Urbanization primarily results in the physical growth of urban areas, leading to environmental changes. It is a global trend that results from economic development. Malaysia is among the fastest growing developing countries in the East [1], and the unprecedented movement of people into these areas is predicted to accelerate in the future [2]. A lot of problems have arisen as a result of urbanization and Malaysia is no exception. Among the problems that often take center stage in urbanization debates include environmental pollution, space, population density and the destruction of natural ecology [3]. The socioeconomic effects of urbanization have been comprehensively studied by socio-ecologists [4–6]. However, the ecological effects and their impact on vector biology and vector-borne infectious disease transmission remain unclear.

Most of the previous studies were focused mainly on oviposition ecology from larval habitats and abundance of Aedes species in various urbanized settings [3,7,8]. However, the biting activity, fecundity and survivorship of individual female Ae. albopictus are unknown in response to urbanization level particularly in Penang Island. In order to determine how environmental changes due to urbanization affect the life history traits of Ae. albopictus in terms of survival and reproductive fitness, this present study was conducted to determine the biting rhythm, egg production and longevity of adult female Ae. albopictus strains from Jelutong (urban), Batu Maung (suburban), and Balik Pulau (rural) in Penang Island in comparison to a laboratory strain. Since immature mosquitoes are sensitive to environmental changes [3,9,10], we hypothesized that urbanization increases Ae. albopictus eggs production and adult survivorship. The findings would provide valuable information on Ae. albopictus and help in improving current vector control and surveillance strategies for dengue that are adapted for specific settings in Penang Island.

Based on the 24 h biting activity of all the mosquito strains, Ae. albopictus females showed a clear bimodal activity, with morning (06:30 h to 09:30 h) and evening twilight (18:30 h to 20:30 h) peaks, similar as observed elsewhere in Southeast Asia and South Asia through human landing catch technique in the field [15,18,20–22]. However, we observed the biting activity under uncontrolled laboratory conditions, where Ae. albopictus females were offered a restrained mouse as their blood meal at 20:30 h. When we checked for engorgement at the next hour in accordance with the time points, surprisingly, blood-feeding and host-seeking activities were inactive. The same situation happened for almost ten hours of the experiment (21:30 h to 06:30 h). No engorged mosquitoes resting on the cage wall were recorded within that duration. Our finding was supported by Chen et al. [21] which showed biting peaks for Ae. albopictus at 07:00 h to 09:00 h and 17:00 h to 19:00 h. Chen et al. [22] also reported on the biting activity in urban residential areas in Kuala Lumpur was detected throughout the day, but the biting peaked between 06:00 h to 09:00 h and 15:00 h to 20:00 h, and had low biting activity from late night until the next morning (20:00 h to 05:00 h). In general, biting activity of Aedes was active throughout the day and night but no biting activities were recorded after 23:00 at any study site [22].

This behavior might simply explain the biting nature of this species. According to Kawada et al. [23], the nocturnal host-seeking activity positively correlated with the increasing light intensity as Ae. albopictus is sensitive to dim light. In their study, they found out that the host-seeking activity for this species is deactivated in complete darkness even during the daytime, irrespective of their increasing flight activity controlled by their intrinsic circadian rhythms [23]. The host-seeking activity changes with variation in the light intensity during the scotophase (0 to 100 lux) [23]. The rapid drop in activity level following the onset of darkness suggests that light promotes activity or, less likely, that the absence of light reduces the activity. Light may have a direct effect in determining the amount of activity and indirect effect through setting the phase of the endogenous rhythm [24]. The nocturnal feeding might not be due to the evolutionary adaptation to light, but by the intrinsic reaction of mosquito to light [23]. Thus, the potential risks of transmission possibilities of dengue virus exist wherever the vector inhabits (urban, suburban or rural areas).

Previous studies were mainly on oviposition ecology and abundance of species as influenced by urbanization [3,7,23] without knowing how many eggs one female could produce in a lifetime. By increasing eggs production by Aedes mosquitoes, urbanization could potentially worsen the epidemic risk factors for arboviruses. An increase in Ae. albopictus prevalence and abundance by urbanization was reported by [3] and it was stated that this phenomenon is probably due to elevated numbers of Aedes breeding sites such as tires, discarded cans or water storage containers, provided by urbanizing environments [3]. They reported that an urbanized environment accelerates Aedes mosquito development and survivorship. A deeper understanding of the modifications induced by urbanization in the ecology of Ae. albopictus is indispensable to improvise vector control strategies in the future.

In the present study, fecundity or mean number of eggs laid per female of Ae. albopictus in the first gonotrophic cycle was high in the urban area (107.69 ± 3.98) than those in suburban (94.48 ± 5.18), and rural areas (72.52 ± 3.87). This finding is supported by a study done by [25] where they found that Aedes aegypti which exist in forests had lower reproductive potentials than the typical form which lives in urban and suburban areas. Therefore, they speculated that the forest probably provides a more homogenous environmental stress than the urban habitat, where urban populations have adapted to a fluctuating environment which is probably related to variation in the availability of larval habitats, food source, temperature and humidity. Egg production in the field is dependent on environmental factors such as temperature and relative humidity since these factors influence the survival of adult mosquitoes. Warmer temperature in urban areas will lead to increased human biting frequency and subsequently accelerate the digestion of blood meals taken by mosquitoes, and eventually increased fecundity and reproductive fitness [26]. Apart from that, the number of eggs laid by Ae. albopictus females also depends on the physiological age, the body weight after emergence and particularly the size of the blood meal [27]. The development of the immature stages may influence egg production too. An optimum condition during the growth of immatures will result in larger and healthier adults who can consume more blood from the hosts [12]. The amount of blood imbibed and the blood digestion rate by the female determines the number of eggs produced. More eggs will be produced when an adequate amount of blood is consumed and rapidly digested [28].

