Abstract Due to the limited understanding of the sylvatic cycle of Chagas disease transmission, an efficient method to attract and capture sylvatic triatomines (Hemiptera: Reduviidae) is essential to monitor human exposure risk. Current collection methods for sylvatic species, though effective, are labor- and time-intensive. This study evaluated whether modified cross-vane panel traps (commonly used in forest entomology) can be used to attract and capture flying life-stages of sylvatic triatomines and whether a commercially available lure is effective in attracting sylvatic triatomines in the field. We evaluated four trap treatments in both the wet and dry seasons in central Panama: a cross-vane panel trap fitted with an ultraviolet (UV) light, a cross-vane panel trap fitted with a commercially available human-volatile lure, a cross-vane panel trap fitted with both a UV light and a human-volatile lure, and a white sheet fitted with a UV light (a standard collection method) as a control. A total of 45 adult Rhodnius pallescens Barber were captured across 10 nights of trapping representing 112 trap-nights. There was a significant overall effect of trap type on collection success; sheet traps collected more triatomines than lure traps, and there were no differences between the sheet trap and the UV trap, nor between the sheet trap and the UV + lure trap. The lure-only trap did not capture any triatomines in this study. These results indicate that cross-vane panel traps with a UV light are as effective as a sheet trap but offer the advantage of requiring less time and effort to maintain and monitor. Triatominae, chagas disease, vector ecology, Public Health Entomology, sylvatic habitat Introduction Surveillance of blood-feeding insect vectors using consistently replicable collection methods is an important component of vector-borne disease management and vector control. Triatomine (Hemiptera: Reduviidae) “kissing bugs” are blood-feeding insects capable of transmitting the parasite Trypanosoma cruzi, the causative agent of Chagas disease (Lent and Wygodzinsky 1979). Some triatomine species have adapted to complete their life cycles within homes, and substantial research has been performed on collection methods allowing researchers to monitor these domestic populations (Gürtler et al. 1999, Abad-Franch et al. 2011, Rojas de Arias et al. 2012). However, few studies have addressed population dynamics of sylvatic (i.e., wild-living) triatomine species, particularly with respect to how fluctuations in these populations may affect disease transmission risk to humans. Current methods for monitoring sylvatic triatomine populations can be labor-intensive, time-consuming, and expensive (Noireau et al. 2005) and there is need for more efficient collection methods (Coura et al. 2014, Hotez et al. 2014). Methods for intradomiciliary triatomine collections include the pitfall trap (Guerenstein et al. 1995, Lorenzo et al. 1998, Milne et al. 2009), baited or unbaited sticky traps (Abrahan et al. 2011, Rojas de Arias et al. 2012), and timed manual searches (Gürtler et al. 1999). To capture sylvatic triatomines, typically either a standard insect light trap (i.e., a light reflected on a white sheet) (Vazquez-Prokopec et al. 2004, Rebollar-Téllez et al. 2009) or Noireau trap (i.e., a sticky trap baited with a live animal, such as a mouse) is used (Abad-Franch et al. 2000, Noireau et al. 2002). Both methods can be labor- and time-intensive and, in the case of Noireau traps, require maintaining and deploying live animals in the field. Additionally, although Noireau traps have been effective in trapping triatomines in palms and hollow trees (Abad-Franch et al. 2000, Noireau et al. 2002), in some cases they have not been as effective in other habitats (Suarez-Davalos et al. 2010). In Panama, the vast majority of vector species, including Rhodnius pallescens (Barber), the most important vector of Chagas disease in Panama, are sylvatic (Christensen and de Vasquez 1981, Zeledón and Rabinovich 1981). Noireau traps are commonly used for the capture of sylvatic R. pallescens from their principal habitat of palm crowns (Whitlaw and Chaniotis 1978; Gottdenker et al. 2011, 2012). Various alternatives to live baits have been tested including baker’s yeast (Guerenstein et al. 1995; Lorenzo et al. 1998, 1999) and synthetic host-odor mimics with CO2 (Barrozo and Lazzari 2004). Recently, a multimodal bait has been shown to attract Triatoma infestans (Klug) in the laboratory and the field and Rhodnius prolixus (Stal) in the laboratory (Ryelandt et al. 2011). Additionally, a commercially available lure designed to attract Aedes spp. mosquitoes attracted Rhodnius prolixus under laboratory conditions (Guidobaldi and Guerenstein 2013, 2016). However, these alternative baits have not yet been tested for other sylvatic species of triatomine, nor extensively tested under field conditions. This study had two main objectives: first, to determine if a cross-vane panel trap (Fig. 1), commonly used in forest entomology (McIntosh et al. 2001, Graham et al. 2010), could be modified to attract and capture flying life-stages of sylvatic triatomines, and, second, whether a commercially available lure would be effective in attracting sylvatic triatomines in the field. In total, four trap treatments were experimentally evaluated across wet and dry seasons in central Panama where R. pallescens and several other species of sylvatic triatomines occur. Fig. 1. View largeDownload slide Representation of trap types. Drawings not to scale. Fig. 1. View largeDownload slide Representation of trap types. Drawings not to scale. Methods Study Site This study was conducted in Llanito Verde, Panama Oeste, Panama. This community was chosen due to previous collection of several sylvatic triatomine species within and around the community (unpublished data). Three transects were established approximately 230–330 m apart at the edges of residential properties in small pockets of natural habitat consisting of trees and other vegetation, including Attalea butyracea palms, which are known to be an important habitat for Rhodnius pallescens (Whitlaw and Chaniotis 1978, Lent and Wygodzinsky 1979). Based on the availability of these habitats, the three transects were 94 m, 85 m, and 62 m long, and one of each of the four different trap types were equally spaced across each transect with a minimum distance of 20 m between traps. Trap Description and Deployment Cross-vane panel traps consisted of two 30 × 30 cm squares of corrugated white plastic coated in Fluon, notched and fitted together to form an X pattern, attached to a large funnel made of the same plastic. This funnel was attached to another 30 cm-diameter round funnel fitted with a 950 ml-wide mouth jar. Cross-vane traps with three different potential attractants were tested: a cross-vane panel trap fitted with a ultraviolet (UV) light (Flourescent, U-shaped FUL 4-pin GX10Q 18W or 15W black light, hereafter, “UV trap”), a cross-vane panel trap fitted with a chemical lure designed to mimic human skin volatiles (“BG-Lure-Cartridge”, Biogents, Regesberg, Germany, hereafter, “lure trap”), and a cross-vane panel trap fitted with both a UV light and a chemical lure (hereafter, “UV + lure trap”) (Fig. 1). A white sheet (approximately 159 × 260 cm) suspended vertically between two trees and illuminated by a UV light (hereafter, “sheet trap”), served as a control as this is commonly used for capturing sylvatic triatomines (Vazquez-Prokopec et al. 2004, 2006; Carbajal de la Fuente et al. 2007; Rebollar-Téllez et al. 2009). Under MiAmbiente permit SC/A-43-16, traps were deployed for six nights in July and August 2016 during the wet season and four nights in December 2016 at the beginning of the dry season. The location of each trap on each transect was rotated every night, such that each trap was at each location at least once per season, using a modified Latin Square design. One of each of the four trap types were deployed on each transect for 3.5 hours per night, starting approximately 15 min before sunset, as these hours immediately following dusk are when triatomines tend to be most active (Rebollar-Téllez et al. 2009). Due to occasional failure of lights, total trap-nights were: sheet trap (27 trap-nights), UV trap (27 trap-nights), lure trap (30 trap-nights), and UV + lure trap (28 trap-nights). Two wattages of UV light were used (15 W and 18 W) due to equipment failure and lack of access to replacement bulbs. All UV lights were powered with 12 V rechargeable DC batteries and fitted with timers that activated and deactivated simultaneously. Sheet traps were either monitored continuously or checked at 15–20 minute intervals; all triatomines on sheets were collected immediately. Cross-vane panel traps were not monitored throughout the night, and all captured triatomines were retrieved at the end of the 3.5-h interval. Captured triatomines were stored in 