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Diel patterns of Aedes aegypti (Diptera: Culicidae) after resurgence in St. Augustine, Florida as collected by a mechanical rotator trap

2018; Wiley; Volume: 43; Issue: 1 Linguagem: Inglês

10.1111/jvec.12302

1948-7134

Morgan L. Smith, Daniel Dixon, Christopher S. Bibbs, Dena Autry, Rui‐De Xue,

Viral Infections and Vectors

In 2016, Aedes aegypti mosquitoes exhibited a significant resurgence in St. Augustine, Florida. The population focally established itself in downtown St. Augustine, an urban tourist destination with millions of visitors annually. Aedes aegypti is of particular concern, being the primary vector of Zika, dengue, chikungunya, and yellow fever. The reintroduction of Ae. aegypti to high traffic areas of St. Augustine presents an unwelcome risk to the local population, supporting the need for further research into more effective ways to control this species and mitigate its ability to spread disease to the public. An understanding of the host-seeking diel patterns of mosquitoes could contribute to their control. According to Leming et al. (2014), there are physiological processes and behaviors that are regulated by the biological rhythms of mosquitoes. These processes and behaviors play a large role in the transmission of many mosquito-borne diseases. A study focusing on dengue vectors (Ae. aegypti and Ae. albopictus) stated how influential the activity rhythms are to understanding not only the mosquito species and their behaviors but also the characteristics of their virus transmission (Lima-Camara 2010). Due to this direct connection between biological rhythms, such as diel patterns, and disease transmission, a more sound understanding of these patterns will increase the success of our integrated mosquito control practices. To our knowledge, the diel patterns of Ae. aegypti have principally been evaluated by human landing rate counts. These diel patterns have been documented in Tanzania occurring between 06:00 to 07:00 and again between 17:00 to 19:00 (Trpis et al. 1973). A study conducted in Trinidad found similar morning and afternoon peak time periods, including 07:00 and 17:00. However, this study did show a variation as a third peak of activity was found at 11:00 (Chadee and Martinez 2000). This presented a trimodal pattern of activity as opposed to the bimodal pattern recorded in Tanzania. According to their results, 90% of females in urban areas were recorded during daylight and twilight time periods and 10% were recorded during the nighttime period. In contrast, no nocturnal activity was recorded in rural areas. (Chadee and Martinez 2000). These peak periods can only be used as a reference for beginning to understand Ae. aegypti in Saint Augustine, FL. The local Ae. aegypti have varying characteristics and behaviors that need to be analyzed to determine the most efficient control measures. Using a mechanical trap design provides multiple advantages when compared to human landing rate counts. The most notable advantage is elimination of the risk of pathogen transmission, such as Zika, to human subjects. Another advantage is consistent data collection, as traps are not threatened by the natural variability among human attractiveness and implementation of landing rate protocols. While using a mechanical trap does increase efficiency and safety, it may track mosquito abundance less dramatically, since it does not possess as many attractive qualities as a live host. However, the deployment of a mechanical rotator mosquito trap to analyze the host-seeking diel patterns of Ae. aegypti in St. Augustine would allow a reproducible understanding of the host-seeking behaviors of Ae. aegypti. Additionally, it is an opportunity to judge the concept of using mechanical rotator traps to assess the diel activity patterns of mosquitoes despite human competition in the target habitat. It is predicted that the host-seeking diel patterns of Ae. aegypti in St. Augustine will be similar to the biomodal patterns of activity recorded in Tanzania, but due to varying weather patterns and climate differences, there are likely slight variations as to the exact peak time frame. Surveillance data collected by Anastasia Mosquito Control District of St. John's County (AMCD) revealed a strong presence of Ae. aegypti located in the downtown area of Saint Augustine during the 2016 season. From this data, three separate sites were chosen throughout the downtown Saint Augustine area based on their high activity of Ae. aegypti. These sites included Site 1 (29.883834, −81.314417), Site 2 (29.895839, −81.315446), and Site 3 (29.895532, −81.316158). Each site had characteristics of ideal habitats for Ae. aegypti, including bromeliads, shaded areas, containers, and other vegetation. There were similar street lights at all three sites. The site 1 traps were placed behind a church located in a heavily populated area in which lots were close to one another with moderate traffic flow. The traps were placed near heavy vegetation that included copious amounts of bromeliads and ample coverage by palms that provided shade. Surrounding areas beyond the trap location included a concrete area outside the church building as well as a wooden fence line directly behind the traps. This site did not possess a large number of artificial containers when compared to the other two sites. Site 2 was located in an alley with houses tightly congested in the midst of downtown Saint Augustine. This differed from the slightly less congested area of site 1. Although the alley itself did not have a lot of traffic concerns due to its compact size, the area immediately adjacent to the alley was a heavy traffic area of downtown Saint Augustine. The trap location had an air conditioner unit located directly beside and was completely shaded. The bordering yards also contained a moderate amount of vegetation, including bromeliads, and were densely encompassed by containers. This differed from the surrounding area of site 1, in which the number of artificial containers was limited. As for site 2, site 3 was located in the backyard of a residence in a heavily populated area with a considerable amount of traffic, as it was also located in close proximity to downtown Saint Augustine. This yard had copious amounts of artificial containers with a moderate amount of vegetation surrounding the traps themselves. The traps were placed on the back fence line behind a shed and were shaded by palms. All three locations had a considerable amount of shade. A cistern was also located in the neighboring