TY - JOUR
AU - Cardé, Ring, T
AB - Abstract Aedes aegypti (L.) is an important vector of viruses causing dengue, Zika, chikungunya, and yellow fever and as such is a threat to public health worldwide. Effective trapping methods are essential for surveillance of both the mosquito species and disease presence. The BG-Sentinel (BGS) is a widely used to trap Ae. aegypti but little is known of its efficiency, i.e., what proportion of the mosquitoes encountering the trap are captured. The first version of the BGS trap was predominantly white, and the current version is mostly navy blue. While this trap is often deployed without any olfactory lure, it can also be deployed with CO2 and/or a human skin odor mimic lure to increase capture rates. We tested the efficiency of capturing Ae. aegypti under semi-field conditions for the original white version without lures as well the blue version with and without various lure combinations. None of the configurations tested here captured 100% of the mosquitoes that encountered the trap. A navy-blue trap emitting CO2 and a skin odor mimic produced the highest capture (14% of the total insects in the semi-field cage), but its capture efficiency was just 5% (of mosquitoes encountering the trap). Mosquitoes often had multiple encounters with a trap that did not result in capture; they crossed over the trap entrance without being captured or landed on the sides of the trap. Understanding these behaviors and the factors that induce them has the potential to suggest improvement in trap design and therefore capture efficiency. Aedes aegypti, mosquito, Biogents Sentinel trap, trap efficiency Aedes aegypti (L.) is a vector of several arboviruses, causing dengue, Zika, chikungunya, and yellow fever. The global incidence of dengue has grown in recent years, and there are an estimated 390 million cases annually (Bhatt et al. 2013), making dengue the most prevalent arboviral disease worldwide (Wilder-Smith et al. 2019); the World Health Organization (WHO) estimates that half the world’s population is now at risk (WHO 2018). To monitor the success of arboviral control programs such as with the endosymbiont Wolbachia infection (O’Neill et al. 2018, Pan et al. 2018, Ritchie et al. 2018, Zheng et al. 2019), efficient surveillance of the primary dengue vector, Ae. aegypti and other vectors (e.g., Aedes albopictus Skuse) is required (Ball and Ritchie 2010a). The BG-Sentinel trap (BGS) (Biogents, Biogents AG, Regensburg, Germany) was developed as a safe alternative to human landing/biting collections in the surveillance of Ae. aegypti and other dengue vectors (Kröckel et al. 2006) and was one of the first effective sampling devices for capturing adult Ae. aegypti mosquitoes (Johnson et al. 2012). It is a commercially available, ‘highly effective’ (Kröckel et al. 2006) device for monitoring populations of Ae. aegypti in urbanized areas (Maciel-de-Freitas et al. 2006, Williams et al. 2007, Ritchie et al. 2011, Johnson et al. 2012, Li et al. 2016, Wilke et al. 2019) and to monitor Ae. albopictus in the United States (Farajollahi et al. 2009). To improve monitoring and control of mosquito vector populations, it will be useful to understand mosquito host-finding behaviors and the response to trap designs that exploit these cues. There is widespread use of the BGS trap, both in domestic settings and in research, with carbon dioxide (CO2) and a synthetic human skin-odor lure (BG-Lure). For example, the BGS is widely used as a monitoring tool in ‘rear and release’ programs (Lacroix et al. 2012, Carvalho et al. 2015, Nguyen et al. 2015, O’Neill et al. 2018) and in repellent testing (Peach et al. 2019). BGS traps have been tested under semi-field conditions for the effects of physiological state, age and body size on capture bias (Ball and Ritchie 2010a) and for the effects of a visually competitive environment (Ball and Ritchie 2010b), as well as for optimal location in human-occupied experimental huts (Salazar et al. 2018). The first version of the BGS trap was predominantly white with a soft cloth supported by a wire coil but has undergone several scientifically informed modifications to its current form (BG Sentinel 2, Biogents, Biogents AG, Regensburg, Germany). The BGS 2 has a hard, white top with a black entrance funnel and a navy-blue body (Barrera et al. 2013), a pop-up assembly design, granulated formulation of the lure encased in a plastic cartridge (Arimoto et al. 2015) which has been tested with Aedes spp. (Crepeau et al. 2013, Wilke et al. 2019). Other additions to the BGS have included the addition of live mice to enhance trapping of Ae. albopictus (Le Goff et al. 2016), the use of yeast-produced CO2 to reduce field costs (Jerry et al. 2017), and the addition of a catch pot with a sucrose-soaked sponge or nucleic acid preservative card to improve longevity of captured mosquitoes and augment arbovirus detection, respectively (Timmins et al. 2018). In a large-scale field study, Staunton et al. (2019) found that