, 61, 63, 64, 75]. However, a positive impact on fecundity was observed in An. arabiensis [84]. Regarding the gonotrophic cycle (i.e., blood feeding, egg maturation, and oviposition, which are repeated several times throughout adult life), many studies demonstrated that it was shorter at higher temperatures [49, 60, 68, 85, 86]. For instance, Shapiro et al. (2017) found that the average length of the gonotrophic cycle of An. stephensis was 5 days at 21°C, compared to approximately 3 days at 34°C [68]. In addition, An. pseudopunctipennis may lay eggs during 2–3 consecutive nights at high temperature (35°C) and > 10 at low temperature (12°C) [85].

Altogether, these results are in favor on a positive impact of temperature increase on mosquito flight activity, biting rates, and blood feeding habits, thus increasing both the probability of encountering more vertebrate hosts and thus pathogen transmission. However, regarding mosquito oviposition behavior, temperature increase would tend to inhibit reproduction.

Temperature and Vectorial Capacity

Temperature is one of the most significant abiotic factors affecting major components of vectorial capacity, i.e., opportunities for acquisition and transmission of pathogens [87]. Vectorial capacity is partly shaped by mosquito life history traits, mosquito density, and biting rate. As previously described, all these factors can be affected by temperature increase and can thus have major impacts on the vectorial capacity. Vector competence is another important component of vectorial capacity and is defined as the ability of a mosquito species to infect, replicate, and transmit a pathogen to a subsequent host. Moreover, mosquito lifespan and vector competence are strongly linked to the extrinsic incubation period (EIP), i.e., the time it takes for a pathogen to develop within a mosquito, and become transmissible. Previous studies showed that temperature affects both the average and the variability of the duration of EIP [88]. For instance, higher temperatures lead to accelerated DENV replication and induce shorter extrinsic incubation in Ae. albopictus [89]. Similar observations were made for other arboviruses such as ZIKV, CHIKV, or WNV [57], suggesting that reduced extrinsic incubation period promotes the risk of MBID emergence [90–92]. Conversely, opposite effects were also observed. For instance, Mordecai et al. (2013) demonstrated that the optimum temperature for malaria transmission is 25°C and declined above 28°C [93]. Zouache et al. (2014) showed that Ae. albopictus from Brazil exhibited higher CHIKV transmission at 28°C compared to 20°C (85% vs 37.5%), whereas no differences were observed for Ae. albopictus from Italia or La Reunion [94]. Similarly, Mercier et al. (2022) found that Ae. albopictus could transmit CHIKV either at 20°C or 28°C, while DENV transmission only occurs at 28°C [95]. These results highlight the importance to consider genotype-by-genotype-by-environment interactions (mosquito population × virus strain × temperature) to better predict the impact of temperature increase on vector competence and more broadly vectorial capacity. Moreover, it is important to consider that the temperature has also a direct impact on vector-borne pathogens and could modify their virulence (reviewed by [91–93]).

Following previous observations, integrated studies are needed to evaluate as a whole the impact of UHI and temperature increase on mosquito physiology and behavior and which consequences these complex interactions may have on the emergence risk of MBIDs in urban areas. In addition, the duration of the mosquito gonotrophic cycle is a proxy of mosquito density and frequency of host–mosquito contacts [99]. It means that a decrease of this duration time would increase daily biting frequency and thus increase vectorial capacity. Some studies also highlight that temperature increase could also modify mosquito response to insecticide exposure. It was shown that exposition to higher temperature promote insecticide resistance in Cx. quinquefasciatus [100]. Conversely, malathion exposure combined with high temperature induced higher thermo-tolerance and survival to adulthood of Cx. pipiens and Ae. albopictus [101]. More globally, studies established that where urban heat islands (UHI) exist, most likely urban pollution islands coexist (UPI) [102, 103].

