https://orcid.org/0000-0002-5363-9954
Figures
Abstract
Background
Aedes (Stegomyia) albopictus (Skuse) impacts human outdoor activity because of its aggressive biting behavior, and as a major vector of mosquito-borne diseases, it is also of public health importance. Although most mosquito species exhibit crepuscular activity by primarily host seeking at dawn and dusk, Ae. albopictus has been traditionally characterized as a diurnal or day-biting mosquito. With the global expansion and increased involvement of Ae. albopictus in mosquito-borne diseases, it is imperative to elucidate the diel activity of this species, particularly in newly invaded areas.
Methodology and principal findings
Human sweep netting and carbon dioxide-baited rotator traps were used to evaluate the diel activity of Ae. albopictus in two study sites. Both trapping methods were used in New Jersey’s Mercer County, USA (temperate/urban), while only human sweep netting was used in Florida’s Volusia County, USA (subtropical/suburban). Human sweep netting was performed to determine adult mosquito activity at Sunrise, Solar Noon, Sunset, and Lunar Midnight. Because New Jersey is in a temperate area, diel activity was investigated during the early season (3–19 July), peak season (25 July-19 September), and late season (22 September- 22 October). Aedes albopictus showed the highest activity during peak and late seasons at Solar Noon (P < 0.05). At Sunrise and Sunset during the peak season, Ae. albopictus activity was similar. Lunar Midnight activity was significantly lower than Sunrise and Solar Noon (P < 0.05) but was similar to that of Sunset. In the late season, the highest activity was observed during Solar Noon while the least activity was observed during Sunrise and Lunar Midnight (P<0.05). Bottle rotator traps used in conjunction with the human sweep net technique exhibited similar results. Seasonal activity was not differentiated in Florida due to the consistent subtropical climate. The highest adult activity was observed at Sunrise using human sweep netting, but it was not significantly different from Solar Noon and Sunset. The lowest adult activity was observed at Lunar Midnight; however, it was not significantly different from Solar Noon and Sunset. These results provide evidence that the diel activity of Ae. albopictus, contrary to the common perception of its diurnal activity, is much more varied.
Conclusion/Significance
Involvement of Ae. albopictus in the transmission of debilitating mosquito-borne pathogens such as chikungunya, dengue, and Zika virus, coupled with its affinity to thrive in human peridomestic environments, substantiates that our findings have global implications in areas where Ae. albopictus populations established. It also highlights the importance of behavioral studies of vector species which will not only help mosquito control professionals plan the timing of their control efforts but also provides empirical evidence against conventional wisdoms that may unjustly persist within public health stewards.
Author summary
The Asian tiger mosquito, Aedes albopictus, is an invasive mosquito which is now established in at least 40 states in the USA. Lack of efficient surveillance and control methods against Ae. albopictus, in addition to human-aided accidental transportations, have played a great role in its rapid expansion. Although surveillance measures are becoming more systematic and effective, control of this species still poses a great challenge. Aedes albopictus is difficult to control in the larval stage because it primarily develops in artificial containers that are widespread in peridomestic habitats. These habitats are not only ubiquitous in these environments, they are also cryptic, inaccessible, and extremely difficult to control. Therefore, control of Ae. albopictus in these environments often relies on adult control measures which utilize insecticides dispersed through ultra-low volume equipment as a cold aerosol space spray. These adulticide applications are often conducted at night against endemic mosquito species which are primarily active between dawn and dusk. However, since Ae. albopictus has been traditionally classified as a day-biting mosquito, mosquito control specialists have had doubts about the efficacy of a nocturnal application against a diurnally active mosquito. These uncertainties about intervention efforts become even more important during public health outbreaks of mosquito-borne pathogens such as chikungunya, dengue, or Zika viruses when protection of public health is of paramount importance in peridomestic habitats. Our investigations provide evidence that Ae. albopictus exhibits activity throughout the day and night and that nighttime adulticide applications may indeed be effective against this species, and should not be disregarded.
Citation: Unlu I, Faraji A, Indelicato N, McNelly JR (2021) Do tigers hunt during the day? Diel activity of the Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae), in urban and suburban habitats of North America. PLoS Negl Trop Dis 15(8): e0009438. https://doi.org/10.1371/journal.pntd.0009438
Editor: Roberto Barrera, Centers for Disease Control and Prevention, Puerto Rico, UNITED STATES
Received: April 28, 2021; Accepted: July 9, 2021; Published: August 20, 2021
This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Data Availability: All relevant data are within the manuscript and its Supporting Information files.
Funding: Work is supported by USDA National Institute of Food and Agriculture Hatch project accession number 1020755 through the New Jersey Agricultural Experiment Station (IU, AF). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Most terrestrial organisms are exposed to daily changes in light, dark, and temperature cycles. They have adapted to these changes and express specific behaviors which are genetically controlled. Aedes albopictus (Skuse), the Asian tiger mosquito, is a competent vector of many mosquito-borne viruses such as dengue (DENV) and chikungunya (CHIKV) [1,2]. It is also a major pest species that can drive children indoors and detrimentally impact human quality of life [3,4]. Understanding the diel activity of Ae. albopictus, specifically the times when it may be host seeking, is essential because of its vectorial status as well as the need for effective control measures.