These results reflected in the abundance of pupal and larval density in urban rather than suburban and rural areas [3,29]. This might be due to the fact that urban areas had less predators, more nutrition from a “dirtier” environment, or even less drift from agricultural insecticides [3]. The pupal productivity is a good indicator of the abundance of adult mosquitoes [30–32].

Higher mosquito fecundity does not necessarily lead to increased disease transmission if adult mosquitoes have a very short life span. This is because longevity must be sufficiently long in order to allow for the development of pathogens in their bodies to be completed. We found that female mosquitoes in urban areas had the longest life span compared to the other two areas. This result may be due to environmental factors such as temperature and humidity, where the average temperature in urban areas is higher than in suburban and rural areas [3]. This finding is similar to a previous study by [33], where they found that the median survival of Anopheles arabiensis in the deforested area was 49 to 55% higher than those in the forested area and the net reproductive rate of female mosquitoes in the deforested area was 1.7 to 2.6 fold higher than that in the forested area in the East of Africa. Therefore, they concluded that deforestation or urbanization enhanced the survivorship of adult mosquitoes [33].

Longer adult female longevity may enhance disease transmission, although the exact correlation between vector capacity and adult life span needs to be further explored. In this study, we fed the female mosquitoes with 10% sucrose solution without blood, which might have exerted stress on the females during the gonotrophic cycle and affected the longevity of the female mosquitoes [12]. Thus, we predict that the females will live much longer if they were given access to blood like in the natural environment. Overall, the findings clearly showed how Aedes mosquitoes are better adapted to urban environment.

The fecundity and longevity of the laboratory strain was the lowest in comparison to the other strains. This might be due to the environmental stress as the experiment was conducted under uncontrolled laboratory condition, where they are not used to. Abiotic factors such as temperature, relative humidity and rainfall affect the biology of the mosquito [34]. As reviewed by [34], temperature affects the development and survivorship of immature and adult stages of Ae. albopictus. It is also likely to influence biting rate because the durations of gonotrophic cycles are reduced at higher temperatures and at least a blood meal is accessed at each cycle [34], possibly affecting fecundity. Also, a study by [35] in Penang, Malaysia observed a strong correlation between rainfall and eggs of Ae. albopictus collected in urban and suburban areas. Hence the low performance of the laboratory strain compared to the field strains may be due to its less adaptability to the uncontrolled environmental conditions although it was carried out in the laboratory.

The blood meal of the mosquitoes in the various environments could differ depending on their host range. The rural environment is likely to have more diverse and broader host range compared to the suburban and urban areas where hematophagy is more likely to be on humans and in some instance’s pets. In neighboring Singapore, [36] reported that blood meals of Ae. albopictus were exclusively human in urban areas and though mostly human in rural areas, blood meals from animals (domestic and non-domestic) were also observed. However, in other geographic areas, anthropophagy is significantly more common in suburban than urban areas [37]. This shows that hematophagic activity can be on diverse and multiple hosts and varies in different urbanized and geographic settings, potentially impacting on fecundity of the mosquito. There is fewer vegetation as one progresses from rural to urban areas. Sugar (sucrose) is an important nutrient resource for mosquitoes and it has been shown to affect longevity of Ae. albopictus under laboratory conditions [38]. More sugar is likely to be consumed by mosquitoes in rural areas where vegetation is abundant compared to urban areas and this could affect hematophagic activity and consequent processes such as fecundity. Although body sizes of the strains were not assessed, it is likely they could affect biting rates, fecundity and longevity [38,39] of Ae. albopictus from the different urbanized areas if the variation in adult body size is significant.

The results of this study indicate that urbanization might have a significant impact on the ecology and biology of Aedes albopictus. In the urbanizing and urbanized area, the changed environment probably serves as a suitable place for the growth and development of Ae. albopictus; the condensed human population produced more types of containers for larval habitats and more blood sources for adult reproduction. Warm climate may facilitate larval development; enhance vector survivorship and reproductive fitness. These might be the reasons for quick adaptation of Ae. albopictus in urban areas and thus susceptibility of this environment to the mosquito. Urbanization in Penang Island has exhibited strong positive effects on the reproductive and survivorship of adult mosquitoes through effects on the microclimatic condition of the mosquitoes, hence encourage dengue outbreak. The implications of these findings are that, if the current trends of urbanization continue in rural areas, Ae. albopictus could adapt to the changing environment and proliferate in rural areas, resulting in vast dengue outbreak in the future. These findings provide crucial information to the dengue vector control program and may be helpful to vector control experts in predicting outbreaks which could worsen if urbanization occurs without limits.