Impact of Human Activity–Induced Pollution on Urban Mosquito Spreading

Urban pollution includes diverse sources (atmospheric, agricultural, wastewater, and light) that can affect mosquito physiology throughout its life cycle (Fig. 2) [104–108]. Notably, ubiquitous environmental pollutants in urban water bodies include polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), heavy metals (Fe, Pb, Cd, Hg…), agricultural chemicals (fertilizers), or human drugs [109–111].

Fig. 2.

Influence of urban pollutants on mosquito spreading. Urban pollution includes diverse sources (pharmaceutical, agricultural, industrial, and light) that can affect mosquito physiology throughout its life cycle. Agricultural pollution includes fertilizers such as nitrogen-, phosphorous-, and potassium-based (NPK) fertilizers and pesticides. Pharmaceuticals include anti-inflammatory drugs such as ibuprofen and aspirin as well as antibiotics. Industrial activities can induce heavy metal (in particular Cu, Fe, Pb, Cd, Hg, Cr, Tl, Ni), microplastics, and polycyclic aromatic hydrocarbons’ (PAHs) pollution. Light pollution induces an extensive expansion of artificial light at night (ALAN). The plus sign represents a positive effect, and the minus sign indicates a negative effect. Created by Biorender.com

Urban Gardening– and Urban Agricultural–Induced Pollution

Urban gardening is a well-established phenomenon, whereas urban agriculture (or urban farming) has been developing in many countries in the past 10 years. According to the Food and Agriculture Organization (FAO), urban agriculture is defined as the growing of crops and raising of animals in and around cities. It generally includes the spaces cultivated by farmers who distribute the fruits of the land they work in the environs of the zone of production, as well as urban farming in private homes and in public spaces such as community gardens [105, 112]. Those spaces create a multitude of artificial containers that frequently serve as larval development sites for mosquito reproduction and also become a pollution source through fertilizer and pesticide applications [113, 114]. Previous studies showed that these compounds could influence mosquito fitness, survival, fecundity, and oviposition site selection. Laboratory studies showed that water containing fertilizers attracted significantly more gravid females than water alone [115–118]. Both mosquito species An. Arabiensis and Cx. Quinquefasciatus had preference to oviposit in nitrogenous fertilizer treatments (diammonium phosphate or ammonium sulfate) relative to pesticide treatments (cypermethrin or glyphosate) or control [118]. Interestingly, Ae. albopictus females feeding on a sugar-supplemented substrate contaminated by nitrogen, phosphorous, and potassium-based (NPK) fertilizer laid significantly more eggs compared to sweetened solutions only. Some studies also demonstrated that Cx. quinquefasciatus larvae reared in water supplemented with NPK fertilizers developed faster compared to larvae reared in water only, i.e., 8 (± 2) days to reach the pupae vs 10 (± 3) days [54]. On the opposite, Kibuthu et al. (2016) demonstrated that larval development time of An. arabiensis and Cx. Quinquefasciatus mosquito species was longer with agrochemical treatments (diammonium phosphate and ammonium sulfate) than control [118]. Although the nitrogen, phosphorus, and potassium supplied by the fertilizer are not directly assimilated by mosquito larvae, it seemed that water enriched with fertilizers would be more attractive for gravid females and favor microbial growth. Interestingly, previous studies highlighted a critical role of environmental microorganisms in the attractiveness of breeding sites for gravid females through the production of volatile organic compounds (VOCs) [119–123]. Fertilizers could thus have a direct impact on larval habitat composition that in turn could have broad implications on water colonization by gravid females [124, 125]. Muturi et al. (2016) showed that fertilizer treatments (ammonium sulfate and potassium chloride) altered bacterial diversity and community structure in Ae. albopictus breeding sites [126]. In outdoor experimental mesocosms, Duguma et al. (2017) showed that Cx. nigripalpus larval environments supplemented with low- and high-organic-nutrient regimens were preferentially associated with Clostridiales and Burkholderiales, respectively [127]. All together, these studies seem to show that gravid females deposited offspring in locations that maximize larval survival and growth rate, suggesting that the presence of fertilizers in water would contribute to guide female choice. However, how changes in microbial composition following fertilizer exposure impact oviposition site selection are still an open question and remain to investigate.