The need for successful and sustainable Ae. albopictus control programs became more evident due to the recent outbreak of arboviral diseases globally, particularly with the expansion of Zika virus (ZIKV) [5]. Additionally, outbreaks of DENV in locations such as the Seychelles Islands, China, La Réunion, Hawaii, Mauritius, and Europe have implicated Ae. albopictus as the primary vector [6,7]. Autochthonous transmission of CHIKV implicating Ae. albopictus as the main vector, has also been documented both in France [8] and Italy [9]. In Gabon, central Africa, epidemiological surveillance has determined that Ae. albopictus was the principal vector of ZIKV during an urban outbreak in 2007 [10]. The species has also drawn the attention of vector control and public health professionals, particularly in expanding and newly invaded areas [11–13].
When an invasive species becomes endemic in a new area, it may display different biological behaviors, including host preference, diel activity, and vector competence [10,14–16], which all pose new challenges for vector control specialists. The first detection of Ae. albopictus in the continental United States in 1985 and its subsequent spread displayed that mosquito control districts were not equipped with effective methods to conduct surveillance and control for this peridomestic species. For example, the establishment of Ae. albopictus in New Jersey was first recorded in 1995 from a trap collection in Keyport, Monmouth County [17], however it wasn’t until 2008 that all 21 mosquito control districts in New Jersey finally obtained an effective trap to conduct surveillance for this species [18,19]. Prior to this, the presence of Ae. albopictus was only detected using New Jersey light traps, which are poor devices in gauging the presence or abundance of this species [20]. In the late 2000’s, after numerous field evaluations, the newly created Biogents Sentinel (BGS) (Biogents AG, Regensburg, Germany) traps were recognized as the standard surveillance tool for Ae. albopictus and Aedes aegypti L. [20–22]. Even though the BGS traps are generally operated over a 24-hour period, they do not provide information about the diel host seeking periods of invasive Aedes mosquitoes such as Ae. aegypti and Ae. albopictus. Elucidating the diel activity of these species is crucial to understanding their behavior, which helps vector control and public health professionals better focus their surveillance and control efforts to maintain quality of life and prevent disease outbreaks.
In Hawley’s (1988) review of Ae. albopictus biology, field studies on diel activity patterns conducted in several countries in Asia reported peak blood feeding during daylight but rarely during the night hours [23]. Almeida et al. (2005) reported from the Chinese Territory of Macao, that Ae. albopictus displayed a bimodal biting peak activity during the morning and later afternoon [24]. Similar results were reported on La Reunión Island where bimodal blood feeding activity for Ae. albopictus females was higher in the morning and afternoon peaks [25]. Hassan (1996) found morning and evening twilight peaks for both sexes of Ae. albopictus in Malaysia [26]. On the contrary in Japan, researchers determined active Ae. albopictus behavior through night time nectar feeding between 2100 and 2130 hours [27]. In addition, although researchers observed bimodal activity in Macao, they also detected some activity during all 24 hours of the day for Ae. albopictus [24]. However, the vast majority of previously published investigations all incriminate Ae. albopictus as primarily diurnal [24–26,28]. This has led to the acceptance of certain fallacies that have permeated vector control communities, particularly in the USA. For example, adult mosquito suppression methods generally utilize adulticides which are applied as ultra-low volume (ULV) cold aerosol sprays during the night. But because ULV applications have not been efficacious or long lasting in controlling diurnally active urban mosquitoes, they have been declared ineffective, particularly for reduction of disease transmission, as reviewed in [29]. One reason for failure of control has been attributed to the nocturnal resting behavior of day-biting mosquitoes in natural and artificial places that are sheltered from the insecticide plume. The ineffectiveness of nighttime ULV applications against diurnal mosquitoes has unfortunately become the conventional wisdom within the modern vector control community and many vector control programs simply do not attempt to adulticide against Ae. albopictus because they are under the assumption that this species may not be active at all during the nighttime ULV application periods.
However, during a variety of field investigations aimed at elucidating the biology, ecology, and effective control methods against Ae. albopictus in temperate central New Jersey [30–32], it has been observed that this species may also be active even during the nighttime hours [29,33]. As a result, the goal of this study was to investigate the diel activity of Ae. albopictus in New Jersey and Florida, in order to further elucidate the biology of this important vector mosquito. Our primary objective was to provide empirical data to prove that invasive Aedes mosquitoes, such as Ae. albopictus, are indeed active throughout the 24 hr diel period and to challenge conventional wisdoms that night time applications of adulticides may indeed be effective during those periods because of the continuous activity of the target species around the clock.
Materials and methods
Site selection
All study sites in New Jersey were highly urbanized, residential sites within the City of Trenton and were comparable to the field site descriptions provided by Unlu et al. (2011) and Farajollahi et al. (2012). The study area encompassed a mix of two-story row homes or duplexes and occasionally, abandoned homes subject to occupation by transients. Study sites in Florida were selected in suburban neighborhoods in the City of Edgewater. Edgewater is located along the Indian River, adjacent to the Mosquito Lagoon.