95% ethanol and identified according to Lent and Wygodzinsky (1979). Statistical Analysis We conducted statistical analysis in R using the lme4 package (Bates et al. 2015). A linear mixed model was performed on log + 1 transformed capture data. Trap type (four types) and season (wet vs dry) were included as fixed variables, whereas location within transect was included as a random variable. Similar analyses (linear mixed models on log + 1 transformed data) were conducted to determine if wattage of light and whether sheet traps were continuously monitored contributed significantly to differences in trap success. Results We captured a total of 45 adult triatomines, 20 female and 25 male Rhodnius pallescens, across 112 trap-nights. There was an overall effect of trap type on collection success (F = 3.68, P = 0.015; Fig. 2), and no difference in collection across season (F = 3.28, P = 0.07; Fig. 3). Post hoc analyses revealed sheet traps collected more triatomines compared to the lure traps (Tukey’s HSD: P = 0.008), which did not capture any triatomines throughout the study. There were no differences between the sheet trap and the UV trap, or between the sheet trap and the UV + lure trap (Tukey’s HSD: P = 0.85 and 0.62, respectively). Fig. 2. View largeDownload slide Mean number of triatomines captured per night by trap type. Error bars represent one standard error. Fig. 2. View largeDownload slide Mean number of triatomines captured per night by trap type. Error bars represent one standard error. Fig. 3. View largeDownload slide Mean number of triatomines captured per night by season. Error bars represent one standard error. Fig. 3. View largeDownload slide Mean number of triatomines captured per night by season. Error bars represent one standard error. Sheet traps were either monitored continuously (12 trap-nights) or checked every 15–20 minutes (15 trap-nights); there was no difference in capture rates based on continuous versus periodic monitoring (P = 0.83). Finally, there was no difference in capture rates based on wattage after controlling for the effect of transect (P = 0.21). Discussion An efficient method for attraction and capture of sylvatic triatomine species is essential to monitor populations in areas where human risk may exist. This study captured a total of 45 Rhodnius pallescens using primarily unmonitored traps fitted with a UV light. The majority of these were collected during the dry season, although the effect of season on capture success was not significant. Traps captured two other species of triatomine (Triatoma dimidiata (Latreille) and Pantstrongylus geniculatus Latreille) during preliminary testing (unpublished data); however, only R. pallescens was captured during the experiment described here. Throughout the study, neither triatomines nor bycatch were collected in traps fitted with only a chemical lure. However, traps fitted with either a UV light or with both a UV light and chemical lure were equally effective in attracting and trapping triatomines, and the capture rate of these traps was similar to those of a standard sheet trap. Capturing sufficient numbers of triatomines to estimate infection prevalence and population dynamics can be a time- and labor-intensive process. Noireau traps, while effective with capture rates of 2.25 (Gottdenker et al. 2011) to 2.5 (Abad-Franch et al. 2000) triatomines per trap, require extensive equipment, maintenance of live animal colonies, and knowledge of nesting sites of triatomines (Abad-Franch et al. 2000, Noireau et al. 2002). The standard method of collection using a UV light yields capture rates of 0.3–0.4 (Vazquez-Prokopec et al. 2004, 2006), or more (Carbajal de la Fuente et al. 2007, Rebollar-Téllez et al. 2009) triatomines per trap, but requires constant or frequent monitoring by observers to capture and remove any triatomines that land on the sheet, limiting the overall number of traps that can be deployed. This study used a trap with the same attractant properties, yielding a capture rate of 0.54 triatomines per trap (considering only traps with UV lights), while allowing for triatomines to be captured in a collection container without the need for monitoring or intervention. Triatomines flying toward the light collide with the sides of the cross-vane panels and fall down the Fluon-coated surface into the collection container (Graham et al. 2010). Limitations to this study include the use of UV lights as the source of light. Although UV light