Pesticides are also widely used in urban agriculture to control pests and disease infestations. Glyphosate is the most widely used herbicide for urban weed control, and previous studies have already evaluated its impact on mosquitoes [128]. After application, glyphosate and its major metabolite aminomethylphosphonic acid (AMPA) can persist in the soil for weeks, or derivatives can easily be transported by wind or rain into aquatic environments [129]. Glyphosate exposure was shown to influence many important biological traits in mosquitoes such as reproduction, survival rates, development time, and wing size [118, 130–134]. For instance, Kibuthu et al. (2016) demonstrated that Cx. quinquefasciatus and An. arabiensis females laid significantly less eggs after glyphosate exposure compared to control [118]. Glyphosate exposure also induced an approximately 2-day increase in larval development time of Cx. quinquefasciatus. In addition, glyphosate application in breeding sites instantly decreases the larval density [133]. More recently, it was even shown that glyphosate alters mosquito survival and a mechanism involving melanin inhibition that in turn render mosquitoes more susceptible to parasite infection [135]. Furthermore, one study showed that glyphosate exposure induces higher resistance to insecticides by increasing the expression of detoxification genes such as glutathione S transferase activity [134]. Similarly, exposure to the herbicide atrazine induced increased Ae. aegypti larvae tolerance to the organophosphate insecticides temephos and permethrin [136, 137].

To date, we have identified only one study that has investigated the impact of herbicides on mosquito microbiota. Glyphosate was shown to alter the composition of the A. gambiae midgut microbiota with a decrease in the relative abundance of Enterobacteriaceae and an increase in relative Asaia sp. populations [135].

Urban Pharmaceutical–Induced Pollution

Among pharmaceuticals, many compounds are commonly used, and their annual consumption has increased over the past decades [138]. The most used pharmaceuticals are analgesics and antibiotics. In the urban water cycle, hospital wastewater has been identified as a problematic point source due to high concentrations of pharmaceutical contaminants. Most of them cannot be removed and filtered through treatment processes leading to the presence of low concentrations in tap water [139]. Several urban breeding sites are composed of tap water only, or a mix with rainwater, which expose urban mosquitoes to low concentrations of pharmaceutical contaminants [140–143]. Previous studies, under laboratory conditions, showed that human drugs such as ibuprofen and aspirin could influence mosquito biology. Ibuprofen, a commonly used anti-inflammatory, was shown to accelerate Ae. aegypti larval development at environmental concentration [142]. When Ae. aegypti was exposed, this species had better larval survival and population growth rates compared to non-exposed generations [142]. Moreover, multigenerational exposure to this drug induced an emergence of tolerance to the bio-insecticide, Bacillus thuringiensis israelensis (Bti). Molecular mechanisms of mosquito ibuprofen tolerance are still unknown but could be explained either by a multi-generation drug acclimation at low concentrations or the selection of a physiological status allowing tolerance in mosquito population [142]. Aspirin, a nonsteroidal anti-inflammatory drug, is one of the most abundant pharmaceutical found in urban wastewater samples [140]. Aspirin exposure showed an inhibition of mosquito prostaglandin synthesis and an alteration of mosquito reproduction in Ae. albopictus [143].

Regarding microbiota, Pennington et al. (2016) evaluated the impact of common pharmaceutical and personal care products (PPCPs) found in wastewater on larval microbiota of Cx. quinquefasciatus. They showed that mixture treatments composed of antibiotic and hormone treatments with acetaminophen and caffeine had a greater impact on bacterial species richness and evenness compared to antibiotic treatments alone. The authors suggest a possible impact of other contaminants on facilitating growth of different bacteria. In addition, one study showed that antibiotics in ingested human blood enhance the susceptibility of An. gambiae mosquitoes to malaria infection by disturbing their gut microbiota [144].