Human sweep net collections
Human sweep net collections were made using a standard 30.5 cm diameter sweep net purchased from Fisher Scientific (Atlanta, GA, USA). In both locations, the same individuals conducted human sweep netting for the duration of the experiment. With two collectors per residential properties, the collectors took turns walking around the perimeter of the parcel, as the geography allowed, and ending at the pre-determined sampling location which was a shaded or partially shaded area free of obstruction. At the sampling location, each collector stood still and moved the sweep net in a figure eight pattern (Fig 1) for five minutes to collect mosquitoes. On each minute mark, the collector rotated 90 degrees, such that in the final minute the individual was in the original (first minute) position. After completing the sampling process, the first collector returned to the vehicle to place the net in a cooler with dry ice and after 15 minutes, the second collector repeated the process with a second net. A single collector performed all sampling in Florida following the same experimental protocol used in New Jersey. All mosquito specimens collected were counted and identified to species. Weekly collections were made between 8 August and 22 October in New Jersey and between 16 July and 9 September 2013 in Florida. For analysis of New Jersey data, the study was divided into two seasonal periods: 1) peak (8–29 August), and 2) late (5 September—3 October).
Sampling time–diel periods
A 24 h day was divided into four discrete sampling periods: Sunrise, Solar Noon, Sunset, and Lunar Midnight. Solar Noon was identified using the National Oceanic & Atmospheric Administration solar calculator (http://www.esrl.noaa.gov/gmd/grad/solcalc/) and Lunar Midnight was defined as 12 h post Solar Noon. Sunrise and Sunset were delineated using Weather Underground’s regional times for sunrise and sunset (https://www.wunderground.com/). Ten and six residential properties were chosen in New Jersey and Florida, respectively, which required that the human sweep netting be initiated 30 mins prior and ending no more than 30 mins post the determined sampling periods.
Carbon dioxide-baited bottle rotator trap collection
In New Jersey the diel activity of Ae. albopictus was also measured using a collection bottle rotator (CBR) equipped with a CDC miniature light trap (model 1512 and 512 respectively, John W. Hock Company, Gainesville, FL, USA). The CBR consists of a programmable timer powered by a 12-volt, ten-amp rechargeable DC battery which allows for the collection of adult mosquitoes at eight different times during a 24 h period. A voltage regulator (BioQuip Products Inc., Ranco Dominguez, CA, USA) was added to allow the use of the 6-volt CDC miniature trap on the 12-volt CBR system. A CBR with eight jars was used to segregate collections into eight time periods, each lasting three hours. The periods were defined as: 0700–1000, 1000–1300, 1300–1600, 1600–1900, 1900–2200, 2200–0100, 0100–0400, and 0400–0700. Traps were re-programmed weekly to compensate for seasonal changes according to Solar Noon. The CBR traps were baited with CO2 and BG Lures (Biogents AG, Regensburg, Germany). Traps were held in place using a cast-concrete base and positioned 0.5 m above ground level. Adult mosquito collections took place between 3 July and 22 October 2013. At the end of 24 h sampling period, traps and trap contents were transported to the laboratory, identified to species, and counted. Female and male Ae. albopictus were recorded separately. For data analysis, the study was divided into three seasonal periods: 1) early (3–19 July), 2), peak (25 July-19 September), and 3) late (22 September- 22 October).
Comparison of biogents sentinel trap catches with human sweep net collection
Biogents Sentinel traps were deployed in conjunction with human sweep net surveillance in order to investigate the correlation between the two. Biogents Sentinel traps were baited with a BG-Lure, and deployed for a 24 h sampling period. Traps were deployed in the same parcels where human sweep netting was performed. The traps were placed no closer than 7.5 m and no more than 10.5 m away from the location of the human sweep netting. At the end of 24 hours, traps and trap contents were transported to the respective laboratories in New Jersey and Florida, identified to species, and counted. Female and male Ae. albopictus were recorded separately.
Data analysis
Analysis of human sweep net collection data.
To determine the peak activity for Ae. albopictus, we compared the number of adults, female and male, collected during four time periods using a generalized linear model [34]. Overdispersion was detected via the Poisson model (value/df = 1.986), and the model was refit using negative binomial distribution (PROC GENMOD, SAS version 9.3; SAS Institute 2011) with site, season, time and interaction term season*time all used as predictors. The model was determined to fit the data adequately (χ2 = 76.62, df = 63, P = 0.116) in New Jersey and the interaction term was significant (χ2 = 65.20, df = 3, P < 0.001). The association between Florida human sweep netting counts and time were investigated using Poisson regression adjusted for overdispersion (PROC GENMOD, SAS version 9.3; SAS Institute 2011), with site and time as predictors. The model fit adequately (χ2 = 20.61, df = 15, P = 0.150) and the main effect of time was significant ((χ2 = 9.94, df = 3, P = 0.020). The P values between comparisons were adjusted using Holm’s test, which adjusts the calculation of probability in line with the number of comparisons made to avoid type I errors (Holm 1979).