yard in close proximity to the traps. For this study, two separate eight-bottle rotator traps (PN1512.5, John W. Hock Company, Gainesville, FL) were used. Each trap had eight jars but only six of them were set per trap to rotate every two h. Each trap was set to run for 12 h total, accounting for a total 24 h period for each collection. The traps were programmed to begin collecting at 09:00 for every round. Traps were baited with concurrent emissions of skin lure (BG-Lure™ cartridge, BioGents AG, Regensburg, Germany) and CO2 from dry ice suspended near the traps. These traps were collected after a 24 h period and mosquitoes were identified individually through light microscopy and recorded according to their corresponding two-h time periods. Species diversity and abundance per two h were recorded, along with the total collection numbers. The mean Ae. aegypti counts for each time period for each site were analyzed using analysis of variance (ANOVA) with a Tukey's HSD test (P = 0.05) performed through JMP 13.1.0 (SAS Institute, Inc., Cary, NC). Collection via a mechanical rotator trap indicated the target Ae. aegypti population had bimodal activity at 17:00–19:00 and 19:00–21:00 (F11=4.64, p < 0.05) (Figure 1). Further comparison through a paired T-test confirmed significantly higher collection of Ae. aegypti during the hours of 17:00 to 19:00, 19:00 to 21:00, and also included 15:00 to 17:00. All analysis recognized the 17:00 to 19:00 period to be of the most significance, followed by 19:00 to 21:00. There was a gradual increase in activity leading up to the peaks, as well as a gradual decrease in activity moving away from the peak hours (Figure 1). The results of this study revealed several differences from the previous human-baited landing rate studies. Our data corroborated the peak evening time frame of host-seeking activity occurring between the hours of 17:00 to 19:00. However, the mechanical rotator trap also allowed detection of peak activity in the 19:00 to 21:00 time frame and 15:00 to 17:00 (though less significant), extending the previously recorded time frame. This extension of the higher host-seeking activity is important to the Saint Augustine community as it reveals a longer time period in which the community is at a higher risk. Although not found to be statistically significant, the 07:00 to 09:00 period showed a slight increase in activity. This finding was similar to that of Gouck and Smith (1962) regarding the effect of the age and time of day on human host avidity in Ae. aegypti, with a high biting rate in the afternoon and the diel activity patterns of Ae. albopictus Skuse (Xue and Barnard 1996, 1997). This information should be disseminated to the public to be made aware of their risk due to human host variability in exposure time and high human outdoor activity patterns in specific areas (Ajelli et al. 2017). Many variables affect the host-seeking behaviors and flight patterns of certain species of mosquitoes. The surveillance area was a high human traffic area, replete with mixed harborage types and abundant artificial lighting. Lighting has been shown to have an effect on landing periodicity of mosquitoes. Studies have demonstrated that most host-seeking behavior of Ae. aegypti has been documented during daylight hours (Chadee and Martinez 2000), however some species of forest mosquitoes, such as Anopheles bellator in Trinidad, have been known to alter their host-seeking behavior from 16:00 to 18:00 and 18:00 to 20:00 during periods with more moonlight (Chadee and Martinez 2000, Chadee 1992). According to Chadee and Martinez (2000), the extension of host-seeking Ae. aegypti during nocturnal hours in urban areas could be due to the increase in use of electrical lighting in these more populated areas. They hypothesize that Ae. aegypti may be reacting to the lighting in the same way the activity of Anopheles bellator was extended to hours of more moonlight. This may account for the fluctuation we saw periodically between the 17:00 to19:00 and 19:00 to 21:00 peaks (Figure 2), with the average sunset time period being 19:00. Some evidence suggests that this species may be less motivated to feed by light patterns and more by the availability of hosts (Gubler and Bhattacharya 1972, Benelli 2014). The results of our study support this theory, as the peak activity time frame identified is also a highly active time period for people inhabiting the downtown area. Male mosquitoes can be used as an indicator for female host-seeking activity as well. Male Ae. albopictus swarm around human hosts five to ten min before the arrival of female mosquitoes (Gubler and Bhattacharya 1972). Mating behavior also peaked in this time frame. This suggests that male mating behaviors mirror the activity window of female mosquitoes. Benelli (2014) in Pisa, Italy, found that daylight hours had no significant effects on the recorded courtship duration of male Ae. albopictus mosquitoes. This is compelling because, were there a biological drive of diel patterns to influence host-seeking behavior of females, it is expected that this would be seen in male mating behaviors as well, as these two activities are dependent on one another. It is expected that Ae. aegypti would follow similar activity patterns as Aedes albopictus, as the two species are known to have comparable activity patterns. This study is proof of concept that host-seeking Ae. aegypti can be collected over a 24-h period with a mechanical rotator trap. Continuing to monitor and evaluate changes to these patterns will obtain a more specific time frame for their peak host-seeking activity. With a refined timing of host-seeking activity, there would be a more accurate time frame to treat for Ae. aegypti. The correlation of Ae. aegypti host-seeking activity and human activity in the surrounding areas should also be evaluated further to explore the theory of opportunistic biting behavior. This could include examinations of phototaxis when host-seeking during weather anomalies, varying lunar phases, and artificial light sources. This information would give a better understanding of the urban ecology of Ae. aegypti, including how to exploit container-inhabiting mosquito ecology so as to mitigate risks to humans. We acknowledge the University of North Florida for allowing collaborative research between the public health program and the AMCD. The Center for Disease Control and Prevention Southeastern Regional Center of Excellence in Vector Borne Disease: The Gateway Program provided the funding to complete this study (CDC grant 1U01CK00510–01).