Due to their increasing presence in urban aquatic habitats, further studies are needed to investigate the impact of pharmaceutical contaminants on mosquito physiology and especially in interaction with other abiotic factors such as temperature. Notably, studies dealing with contraceptive, painkillers, and antidepressants would be of interest given their high prevalence in urban wastewater and effluents [140].

Urban Industrial–Induced Pollution

Microplastics (MPs), heavy metals pollution, and polycyclic aromatic hydrocarbons (PAHs) are prevalent in urban environments. Even though MP contamination is increasing worldwide, knowledge on the sources, fate, and transfer in urban areas remain poorly known [145–147]. Bisphenol A (BPA) is one of the most common chemicals produced by the plastics industry. It is used in combination with other chemicals in manufacturing of various plastics and resins [148]. Some studies examined the impact of BPA on aquatic invertebrates and found estrogenic activity and other potential disruptions of estrogenic activity for some invertebrates [149]. To our knowledge, only four studies analyzed the effect of BPA or its derivatives on mosquitoes [142, 150–152]. For example, at environmental concentration, these compounds were showed to accelerate the development of Culex sp. nor Aedes sp. [142, 151, 152]. Gayathri et al. (2021) revealed that eggs deposited in water containing 1–4 ppm BPA hatch in 4 h less time compare to water without BPA. BPA seems also to accelerate mosquito embryonic development [151]. Increased plastic waste-derived BPA concentration (from 1 to 4 mg/L) in breeding sites of Cx. quinquefasciatus was shown to decrease the time to emerge as adults from 10 days to 8.5 days [152]. A recent study revealed that plastic waste-derived BPA is a developmental agonist of Cx. quinquefasciatus [152]. Conversely, Prud’homme et al. (2017) showed that short- or long-term BPA exposure had no influence on the duration of Ae. aegypti larval development [142]. Dose–response effect was observed on mosquito survival with a negative impact at high concentrations. However, Rachel et al. (2011) found no effect of different BPA concentrations on sex ratios, time to adulthood, and mass of Ae. albopictus and Ae. aegypti. [150].

Regarding their impact on microbiota, Edwards et al. (2023) demonstrated that MP contamination altered the bacterial and fungal composition of Ae. aegypti and Ae. albopictus, with an increase of Elizabethkingia density. Interestingly, such an impact was shown to have potential negative impacts on infection rate of ZIKV in Ae. albopictus [153].

Heavy metals are another kind of pollutants widely spread in urban areas. This pollution is mainly due to industrial activities such as foundries and leaching of metals from different sources (automobiles, runoffs, landfills…) [154]. Previous studies showed that heavy metals such as copper (Cu), ferrum (Fe), and lead (Pb) were detected in mosquito larval urban habitats [155, 156]. Arguably, mosquitoes are adapted to a wide range of heavy metals present in breeding sites, and these metals could be attractive to some mosquito species [155–157]. Mireji et al. (2008) demonstrated that copper was positively correlated with the presence of Ae. aegypti, An. gambiae, and Ae. aegypti [156]. Two studies have also shown that An. gambiae could breed in water polluted with heavy metals and seemed to be well adapted to a wide range of heavy metal pollution [155, 157, 158]. Jeanrenaud et al. (2020) showed that a single exposure to metal pollution (cadmium chloride, copper nitrate, or lead nitrate) could impair mosquito life history traits and induce transgenerational effects [157]. For instance, cadmium (Cd) and mercury (Hg) exposure of Ae. aegypti and An. gambiae was shown to affect gene expression (associated with metabolism, transport, and protein synthesis) and consequently mosquito physiology [159, 160]. On the contrary, Akthar et al. (2021) demonstrated that consecutive exposure to Hg caused bioaccumulation in Ae. aegypti larvae associated with higher mortality and toxicity as well as for their aquatic predator, Tramea cophysa [160]. Heavy metals (Hg, Pb, Cr, Cd, Tl, and Ni) were also detected in adult mosquitoes at lower levels than in larvae that can reflect that adults mosquitoes are less exposed to heavy metals at imago stages or less accumulated metals at this stage [160–162]. Interestingly, Maya-Maldonado et al. (2021) evaluated the effects of iron and copper chelation treatment of adult mosquitoes on Plasmodium berghei infectivity and mosquito reproduction [163]. They showed that feeding mosquitoes with iron and copper chelators before and after an infectious blood meal protected the mosquito from parasite infection and affected follicular development in the case of iron chelation.