a trap’s location and the condition of the premises in which it is set influence both male and female Ae. aegypti trap catches of the BGS. For example, a high proportion of vegetative shade elevated trap catches of male and female Wolbachia-infected Ae. aegypti, whereas increasing visual complexity near the trap negatively affected the catch rate of male Ae. aegypti, which substantiates the findings of Ball and Ritchie (2010a). In North Queensland, Australia, Williams et al. (2007) undertook fixed position sampling with one or two traps per house in a 200 m diameter cluster at 72-h intervals; this is recommended for routine monitoring for female Ae. aegypti and provides a reasonable degree of precision for calculating mosquito abundance (Williams et al. 2007). Mosquito behavior has been studied in wind-tunnel assays to qualify responses to long- and short-range cues (Dekker et al. 2005; Cooperband and Cardé 2006a,b; Van Breugel et al. 2015; Majeed et al. 2017). The mosquito behavioral response to currently used trapping systems, including the BGS is not fully understood but is key to improving trap design. Cribellier et al. (2018) analyzed the behavior of the female malaria mosquito Anopheles coluzzii Coetzee & Wilkerson confined in close proximity to an odor-baited trap under climate-controlled laboratory conditions over 15 min. Cooperband and Cardé (2006a,b) analyzed flight behavior of Culex quinquefasciatus Say and Culex tarsalis Coquillett in response to CO2-baited traps (and trap efficiency) in a field wind tunnel. Most recently, Batista et al. (2019) described some host-seeking flight behaviors of Anopheles arabiensis Patton to a modified BGS—the BG-Malaria. However, examination of the behavioral response of Ae. aegypti to the BGS, a ‘gold standard’ (Timmins et al. 2018) trap for this species is, to the authors’ knowledge, yet to be undertaken. The BGS is designed to operate as a visual cue (Williams et al. 2006a), with CO2 often considered to be a long-range olfactory cue and a synthetic human skin odor as a short-range olfactory cue. Because Ae. aegypti is a day-active mosquito, visual cues are important in host finding (Allan and Day 1987, Muir et al. 1992) for both female and males (that find females in proximity to a host, Clements 1999). Van Breugel et al. (2015) also suggest that visual cues play a vital intermediate role in host localization by integrating long- and short-range cues. CO2 is a well-studied long-range olfactory cue for Ae. aegypti (Gibson and Torr 1999); as little as 0.01–0.03% CO2 above background concentration activates resting mosquitoes (Eiras and Jepson 1991). A synthetic human skin odor lure (BG-Lure, Biogents, Biogents AG, Regensburg, Germany) comprises a dispenser cartridge that releases a combination of lactic acid, ammonia, and caproic acid, all substances found on human skin (Bosch et al. 2000) and has been field-tested for Aedes and Culex spp. extensively (Kröckel et al. 2006, Williams et al. 2006b, Irish et al. 2008, Bhalala and Arias 2009). What is unknown is the capture efficiency of the BGS, i.e., what proportion of the mosquitoes encountering the trap are captured? This study aimed to 1) determine the trapping efficiency of BGS in various configurations, e.g., unbaited white and navy blue-bodied, with CO2, with the BG-Lure, with both CO2 and the BG-Lure, for female Ae. aegypti under semi-field conditions and 2) analyze the flight behavior of female Ae. aegypti in response to the BGS in these configurations. Methods Mosquito Colony Mosquitoes used were from a colony of Wolbachia (wMel-strain) infected Ae. aegypti sourced from Cairns (Queensland, Australia) and periodically supplemented with wild material. The Ae. aegypti population in Northern Australia is largely Wolbachia-infected following male releases starting in 2011 (Hoffman et al. 2011). The laboratory colony was maintained at 27°C, 70% RH with 12:12 (L:D) h regime. Adults were provided with a honey/water solution (50:50) and were blood fed three times a week using human volunteers (Human ethics approval from James Cook University H4907) following the protocol in Hoffman et al. (2011). Eggs were collected and allowed to embryonate for 3 d before being stored in air-tight containers for up to 2 mo. Eggs were hatched in water containing 0.2 g bakers’ yeast (Lowan Whole Foods, Glendenning NSW, Australia) per liter. Mosquito larvae were reared on fish food powder (TetraMin Tropical Flakes Fish Food, Tetra, Melle, Germany). Pupae were sexed and transferred to clear plastic containers (300 ml) covered with a white mesh cloth (0.5 mm pore size) with a sponge on top (30 × 40 mm2) soaked with honey/water solution (50:50). Mosquitoes used for bioassays were between 3- and 10-d post-emergence from pupation (dpe). Mosquitoes used for assays were between F1 and F4 generations from field collection. Bioassay The behavioral assays were conducted during daylight hours from February to April 2019 when temperatures in the semi-field cage were