Collection bottle rotator trap analysis.
In order to compare the peak activity for Ae. albopictus using both human sweep netting and CBR trapping, two consecutive time periods from the CBR trapping collections were combined as follows: Sunrise collection was comprised of 05:00–11:00 collections; 11:00–17:00 collections formed Solar Noon; Sunset was comprised of 17:00–23:00; and 23:00–05:00 collections formed Lunar Midnight. The analysis was performed using the generalized linear model (PROC GENMOD, SAS version 9.3; SAS Institute 2011). Overdispersion was detected in Poisson and negative binomial models. Therefore, an ANOVA model was fit to the bottle rotator trap data. The association between season and time were investigated using ANOVA (PROC GLM, SAS version 9.3 for Windows). Since normality and equal variances assumptions were violated, the Box-Cox transformation [35] was used to achieve approximate normality and the eighth root transformation was used to normalize the data. The main effects of site, season and time were used as predictors of the transformed adult counts. The P values between comparisons were adjusted by using Tukey’s tests.
Comparison between human sweep net collection and BGS trap collections.
Linear correlations (Pearson’s correlation) were calculated between the numbers of Ae. albopictus collected for human sweep netting and BGS traps for each state. Each human sweep netting session for each trapping location was 10 min while BGS traps deployed for 24 hrs, therefore a linear correlation test was appropriate to investigate the concordance of the two sampling methods.
Results
Human sweep net
A total of 808 Ae. albopictus adults were collected in New Jersey, with 374 (46.3%), specimens collected during Solar Noon followed by 172 (21.3%) at Sunrise, and 156 (19.3%) and 106 (13.1%) during Sunset and Lunar Midnight, respectively. Of the total number captured, 508 were females (62.9%) along with 300 males (37.1%). The association between human sweep netting counts, season, and time were investigated with site, season, time, and season*time as predictors. The main effect of season*time was significantly associated with the collections (χ2 = 65.20, df = 3, P < 0.001). All pairwise contrasts for season*time were examined and the results are listed in Table 1. Human sweep nett collections showed the greatest activity during Solar Noon in New Jersey during the peak and late season. Substantial activity was also detected at Sunrise, Sunset, and Lunar Midnight during the peak season with no significant difference between Sunset and Lunar Midnight. The mean number of Ae. albopictus per collection declined in late season (Fig 2A). The highest level of activity was at Solar Noon, followed by that of Sunset, and both were statistically different (P < 0.05) from Sunrise and Lunar Midnight.
A. Human sweep netting counts from Florida for all Aedes albopictus during four time periods; Sunrise, Solar Noon, Sunset, and Lunar Midnight (red bars), and human sweep netting counts from New Jersey for all Aedes albopictus over two seasons (peak and late) and four time periods: Sunrise, Solar Noon, Sunset, and Lunar Midnight. B. Count bottle rotator trap counts of all Aedes albopictus at two study sites over three seasons (early, peak, and late) and over a 24 hr period in New Jersey. ¥Values not sharing the same superscript are significantly different (Holm’s test, P < 0.05).
In Florida, a total of 202 Ae. albopictus specimens were sampled with 68 (33.7%) captured at Sunrise, followed by 55 (27.2%) at Solar Noon, 48 (23.8%) during Sunset and 31 (15.4%) at Lunar Midnight. Collections were weighted towards females with a ratio of 5:1. The main effect of time was significantly associated with the collections (χ2 = 9.94, df = 3, P = 0.020). All pairwise contrasts for time were examined and the results are listed in Table 2. The only statistically significant activity for Ae. albopictus adults were found during Solar Noon and Lunar Midnight (Fig 2A).
Collection bottle rotator trap
We tried several statistical models for analysis of the Collection Bottle Rotator trap data set. We found the best fit with ANOVA for these trap collections. The main effects of site (F(1,17) = 13.79, p = 0.002), season (F(2,17) = 11.40, p = 0.001), and time (F(3,17) = 9.03, p = 0.001) were significant predictors of the transformed mosquito counts. The least squares means and corresponding confidence intervals along with the results of post-hoc Tukey’s tests for season and time are provided in the Tables 3 and 4. Aedes albopictus adult activity was highest during peak season followed by early and late season (Fig 2B). For time periods, the highest activity was recorded during Solar Noon and it was significantly different than the other times investigated, excluding Sunset (Table 4). The second highest activity was recorded during Sunset and it was significantly different than Sunrise and Lunar Midnight.
Comparison between human sweep net collection and BGS trap collections
A total of 808 Ae. albopictus adults were collected in New Jersey during human sweep netting collections. The BGS traps collected a total of 1,061 adults, close to a 1:1 ratio (585 females and 476 males). In Florida, a total of 202 Ae. albopictus were collected with human sweep netting and BGS traps captured a total of 349 adults with a 6:1 ratio (299 females and 50 males). Correlation analysis of mosquito collections showed that HSN and BGS trap collections were positively correlated in New Jersey (r = 0.477, p < 0.001) and in Florida (r = 0.401, p < 0.001).