Interestingly, a few examples also demonstrated that exposure to anthropogenic stressors may impact tolerance or resistance to insecticide [157, 164]. PAHs are also widespread air pollutants and are systematically present in urban environments [165, 166]. These pollutants are able to induce metabolic changes on vertebrates and some invertebrates in aquatic environments [167, 168]. To date, no study has yet evaluated their effect on mosquito life history traits, but some studies revealed a modification of insecticide resistance in presence of PAHs. For instance, Ae. aegypti larval exposure to the PAHs, benzo[a]pyrene or fluoranthene, leads to an increase of tolerance to the carbamate insecticide propoxur [126, 129]. However, nitropolycyclic aromatic hydrocarbons (nitro-PAHs) which are derivatives of PAHs showed opposite effects in the mosquito species Cx. Quinquefasciatus with an increase of larval susceptibility to chemical insecticides, i.e., permethrin, imidacloprid, and temephos [169].

Altogether, these observations tend to show that mosquitoes are becoming more tolerant to a wide range of pollutants and thus well adapted to urban areas. This could lead in some cases to increase mosquito tolerance to insecticides. To date, most studies on the impact of microplastics and heavy metals on mosquitoes focus on specific and single molecules. Further studies are needed in order to better understand the complexity of the composition of pollutants in natural breeding sites. Future investigations would also need to test the effect of pollutant mixtures on the mosquito life history traits and its microbiota. Another crucial issue that needs to be dealt with is whether pollutant resistant or tolerant mosquitoes are more likely to transmit vector-borne pathogens than pollutant susceptible mosquitoes.

Impact of Light Pollution

Urbanization and population growth cause an extensive expansion of artificial light at night (ALAN) (i.e., “light pollution”) in terms of both density and spatiotemporal distribution in urban areas [106]. Urban light pollution affects the ecology, behavior, and physiology of plants and animals and is responsible for decline in insect populations [170]. Rund et al. (2020) demonstrated that artificial light at night modify Ae. aegypti behavior through increased diurnal biting rates [171]. Conversely, night light suppressed nocturnal biting behavior of nocturnal species such as An. gambiae [172]. Fyie et al. (2021) suggested that a high light pollution during the night drives mosquitoes to be actively reproducing and biting later in the season [173]. In addition, recent studies on house sparrow (Passer domesticus), an amplifying host for West Nile virus (WNV) and other arboviruses, showed that urban light increased host infectious-to-vector period of 2 days and the risk for WNV outbreak [174, 175]. Interestingly, a very recent review also analyzed how artificial light modulated MBID risks [176]. The authors showed that ALAN alters mosquito biology and could thus have an impact of disease risks.

These observations, i.e., longer reproductive period, increased biting activity, and increased contacts between host reservoir and mosquitoes, are seem to establish that there is a positive impact of light pollution on pathogen transmission risk. Altogether, these results argue the importance to carefully investigate the impact of urban light on mosquitoes and mosquito-borne diseases.

Conclusions

This review highlights important impacts of urbanization on mosquitoes and their associated risks. Urban mosaic brings ecological and build components that create ideal habitats for many mosquito species. In particular, UHI and UPI can interact with each other, and positively impact mosquito proliferation. In the future, the worlds of urban planning, architecture, and science should work together to provide transdisciplinary responses to urban environmental and health issues. Studies on reciprocal interactions between temperature, anthropogenic stressors, and mosquito microbiota are still scarce and merit further investigations given the key role of mosquitoes as medically important arthropod vectors of diseases [177]. More globally, integrated studies that combine different impacts at different levels of mosquito organization would be necessary to propose risk prediction for predicting MBID emergence.