between 26 and 34°C. It was observed in pilot trials that when temperatures in the semi-field flight cage reached 35° or higher, flight activity of Ae. aegypti was greatly reduced. The semi-field cage experimental arena measures 17.5 × 68.7 m and is described in detail by Ritchie et al. (2011). Ball and Ritchie (2010a) found that dark-colored harborage sites near the BGS trap (1 m away) had a negative effect on nulliparous female capture rates. Other stimuli in the cage were, therefore, minimized with, e.g., dark-colored objects covered with lighter-colored materials. Ambient light, temperature, and humidity in the cage were monitored using a data logger that was placed within 2 m of the trap. Wind speed in the cage was measured once during each trial period (1 h). Humidity was maintained at ≥60%; if humidity dropped below 60%, the pavement in the cage was hosed down between trials. New BGS traps were assembled with gloves to minimize human odor interference and left to air out for 7 d in the semi-field flight cage. The BGS trap was deployed in the middle of the cage on the cement pathway with garden on either side and paving behind. The trap was assembled as per manufacturers’ instructions with the BG-lure cartridge placed in the assigned hole in the trap lid; a 10-liter CO2 tank fitted with a pressure reducing regulator (Biogents AG, Regensburg, Germany) provided gas at 200ml/min through the tubing and nozzle provided with the trap. Two video cameras (Sony Handycam HDR-CX405) were installed to record the trap from directly above and level from the side. White Corflute (corrugated polypropylene 5 mm thickness; Corex Plastics Australia) was placed underneath the trap (circular; 600 mm diameter) and behind the trap (600 × 800 mm) to create a uniform background. One hundred female Ae. aegypti were released into the flight cage once per week. Additionally, every morning mosquitoes were replaced to account for a daily mortality rate of 0.07 (Ritchie et al. 2011). Insects were released remotely from rearing/pupation containers approximately 3 m from the semi-field cage entrance and 3 meters from the trap. Flight activity around traps was recorded for 1 h (frame rate 60i; resolution 1920 × 1080), after which the trap catch bag was replaced and mosquitoes caught were counted; pupal casings in release container were counted to verify the number of insects released. Between trials the insects captured were replaced in the cage to offset those removed via trap capture. Nitrile gloves were worn while handling traps and cameras; door handles, faucets, light switches, release container (and other frequently touched objects) were regularly wiped with EtOH (80%) throughout the experimental period to minimize possible human odor interference. The trap and cameras were removed from the cage overnight. The experimenter wore protective clothing whilst entering the cage during the female trials to ensure that no blood feeding occurred. The BG lure was stored in an air-tight plastic container at 4°C between trials. Once a week the cage was cleared entirely of mosquitoes using a Prokopack aspirator (Vazquez-Prokopec et al. 2009) to ensure the age of the responding mosquitoes remained between 3 and 10 dpe. The age of the mosquitoes in the semi-field cage was recorded for each replicate for analysis; some days there was a mix of two ages (e.g., 3 and 4 dpe) in the cage. A mosquito encountering the trap was defined as (in the video record from above trap) visible above the white Corflute backboard—a 210 mm anulus around the trap, together with the trap comprising a circular 1.2 m diameter field of view. A mosquito was still deemed to be encountering the trap if it left the visible frame (above the white Corflute) and returned (from a feasible direction) within 1 s. The number of encounters refers to the number of times there was a mosquito in the trap vicinity rather than the absolute number of individuals. This is important because each encounter with the trap is still an opportunity to be captured, which overwhelmingly, was missed. Statistical Analysis For proportion data (percentage captured, proportion caught of total encounters, flew over entrance, landed on trap), data was tested for normality using the Shapiro–Wilk normality test. Following this, linear regressions were built and tested incorporating time of day, the age of responding mosquitoes, the mean temperature and relative humidity of each replicate. For time spent during an encounter, catch, and velocity data, a generalized linear model (GLM) with Gaussian distribution was run incorporating time of day, the age of responding mosquitoes, the average temperature and relative humidity of each replicate followed by post hoc pairwise comparisons. Effects were tested with Spearman Rank correlations. To calculate track tortuosity, Emax (a measure of straightness) and sinuosity (trajr package, McLean and Skowron Volponi 2018) were calculated (Getis et al. 2007) and a Gaussian GLM was run incorporating