Discussion
In New Jersey, diurnal activity was clearly greatest at Solar Noon during the peak and late seasons, but did not differ significantly between the two seasons. Activity was different when comparing Sunrise and Sunset in both peak and late season. Interestingly, activity at Lunar Midnight during peak season was only different from than that of Solar Noon. Sampling activity in Florida was initiated in mid-July, when Ae. albopictus populations are often high. Overall, Ae. albopictus activity levels were lower in the suburban Florida environment than those found in New Jersey’s urban habitat. It is also interesting to note that the female to male ratio in suburban Florida (~5:1) was much higher than that observed in urban New Jersey (~1.5:1). However, this difference can be explained by the greater abundance and ubiquity of large container habitats in urban areas, which promote the repeated and asynchronous emergence of both male and female Ae. albopictus [18,31]. There were no statistically significant differences in diel activity between Sunrise, Solar Noon, or Sunset in Florida, and while Ae. albopictus activity was lowest at Lunar Midnight, the level of activity at this time period was only different from that of activity at Sunrise.
Bimodal activity has been documented in a variety of Aedes species including Ae. aegypti in Trinidad [36], Aedes polynesiensis Marks [37] in Samoa, and Aedes woodi Edwards [38] in East Africa. The bimodal activity of Ae. albopictus reported by Hawley (1988) and others, including Delatte et al. (2010) on the island of La Réunion during an outbreak of CHIKV was not observed in either New Jersey or Florida [23,25]. Delatte et al. (2010), however, recorded continuous activity across 24h in a series of human-baited experiments [25]. This is also the case with the data generated by human sweep net collections in New Jersey and Florida, USA. These findings corroborate the previous observations made in New Jersey [29,33] supporting earlier field operations of nocturnal host seeking activity, and research including that of Yee and Foster (1992), Higa et al. (2000), and Barnard et al. (2011), identifying nocturnal host-seeking by Ae. albopictus under both laboratory and field conditions [39–41]. Barnard et al. (2011) found that 25% of all Ae. albopictus activity monitored by human landing rates took place at night [40]. For those organizations charged with the deployment of ULV space sprays, our research provides supporting evidence for the success of adulticiding directed at Ae. albopictus in Mercer County, New Jersey, USA between 2009–2011 [29], where nighttime applications of a pyrethroid insecticide (DUET, Clarke, Roselle, IL, USA) at mid-label rates, when sprayed and spaced one or two days apart, achieved over 80% reduction in Ae. albopictus populations in the same urban habitats in which our current studies took place.
This study demonstrated that, late season diel activity was reduced from that of the peak season in temperate New Jersey climate. Activity levels remained greatest at Solar Noon while activity at Sunrise and Lunar Midnight were negligible. Seasonal influences upon the diel activity of Ae. albopictus have been identified on La Reunion, with diel activity at night being reduced, and during winter being entirely absent as a result of lower temperatures [25]. Decreasing temperatures in New Jersey are known to influence diel activity of Aedes species, and cause shifting levels of activity between the summer and fall seasons [42]. While a temporal shift in the activity of Ae. albopictus is not apparent in New Jersey, overall activity is curtailed while diel activity remained limited to warmer temperatures between Solar Noon and Sunset. The northern latitude of urban New Jersey is also subject to cooler temperatures in the late season as compared to the southern latitude and sub-tropical environments of Florida. This fact accounts for the less pronounced difference in Ae. albopictus activity in Florida as compared to New Jersey, particularly in the late season when temperatures are on a decline. Generally, mosquito activity (including host seeking) diminishes when temperatures decrease below 15°C, and ceases at temperatures below 10°C.
Differences in the diel periodicity of Aedes mosquitoes from urban and rural locations have also been reported previously [43], and it has been proposed that the increased lumens associated with street and residential lights promotes modifications or adaptations in behavior, including host-seeking. Kawada et al. (2005) performed cross sections of the compound eye of Ae. albopictus to determine ommatidial diameter and interommatidial angle, determinants of vision [44]. The eye parameter value (1.59) identified explains the lower level of light that initiated host-seeking in Ae. albopictus when compared to Ae. aegypti in a laboratory setting, and may explain why Ae. albopictus has a preference for brighter environments. In addition, Sippell and Brown (1953) reported the importance of movement to host location by diurnal species [23,45]. For example, under laboratory conditions, similar sized moving targets attracted twice the number of diurnally active Aedes mosquitoes compared to stationary targets. Trap capture of Ae. albopictus in Japan was attributed to the movement of field personnel walking toward and attending traps [46]. While our research was not designed to determine the potential influence of artificial light (i.e. street lights) in the urban and suburban residences, these might have influenced Ae. albopictus night time activity [43]. Similar to artificial light, use of human sweep netting for surveillance must have provided strong visual cues to host-seeking mosquitoes.