is often used as an attractant for a variety of insects, including triatomines (Noireau et al. 1997, Ashfaq et al. 2005, Vazquez-Prokopec et al. 2006, Shimoda and Honda 2013), it may not be the most relevant light source for peridomestic environments where other lights sources dominate. Additionally, Minoli and Lazzari (2006) found that triatomines may be more attracted to white light wavelengths compared to other wavelengths of light (but see Pacheco-Tucuch et al. 2012). Future studies should test a variety of light types, but in the interim these traps using UV light can be effective, and, by using a potentially less attractive light source we may have underestimated their overall effectiveness. The chemical lure tested in this study is effective in a laboratory environment (Guidobaldi and Guerenstein 2013, 2016); however, it was not effective at capturing triatomines in this study. This lure may be effective at close range but may not be effective at the long ranges necessary to attract flying triatomines in the field. While the lure did not increase capture rates of triatomines when used in combination with a longer-range UV light lure, it is possible that adult triatomines attracted to lights are in search of mates, as male R. prolixus have been shown to initiate flight in response to female pheromones, (Zacharias et al. 2010) and therefore not actively host-seeking. This could make the addition of host odors to a light trap ineffective. Additionally, the lure used in this study has been tested in mosquito traps using a fan to aid in odor dispersal (Harwood et al. 2015, Akaratovic et al. 2017). It remains to be tested whether this lure could function as an attractant for sylvatic triatomines in combination with a fan. Future studies should compare this lure with a more similar attractant, such as a Noireau trap, to establish whether it could be effective in attracting sylvatic triatomines under field conditions, test pheromone lures for attracting flying adults, and potentially include a fan for odor dispersal on the traps. Understanding and monitoring sylvatic triatomine population dynamics is an important aspect of disease management for several reasons. First, in many areas, re-infestation of houses following insecticide treatment is thought to occur from sylvatic populations (Gürtler et al. 1999, Sanchez-Martin et al. 2006, Noireau 2009, Ceballos et al. 2011). Second, some sylvatic species show signs of ongoing domestication (Noireau et al. 1995, Wolff and Castillo 2002, Reyes-Lugo 2009). Finally, in some Chagas endemic areas, including Panama, human transmission may be driven by sylvatic species (Pipkin 1968; de Vasquez et al. 2004; Calzada et al. 2006, 2010; Saldaña et al. 2012). This study represents a new implementation of a trap traditionally used in forest entomology in a medical entomology framework. The traps themselves are lightweight (<1.15 kg without battery), easily transportable, and require the same light and battery as a sheet trap. Furthermore, they can be deployed and captured bugs can be collected without the need for continuous monitoring. These findings present exciting possibilities for research in the field of vector biology, but they also offer potential for an important surveillance tool for public health applications. Acknowledgments We thank Argelis Aneth Sanchez, Erin Welsh, Austin Garrido, and Rachel Crisp for field assistance; Scott Baker and Jared Bear for trap fabrication; Nicole Gottdenker and Azael Saldaña for advice; and May Berenbaum, James O’Dwyer, Andrew Suarez, and the Allan lab for manuscript feedback. Thank you to the Smithsonian Tropical Research Institute for facilitating this research. Funding provided by the University of Illinois Campus Research Board (RB16072) and Graduate College (Dissertation Travel Grant). References Abad-Franch, F., F. Noireau, A. Paucar, H. M. Aguilar, C. Carpio, and Racines J.. 2000. The use of live-bait traps for the study of sylvatic Rhodnius populations (Hemiptera: Reduviidae) in palm trees. Trans. R. Soc. Trop. Med. Hyg . 94: 629– 630. Google Scholar CrossRef Search ADS PubMed Abad-Franch, F., Vega M. C., Rolón M. S., Santos W. S., and Rojas de Arias A.. 2011. Community participation in Chagas disease vector surveillance: Systematic review. PLoS Negl. 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Journal of Medical Entomology – Oxford University Press
Published: Mar 1, 2018
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