time of day, the age of responding mosquitoes, the average temperature and relative humidity of each replicate followed by post hoc pairwise comparisons. For trials in which mosquitoes ranged 2 d in age, the value was rounded up to the older age for input into the linear regression and GLM. All statistical analyses were performed in Program R (R Core Team 2017) using RStudio Version 1.1.463 (2009–2018 RStudio, Inc.). Video Tracking Analysis Video tracking was performed using EthoVision XT Version 9.0 (Noldus Information Technology). Raw numeric data were exported and used in statistical analysis. For data obtained with EthoVision XT, only tracks captured with sufficient detail and minimal interpolation were used; individual tracks were pooled per treatment for analysis (Table 1) and where necessary, tracks were manually corrected. Table 1. Treatments for Aedes aegypti trapping trials in semi-field cage and numbers of tracks used for analysis Trap configuration . Trials (n) . Post hoc group . Tracks used for velocity and Emax (n) . White BGS 17 Trapped 11 Untrapped 22 Over entrance 31 Navy blue BGS 17 Trapped 8 Untrapped 30 Over entrance 19 Navy blue BGS with CO2 19 Trapped 12 Untrapped 92 Over entrance 14 Navy blue BGS with BG-lure 17 Trapped 7 Untrapped 35 Over entrance 22 Navy blue BGS with CO2 and BG-lure 17 Trapped 45 Untrapped 310 Over entrance 60 Trap configuration . Trials (n) . Post hoc group . Tracks used for velocity and Emax (n) . White BGS 17 Trapped 11 Untrapped 22 Over entrance 31 Navy blue BGS 17 Trapped 8 Untrapped 30 Over entrance 19 Navy blue BGS with CO2 19 Trapped 12 Untrapped 92 Over entrance 14 Navy blue BGS with BG-lure 17 Trapped 7 Untrapped 35 Over entrance 22 Navy blue BGS with CO2 and BG-lure 17 Trapped 45 Untrapped 310 Over entrance 60 All BG Sentinel (BGS) traps were assembled and deployed according to manufacturer’s instructions. Open in new tab Table 1. Treatments for Aedes aegypti trapping trials in semi-field cage and numbers of tracks used for analysis Trap configuration . Trials (n) . Post hoc group . Tracks used for velocity and Emax (n) . White BGS 17 Trapped 11 Untrapped 22 Over entrance 31 Navy blue BGS 17 Trapped 8 Untrapped 30 Over entrance 19 Navy blue BGS with CO2 19 Trapped 12 Untrapped 92 Over entrance 14 Navy blue BGS with BG-lure 17 Trapped 7 Untrapped 35 Over entrance 22 Navy blue BGS with CO2 and BG-lure 17 Trapped 45 Untrapped 310 Over entrance 60 Trap configuration . Trials (n) . Post hoc group . Tracks used for velocity and Emax (n) . White BGS 17 Trapped 11 Untrapped 22 Over entrance 31 Navy blue BGS 17 Trapped 8 Untrapped 30 Over entrance 19 Navy blue BGS with CO2 19 Trapped 12 Untrapped 92 Over entrance 14 Navy blue BGS with BG-lure 17 Trapped 7 Untrapped 35 Over entrance 22 Navy blue BGS with CO2 and BG-lure 17 Trapped 45 Untrapped 310 Over entrance 60 All BG Sentinel (BGS) traps were assembled and deployed according to manufacturer’s instructions. Open in new tab Results The trap configuration that caught the most Ae. aegypti in 1 h (mean ± SE) under semi-field conditions was the navy-blue BGS with CO2 and BG lure (13.76 ± 3.42) (Table 2). For this trap, during a replicate there were often more encounters with the trap than there were insects in the semi-field cage (Fig. 2); this demonstrates that at least some mosquitoes were encountering the trap more than once. Table 2. The percentage of female Aedes aegypti captured of total in semi-field cage and proportion captured of total encounters per hour for BGS trap configurations (different letters indicate significant difference [P < 0.05]) BGS trap configuration . Mean (±SE) percentage captured of total in semi-field cage . Mean (±SE) proportion captured of total encounters . White 3.06 ± 0.83a 0.2 ± 0.05a Navy blue 1.65 ± 0.55a 0.16 ± 0.04a Navy blue + CO₂ 3.67 ± 0.9a 0.08 ± 0.02b Navy blue + BG-Lure 1.35 ± 0.41a 0.17 ± 0.05a Navy blue + CO₂ + BG-Lure 13.76 ± 3.42b 0.05 ± 0.01ab BGS trap configuration . Mean (±SE) percentage captured of total in semi-field cage . Mean (±SE) proportion captured of total encounters . White 3.06 ± 0.83a 0.2 ± 0.05a Navy blue 1.65 ± 0.55a 0.16 ± 0.04a Navy blue + CO₂ 3.67 ± 0.9a 0.08 ± 0.02b Navy blue + BG-Lure 1.35 ± 0.41a 0.17 ± 0.05a Navy blue + CO₂ + BG-Lure 13.76 ± 3.42b 0.05 ± 0.01ab Open in new tab Table 2. The percentage of female Aedes aegypti captured of total in semi-field cage and proportion captured of total encounters per hour for BGS trap configurations (different letters indicate significant difference [P < 0.05]) BGS trap configuration . Mean (±SE) percentage captured of total in semi-field cage . Mean (±SE) proportion captured of total encounters . White 3.06 ± 0.83a 0.2 ± 0.05a Navy blue 1.65 ± 0.55a 0.16 ± 0.04a Navy blue + CO₂ 3.67 ± 0.9a 0.08 ± 0.02b Navy blue + BG-Lure 1.35 ± 0.41a 0.17 ± 0.05a Navy blue + CO₂ + BG-Lure 13.76 ± 3.42b 0.05 ± 0.01ab BGS trap configuration . Mean (±SE) percentage captured of total in semi-field cage . Mean (±SE) proportion captured of