Biogents Sentinel traps have proven to be an effective surveillance tool for monitoring host-seeking populations of Ae. albopictus, and are used routinely to estimate population levels and direct decisions on control activities for this species. It is common practice in Florida to use a landing rate in association with a homeowner’s service request in order to determine if the request is generated by Ae. albopictus activity [47]. Biogents Sentinel traps have previously been determined to approximate human landing rate estimates [21,48]. The positive correlation of BGS traps with human sweep net collection in both the urban and suburban environments evaluated during this study is invaluable, when considering landing rate surveillance and the influence of varied levels of attractiveness, and collection and enumerating skills when performed by different individuals [49]. In addition, the availability of a surveillance tool such as the BGS trap, removes any perceived ethical concerns or problems related to personnel performing landing rates during periods of disease activity [50].
The diel activity demonstrated by Ae. albopictus in both New Jersey and Florida increases the potential of mosquito-human contact and therefore places individuals at risk of health impacts related to arbovirus transmission. The ongoing global expansion of Ae. albopictus and dynamics of viral adaptation and vector evolution continues to place more humans at risk [6,13,51]. The introduction of exotic pathogens such CHIKV, DENV, and ZIKV are no longer merely conjectural, but are now considered as regular ongoing occurrences globally. Additionally, DENV is considered the second most important mosquito-borne pathogen, trailing only malaria, which primarily affects impoverished populations and can be considered as a neglected tropical disease. Given the emergence and re-emergence of DENV in both developed and undeveloped regions, and the lack of resources available for effective and timely intervention efforts, our study elucidates additional biological behaviors and diel activity that may prove instrumental for focused control. Furthermore, understanding temporal activity and potential seasonal influences upon levels of activity are also vitally important to the deployment of successful control strategies [52–54]. For personnel actively engaged in organized mosquito surveillance and control programs, this research provides critical information that supports the potential to impact adult populations of a likely disease vector outside widely accepted parameters. These types of investigations will further elucidate the biology and behavior of important vector species, and ultimately lead to more rapid and efficacious intervention efforts against neglected tropical diseases. Our investigations definitively provide evidence that Ae. albopictus displays some level of activity throughout the entire day, and that adult mosquito control measures conducted at night should not be discounted as part of an effective integrated vector management program.
Acknowledgments
The authors thank Charles S. Apperson for his critical review of an earlier draft of this manuscript. We thank James Pulaski for creation of drawings and Garret W. Dow for field assistance.
References
- 1. Gratz NG (2004) Critical review of the vector status of Aedes albopictus. Med Vet Entomol 18: 215–227. pmid:15347388
- 2. Sardelis MR, Turell MJ, O’Guinn ML, Andre RG, Roberts DR (2002) Vector competence of three North American strains of Aedes albopictus for West Nile virus. J Am Mosq Control Assoc 18: 284–289. pmid:12542184
- 3. Halasa YA, Shepard DS, Fonseca DM, Farajollahi A, Healy S, Gaugler R, et al. (2014) Quantifying the impact of mosquitoes on quality of life and enjoyment of yard and porch activities in New Jersey. PLoS One 9: e89221. pmid:24603670
- 4. Carrieri M, Bellini R, Maccaferri S, Gallo L, Maini S, et al. (2008) Tolerance thresholds for Aedes albopictus and Aedes caspius in Italian urban areas. J Am Mosq Control Assoc 24: 377–386. pmid:18939689
- 5. Azar SR, Roundy CM, Rossi SL, Huang JH, Leal G, Yun R, et al. (2017) Differential vector competency of Aedes albopictus populations from the Americas for Zika virus. Am J Trop Med Hyg 97: 330–339. pmid:28829735
- 6. Lambrechts L, Scott TW, Gubler DJ (2010) Consequences of the expanding global distribution of Aedes albopictus for dengue virus transmission. PLoS Negl Trop Dis 4: e646. pmid:20520794
- 7. Perera-Lecoin M, Luplertlop N, Surasombatpattana P, Liégeois F, Hamel R, Thongrungkiat S, et al. (2016) Dengue and Chikungunya coinfection–The emergence of an underestimated threat. Current Topics in chikungunya: 67.
- 8. Gould E, Gallian P, De Lamballerie X, Charrel R (2010) First cases of autochthonous dengue fever and chikungunya fever in France: from bad dream to reality! Clin Microbiol Infect 16: 1702–1704. pmid:21040155
- 9. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli A, Panning M, et al. (2007) Infection with chikungunya virus in Italy: an outbreak in a temperate region. The Lancet 370: 1840–1846.
- 10. Grard G, Caron M, Mombo IM, Nkoghe D, Mboui OS, Jiolle D, et al. (2014) Zika virus in Gabon (Central Africa)–2007: a new threat from Aedes albopictus? PLoS Negl Trop Dis 8: e2681. pmid:24516683
- 11. Unlu I, Farajollahi A (2012) Vectors without borders: imminent arrival, establishment, and public health implications of the Asian bush (Aedes japonicus) and Asian tiger (Aedes albopictus) mosquitoes in Turkey. Hacetteppe J Biol Chem 40: 23–36.
- 12. Benedict MQ, Levine RS, Hawley WA, Lounibos LP (2007) Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis 7: 76–85. pmid:17417960
- 13. Rochlin I, Ninivaggi DV, Hutchinson ML, Farajollahi A (2013) Climate change and range expansion of the Asian tiger mosquito (Aedes albopictus) in Northeastern USA: implications for public health practitioners. PLoS One 8: e60874. pmid:23565282
- 14.