total encounters . White 3.06 ± 0.83a 0.2 ± 0.05a Navy blue 1.65 ± 0.55a 0.16 ± 0.04a Navy blue + CO₂ 3.67 ± 0.9a 0.08 ± 0.02b Navy blue + BG-Lure 1.35 ± 0.41a 0.17 ± 0.05a Navy blue + CO₂ + BG-Lure 13.76 ± 3.42b 0.05 ± 0.01ab Open in new tab Fig. 1. Open in new tabDownload slide Number of female (mean SE) Aedes aegypti captured (a, b) and number of encounters with trap (X, Y, Z) by trap configuration (different letters above columns indicate significant difference [P < 0.05]). Fig. 1. Open in new tabDownload slide Number of female (mean SE) Aedes aegypti captured (a, b) and number of encounters with trap (X, Y, Z) by trap configuration (different letters above columns indicate significant difference [P < 0.05]). The trap configuration, i.e., whether a trap without an olfactory lure, with CO2 or the BG-Lure was incorporated had a significant effect on both the number of female Ae. aegypti captured and the proportion captured of total encounters (Fig. 1, Table 2). The age of mosquitoes affected the number of encounters with the BGS (P < 0.005); age positively correlated with the number of encounters (P = 0.001719). The mean temperature during the trial had an effect on the proportion captured from encounters (P = 0.01125); the mean temp was negatively correlated with the proportion caught (P = 0.02008). The discrepancy between the Navy blue + CO2 + BG-Lure percentage captured and proportion (Table 2) is due to the high number of multiple encounters by individuals with the trap. The trap configuration had no significant effect on time spent during encounters with the BGS (Fig. 2). The only trap configuration that resulted in data having a significant difference in velocity between trapped and untrapped mosquitoes was the white BGS (P = 0.0061) (Fig. 3). The navy blue + BG-Lure treatment also yielded significantly higher velocity for both trapped and untrapped mosquitoes (P < 0.001) (Fig. 3). Fig. 2. Open in new tabDownload slide Time spent (s) by Aedes aegypti females during encounters with BG-Sentinel (BGS) trap (captured males included; instances where females landed on trap excluded) (× = mean). There was no significant difference in time spent during encounters among treatments. Fig. 2. Open in new tabDownload slide Time spent (s) by Aedes aegypti females during encounters with BG-Sentinel (BGS) trap (captured males included; instances where females landed on trap excluded) (× = mean). There was no significant difference in time spent during encounters among treatments. Fig. 3. Open in new tabDownload slide Velocity of female Aedes aegypti trapped (a, b) and untrapped (X) (× = mean) (different letters above columns indicate significant difference [P < 0.05]; underlined letters indicate significant difference [P < 0.05]). Fig. 3. Open in new tabDownload slide Velocity of female Aedes aegypti trapped (a, b) and untrapped (X) (× = mean) (different letters above columns indicate significant difference [P < 0.05]; underlined letters indicate significant difference [P < 0.05]). Emax describes the straightness of the track, reaching a maximum of 1 for a completely straight track. There were three post hoc treatment groups, untrapped, trapped, and those that flew over the entrance at least once without getting trapped. There were significant differences among treatments for the Emax of untrapped individuals but not among trapped individuals or those that flew over the entrance (Fig. 4). Within treatments, the Emax of trapped individuals was higher (and therefore the track was straighter) than that of untrapped individuals untrapped individuals for the navy blue + CO2 + BG-lure (P < 0.005) (Fig. 4). Fig. 4. Open in new tabDownload slide Flight path straightness (Emax) of XY plane track of female Aedes aegypti untrapped (a, b), trapped (X), that flew over entrance (z) while encountering the BGS trap (× = mean) (different letters above columns indicate significant difference; underlined letters indicate significant difference [P < 0.05]). Fig. 4. Open in new tabDownload slide Flight path straightness (Emax) of XY plane track of female Aedes aegypti untrapped (a, b), trapped (X), that flew over entrance (z) while encountering the BGS trap (× = mean) (different letters above columns indicate significant difference; underlined letters indicate significant difference [P < 0.05]). There were no significant differences in track sinuosity (Bovet and Benhamou 1988) among trap configurations for untrapped or trapped mosquitoes, nor was there for mosquitoes that flew over the trap entrance without being trapped. The velocity of individuals generally increased as they crossed over the trap entrance (Fig. 5). The proportion of individuals whose velocity increased after they crossed over the trap entrance was, for the white BGS 0.67, navy blue 0.75, navy blue + CO2 0.64, navy blue + BG-Lure 0.81, navy blue + CO2 + BG-Lure 0.80. A sample of corresponding video of the front of the BGS of individuals flying over the trap entrance was used to determine the distance at which a mosquito can fly over the entrance without getting pulled in. The shortest distance recorded for an individual flying over the trap entrance without being sucked in was 36.86 mm; the velocity of this individual was 0.26 m/s at this time point (Figs. 6a and b and 7). Fig. 5. Open in new tabDownload slide Proportion of Aedes aegypti females that crossed over the Biogents Sentinel trap entrance at least once without being captured (× = mean) (different letters above columns indicate significant difference [P < 0.05]). Fig. 5. Open in new tabDownload slide Proportion of Aedes aegypti females that crossed over the Biogents Sentinel trap entrance at least once without being captured (× = mean) (different letters above columns indicate significant difference [P < 0.05]). The proportion of mosquitoes that landed on the side of the trap at least once during their encounter varied among trap configurations (P < 0.005) (Fig. 8). The highest mean (±SE) proportion was the most successful trap configuration, the navy BGS + CO2 + BG-Lure, and was 0.14 ± 0.01 (Fig. 8). Fig. 6. Open in new tabDownload slide Example track (shown in red dotted line; dots 1/30 s apart; direction indicated by blue arrow; frame rate 60i) of female Ae. aegypti flying over Biogents Sentinel trap (BGS) entrance without being captured. (a) from above; (b) from front. Fig. 6. Open in new tabDownload slide Example track (shown in red dotted line; dots 1/30 s apart; direction indicated by blue arrow; frame rate 60i) of female Ae. aegypti flying over Biogents Sentinel trap (BGS) entrance without being captured. (a) from above; (b) from front. Fig. 7. Open in new tabDownload slide (a) The Biogents Sentinel trap (BGS): air is sucked into the center funnel (black), is circulated past the lure cartridge inside the body and pushed out through the porous lid; tip of vector arrows (black) is height at which windspeed was measured (the longer the arrow, the stronger the suction). (b) The air velocity of the suction of the BGS at height of rim of center funnel as indicated by white vector circles (the larger the circle, the stronger the suction). Fig. 7. Open in new tabDownload slide (a) The Biogents Sentinel trap (BGS): air is sucked into the center funnel (black), is circulated past the lure cartridge inside the body and pushed out through the porous lid; tip of vector arrows (black) is height at which windspeed was measured (the longer the arrow, the stronger the suction). (b) The air velocity of the suction of the BGS at height of rim of center funnel as indicated by white vector circles (the larger the circle, the stronger the suction). Fig. 8. Open in new tabDownload slide Proportion of female Aedes aegypti that landed on the Biogents Sentinel trap at least once during their encounter (note scale of y-axis) (× = mean) (different letters above columns indicate significant difference [P < 0.05]). Fig. 8. Open in new tabDownload slide Proportion of female Aedes aegypti that landed on the Biogents Sentinel trap at least once during their encounter (note scale of y-axis) (× = mean) (different letters above columns indicate significant difference [P < 0.05]). As ascertained by the track visualizations, there was considerable variability in the trajectory of the tracks within and among trap configurations. The majority of tracks occurred to the bottom right side of the trap (Supp Material [online only]), which can be accounted for by the consistent and slight cross-breeze in the semi-field cage, rendering this area as slightly downwind. The wind speed was ≤ 0.4 m/s throughout the experimental period and was often too low to accurately measure. Discussion This study assessed the efficiency of the widely used BGS mosquito trap. Under semi-field conditions in North Queensland, Australia, the number of female Ae. aegypti mosquitoes encountering a trap was quantified against the number captured. Unsurprisingly, the navy-blue BGS plus CO2 plus the BG-Lure had the highest catch, which supports the idea that these components are acting synergistically (Kline et al. 1991, Takken and Knols 1999, Dekker et al. 2005, Cook et al. 2011, Pitts et al. 2014). None of the BGS trap configurations captured a high proportion of the mosquitoes that came within 210 mm (laterally) of the edge of the trap. Strikingly, even the most successful trap, the navy-blue BGS with CO2 and the BG-Lure captured only 5% of the total encounters. These findings demonstrate a low capture efficiency in a widely used, commercially available trap. Bau and Cardé (2016) and Cardé et al. (2018) found that trap capture efficiency can have a profound effect on detectability and suggested that a trap with low efficiency can produce false negatives in insect surveillance. Our results support previous work in this area. In a mark-release-recapture field experiment in Cairns, Australia, Johnson et al. (2012) found that an unbaited white BGS placed at ground level under a Queenslander-style timber house captured 