Weinstein P, Laird M, Browne GN (1997) Exotic and endemic mosquitoes in New Zealand as potential arbovirus vectors: Ministry of Health Wellington.
- 15. Huang Y-JS, Ayers VB, Lyons AC, Unlu I, Alto BW, Cohnstaedt LW, et al. (2016) Culex species mosquitoes and Zika virus. Vector Borne Zoonotic Dis 16: 673–676. pmid:27556838
- 16. Ayers VB, Huang Y-JS, Lyons AC, Park SL, Dunlop JI, Unlu I, et al. (2019) Infection and transmission of Cache Valley virus by Aedes albopictus and Aedes aegypti mosquitoes. Parasit Vectors 12: 384. pmid:31366369
- 17. Crans W, Chomsky M, Guthrie D, Acquaviva A (1996) First record of Aedes albopictus from New Jersey. J Am Mosq Control Assoc 12: 307–309. pmid:8827609
- 18. Unlu I, Farajollahi A (2014) A multiyear surveillance for Aedes albopictus with Biogents Sentinel trap counts for males and species composition of other mosquito species. J Am Mosq Control Assoc 30: 122–125. pmid:25102596
- 19. Unlu I, Farajollahi A, Healy SP, Crepeau T, Bartlett-Healy K, Williges E, et al. (2011) Area-wide management of Aedes albopictus: choice of study sites based on geospatial characteristics, socioeconomic factors and mosquito populations. Pest Manage Sci 67: 965–974.
- 20. Farajollahi A, Kesavaraju B, Price DC, Williams GM, Healy SP, Gaugler R, et al. (2009) Field efficacy of BG-Sentinel and industry-standard traps for Aedes albopictus (Diptera: Culicidae) and West Nile virus surveillance. J Med Entomol 46: 919–925. pmid:19645298
- 21. Krockel U, Rose A, Eiras AE, Geier M (2006) New tools for surveillance of adult yellow fever mosquitoes: comparison of trap catches with human landing rates in an urban environment. J Am Mosq Control Assoc 22: 229–238. pmid:17019768
- 22. Unlu I, Baker M (2018) Comparison of BG-Sentinel prototype, BG-Sentinel-1, and BG-Sentinel-2: Better results with modification of earlier design. J Am Mosq Control Assoc 34: 237–239. pmid:31442174
- 23. Hawley WA (1988) The biology of Aedes albopictus. J Am Mosq Control Assoc Suppl 1: 1–39. pmid:3068349
- 24. Almeida APG, Baptista SS, Sousa CA, Novo MTL, Ramos HC, Panella NA, et al. (2005) Bioecology and vectorial capacity of Aedes albopictus (Diptera: Culicidae) in Macao, China, in relation to dengue virus transmission. J Med Entomol 42: 419–428. pmid:15962796
- 25. Delatte H, Desvars A, Bouétard A, Bord S, Gimonneau G, Gwenaël V, et al. (2010) Blood-feeding behavior of Aedes albopictus, a vector of chikungunya on La Réunion. Vector Borne Zoonotic Dis 10: 249–258. pmid:19589060
- 26. Hassan A (1996) Patterns in Aedes albopictus (Skuse) population density, host-seeking, and oviposition behavior in Penang, Malaysia. J Vector Ecol 21: 17–21.
- 27. Oda T (1964) Observations on the mosquitoes visiting the flowers of spindle trees, Euonymus japonica. Endemic Diseases Bulletin of Nagasaki University 6: 242–246.
- 28. Chen CD,(2014) Biting behavior of Malaysian mosquitoes, Aedes albopictus Skuse, Armigeres kesseli Ramalingam, Culex quinquefasciatus Say, and Culex vishnui Theobald obtained from urban residential areas in Kuala Lumpur. Asian Biomed 8: 315–321.
- 29. Farajollahi A, Healy SP, Unlu I, Gaugler R, Fonseca DM (2012) Effectiveness of ultra-low volume nighttime applications of an adulticide against diurnal Aedes albopictus, a critical vector of dengue and chikungunya viruses. PLoS One 7: e49181. pmid:23145115
- 30. Fonseca DM, Unlu I, Crepeau T, Farajollahi A, Healy SP, Bartlett-Healy K, et al. (2013) Area-wide management of Aedes albopictus. Part 2: Gauging the efficacy of traditional integrated pest control measures against urban container mosquitoes. Pest Manage Sci 69: 1351–1361. pmid:23649950
- 31. Unlu I, Farajollahi A, Rochlin I, Crepeau TN, Strickman D, Gaugler R (2014) Differences in male–female ratios of Aedes albopictus (Diptera: Culicidae) following ultra-low volume adulticide applications. Acta Trop 137: 201–205. pmid:24907462
- 32. Faraji A, Egizi A, Fonseca DM, Unlu I, Crepeau T, Healy SP et al. (2014) Comparative host feeding patterns of the Asian tiger mosquito, Aedes albopictus, in urban and suburban Northeastern USA and implications for disease transmission. PLoS Negl Trop Dis 8: e3037. pmid:25101969
- 33. Unlu I, A. BM, Indelicato N, Derek D, Zishuo Z, et al. (2018) Nighttime applications of two formulations of pyrethroids are effecvtive against Aedes albopictus J Am Mosq Control Assoc 34: 158–162. pmid:31442153
- 34. Schall R (1991) Estimation in generalized linear models with random effects. Biometrika 78: 719–727.