24.6% of released female mosquitoes in 24 h (mosquitoes being released within 4 and 6.5 m of the BGS). In the present study, the white BGS captured a mean (±SE) of 3.5 ± 0.76 % in 1 h. This exceeds the number caught in Johnson et al. (2012) if extrapolated out to 24 h; however, given that Ae. aegypti are diurnal mosquitoes, if we assume that mosquitoes are being caught in similar Cairns daylight hours (8:00 a.m. to 5:00 p.m.), then the numbers caught per hour are similar (2.73% /h). Johnson et al. (2012) also found that significantly more female mosquitoes were re-captured in the dry season versus the wet season and suggested that exposure to unfavorable conditions, i.e., low humidity in the dry season increased mosquito movement and encounters with traps whereas heavy rain in the wet season impeded mosquito activity. The current work was conducted in the wet season which may have negatively affected capture. The results demonstrate that mosquitoes can have repeated encounters with a BGS trap. Mosquitoes can ‘learn’ (McCall and Kelly 2002, Kaur et al. 2003, Vinauger et al. 2014) and the extent to which experience influences a vector’s choice of host (or trap substituting for a host) or even resting site can affect the vector’s potential for disease transmission (Alonso and Schuck-Paim 2006). Insects are often killed when trapped in an entomological (and usually pest control) setting but, as exemplified in the current study, how many insects may approach a trap and even use it as a resting site, are not caught, leave and return and how many times does this happen? Of course, in the experimental design used there is only one ‘host’ stimulus present in the arena. But perhaps an individual that has investigated the stimulus (be it visual, olfactory, etc.) is more likely to investigate again. The time spent by individuals during encounters with the BGS was similar among treatments; as such there was no significant correlation between the duration of encounter and the number captured. Excluding those landing on the trap, individuals spent a mean (± SE) of 2.83 ± 0.15 s while encountering the most successful configuration, the Navy BGS plus CO2 plus the BG-Lure. The velocity of mosquitoes encountering the trap was significantly higher for the BGS plus the BG-Lure treatment; this is the case for both trapped and untrapped individuals. However, within treatments, only the white BGS yielded a significant difference between trapped and untrapped individuals (the former of which were faster). The presence of the short range (BG-Lure) and the absence of the long-range (CO2) cue may have influenced the velocity at which the mosquitoes fly while encountering a BGS, but this did not correlate with the overall catch or proportion caught from total encounters. In this study, Emax is a measure of the straightness of the mosquito flight in the XY plane while they are encountering the trap. There was a significant difference in Emax between the trapped and untrapped mosquitoes for the most successful trap configuration, the navy BGS plus CO2 plus the BG-Lure; here trapped tracks were straighter than untrapped tracks. A more direct lateral path during an encounter with a BGS plus CO2 plus the BG-Lure appears to result in increased likelihood of capture; the reason for this is unclear. For all trap configurations, a proportion of individuals crossed over the trap entrance without being caught, sometimes multiple times. The data show that there is potential for the BGS to have higher catches if all mosquitoes that cross over the trap entrance are captured. The velocity of individuals generally increased as they crossed over the trap entrance. This may be a mechanosensory response to the suction of the fan. There is evidence of visually-mediated escape responses in Diptera (Hammond and O’Shea 2007), but to the authors’ knowledge, there is no research pertaining to an in-flight mechanosensory escape response mediated by suction. It also could be a response to a sudden change in the visual surround (Cooperband and Cardé 2006a) or both combined. There is evidence that updraft mosquito traps do outperform downdraft traps (Wilton and Fay 1972, Ritchie et al. 2008), which supports the hypothesis of an upward mechanosensory response to suction. To capture individuals flying over the trap entrance, a stronger suction fan and/or a modification to the shape of the entrance to facilitate stronger suction would be required. In order for a mosquito to be captured it must first come into the vicinity and encounter the trap, second fly over the trap entrance and do so at such a height to be sucked in. One-week-old female Ae. aegypti are capable of flying 1.5 m/s in still air (Kennedy 1940). The air downward velocity of the fan of the BGS at 35 mm above the trap entrance is 1.5 m/s. The individual that recorded the shortest distance over the trap entrance (36.86 mm) was traveling at 0.264 m/s at this time point. Somewhat surprisingly, a proportion of mosquitoes landed on