- 35. Osborne J (2010) Improving your data transformations: Applying the Box-Cox transformation. Pract Assess Res Evaluation 15: 12.
- 36. Chadee DD (1988) Landing periodicity of the mosquito Aedes aegypti in Trinidad in relation to the timing of insecticidal space-spraying. Med Vet Entomol 2: 189–192. pmid:2980173
- 37. Samarawickrema W, Sone F, Cummings R (1987) Seasonal abundance, diel biting activity and parity of Aedes polynesiensis marks and A. samoanus (Grünberg)(Diptera: Culicidae) in Samoa. Bull Entomol Res 77: 191–200.
- 38. Trpis M, Gerberg E (1974) Diel periodicity in the biting activity of Aedes woodi in East Africa. Mosq News 34: 443–447.
- 39. Yee WL, Foster WA (1992) Diel sugar-feeding and host-seeking rhythms in mosquitoes (Diptera: Culicidae) under laboratory conditions. J Med Entomol 29: 784–791. pmid:1357175
- 40. Barnard D, Knue G, Dickerson C, Bernier U, Kline D (2011) Relationship between mosquito (Diptera: Culicidae) landing rates on a human subject and numbers captured using CO 2-baited light traps. Bull Entomol Res 101: 277–285. pmid:21205394
- 41. Higa Y, Tsuda Y, Tuno N, Takagi M (2000) Tempo-spatial variation in feeding activity and density of Aedes albopictus (Diptera: Culicidae) at peridomestic habitat in Nagasaki, Japan. Med Entomol Zool 51: 205–209.
- 42. Crans W, Sprenger D (1996) The blood-feeding habits of Aedes sollicitans (Walker) in relation to eastern equine encephalitis virus in coastal areas of New Jersey. III. Habitat preference, vertical distribution, and diel periodicity of host-seeking adults. J Vector Ecol 21: 6–13.
- 43. Chadee DD, Martinez R (2000) Landing periodicity of Aedes aegypti with implications for dengue transmission in Trinidad, West Indies. J Vector Ecol 25: 158–163. pmid:11217215
- 44. Kawada H, Takemura S-Y, Arikawa K, Takagi M (2005) Comparative study on nocturnal behavior of Aedes aegypti and Aedes albopictus. J Med Entomol 42: 312–318. pmid:15962780
- 45. Sippell W, Brown A (1953) Studies of the responses of the female Aedes mosquito. Part V. The role of visual factors. Bull Entomol Res 43: 567–574.
- 46. Kusakabe Y, Ikeshoji T (1990) Comparative attractancy of physical and chemical stimuli to aedine mosquitoes. Med Entomol Zool 41: 219–225.
- 47. Lloyd AM, C.R. C, D.B C (2018) Florida White Paper. Florida Coordinating Council on Mosquito Control Florida Mosquito Control: The state of the mission as defined by mosquito controllers, regulators, and environmental managers.
- 48. Obenauer P, Kaufman P, Kline D, Allan S (2010) Detection of and monitoring for Aedes albopictus (Diptera: Culicidae) in suburban and sylvatic habitats in north central Florida using four sampling techniques. Environ Entomol 39: 1608–1616. pmid:22546459
- 49.
Silver JB (2007) Mosquito ecology: field sampling methods: springer science & business media.
- 50. Association AMC (2017) Best Practices for Integrated Mosquito Management: A Focused Update. https://cdn.ymaws.com/www.mosquito.org/resource/resmgr/docs/Resource_Center/Training_Certification/12.21_amca_guidelines_final_pdf.
- 51. Egizi A, Fefferman NH, Fonseca DM (2015) Evidence that implicit assumptions of ‘no evolution’of disease vectors in changing environments can be violated on a rapid timescale. Philos Trans R Soc Lond B Biol Sci 370: 20140136. pmid:25688024
- 52. Suárez-Mutis MC, Fé NF, Alecrim W, Coura JR (2009) Night and crepuscular mosquitoes and risk of vector-borne diseases in areas of piassaba extraction in the middle Negro River basin, state of Amazonas, Brazil. Mem Inst Oswaldo Cruz 104: 11–17. pmid:19274370
- 53. Godsey MS, Burkhalter K, Delorey M, Savage HM (2010) Seasonality and time of host-seeking activity of Culex tarsalis and floodwater Aedes in Northern Colorado, 2006–20071. J Am Mosq Control Assoc 26: 148–159. pmid:20649124
- 54. Gray KM, Burkett-Cadena ND, Eubanks MD, Unnasch TR (2011) Crepuscular flight activity of Culex erraticus (Diptera: Culicidae). J Med Entomol 48: 167–172. pmid:21485351