the BGS trap during their encounter for all trap configurations. This suggests that the mosquitoes are using the trap as a ‘resting’ site; it is unclear whether they are probing for a bloodmeal but this seems unlikely because some individuals remain stationary for up to 30 min. The results of the current study suggest that by (assuming no excito-repellency) applying a contact insecticide to the outside of the BGS and a catch net around the base, trap capture could potentially be increased by over 25% for the navy-blue BGS plus CO2 plus BG-Lure. All the mosquitoes used in the current work were infected with Wolbachia (wMel strain). There are differences in behavior between Wolbachia-infected and wild-type Ae. aegypti. Evans et al. (2009) found Ae. aegypti infected with wMelpop strain spent more time flying and walking during the day than uninfected individuals. In Drosophila melanogaster, from which wMel is sourced, Wolbachia pipientis infection increases recapture rate of field-released insects compared to uninfected individuals (Caragata et al. 2011). Turley et al. (2014) found that in Y-tube olfactometer assays, infection with Wolbachia (wMelpop strain) did not alter attraction of Ae. aegypti from human odors (worn socks); however, in semi-field conditions with multiple cues acting simultaneously this may differ. The flight behavior of uninfected Ae. aegypti is potentially different from that found here in wMel strain-infected Ae. aegypti and hence the BGS may have different efficiency. This is not only when considering Wolbachia-infection but virus infection as well; Lima-Camara et al. (2011) found that Ae. aegypti infected with dengue virus have increased activity. This is significant when trapping to monitor for arbovirus levels in a wild Ae. aegypti population. Williams et al. (2006a) found differences in absolute attractiveness of several blends between strains of Ae. aegypti in Y-tube olfactometer assays but suggests that the mechanisms making these blends attractive to Ae. aegypti are conserved among populations. One locally supplemented strain with was used in this study which may have biased results; the authors suggest that similar work be conducted with long-standing laboratory strains such as the Rockefeller Ae. aegypti strain. The density of mosquitoes in the semi-field cage used for bioassays was higher than typically found in the field; Ae. aegypti is considered a low-density mosquito species (Scott and Morrison 2003). Koyoc-Cardeña et al. (2019) collected a mean of 13 female Ae. aegypti per house in indoor density estimate sampling in Merida, Mexico. It is unclear whether there were conspecific effects in the current study. For track analysis, an effort was made to only use tracks wherein the subject mosquito was the only individual present; however, in these instances, it was possible that there was another mosquito present resting on the trap, which was not visible in the footage. To the authors’ knowledge there are no conspecific interactions in adult female Ae. aegypti during host-finding. The analysis of the tracks was conducted using only the overhead perspective and, therefore, was only in the XY plane; 3D tracking was not feasible in this setting. The sinuosity and Emax were therefore limited to this plane and, as such, do not capture the entirety of the flight behavior. This may go contribute to the lack of difference noted in sinuosity between treatments and only a difference in Emax between trapped and untrapped insects in the BGS plus CO2 plus BG-Lure configuration. In the applied arena, this work may be used to improve trap design, e.g., in providing estimates for catch improvements from increased suction and contact insecticide on the outside of the trap. These results may also inform density estimates for Ae. aegypti monitoring programs using capture numbers as proxy for total numbers. An understanding of the behaviors associated with a ‘gold standard’ Ae. aegypti trap may assist in further trap design and inform surveillance and control programs for this insect vector. Acknowledgments We thank Michael Townsend and Chris Paton as well as Benjamin DeMasi-Sumner, Emerson Lacey, and Meghan Moore for their support during data collection and analysis, respectively. We acknowledge funding support from the Pacific Southwest Regional Center of Excellence for Vector-Borne Diseases funded by the U.S. Centers for Disease Control and Prevention (Cooperative Agreement 1U01CK000516). References Cited Allan , S. A. , and J. F. Day. 1987 . 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TI - Attraction Versus Capture: Efficiency of BG-Sentinel Trap Under Semi-Field Conditions and Characterizing Response Behaviors for Female Aedes aegypti (Diptera: Culicidae)
JF - Journal of Medical Entomology
DO - 10.1093/jme/tjz243
DA - 2020-05-04
UR - https://www.deepdyve.com/lp/oxford-university-press/attraction-versus-capture-efficiency-of-bg-sentinel-trap-under-semi-nhyXY0Gymd
SP - 884
VL - 57
IS - 3
DP - DeepDyve
ER -