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W4249357159 abstract "Triatoma dimidiata is the vector of Trypanosoma cruzi in the Yucatan Peninsula (YP). Earlier studies have shown that domestic and peri-domestic populations of the vector originated from the sylvan stock and that effectiveness of insecticide-spraying was affected by re-infestations of houses from the sylvan T. dimidiata population. In addition, in the YP most previously published reports have focused on domestic and peri-domestic populations and very little is known about the nocturnal behavior of the sylvan populations. The main aim of our study was to determine the nightly activity patterns of adult T. dimidiata in a selected location in the YP. Secondly, we sought to document the reproductive status and infection rate of active females. During eight sampling nights spaced from late March to late July, 2007, we collected 544 adult T. dimidiata. We found that square-cloth illuminated white traps were effective to attract the sylvan individuals and that T. dimidiata adults exhibited a unimodal activity pattern throughout the night. The accumulated mean of captured bugs also showed a non-linear distribution for females and males. Furthermore, we found that male and female catches were significantly correlated with the means of temperature and humidity recorded during the sampling period. Out of 46 dissected females, we observed that 43.5% of females had fully-formed eggs in their abdomens, and only two females (4.4%) had sperm within the spermatheca. The infection rate of T. dimidiata harboring T. cruzi was found to be 3.7%. The implications of the light attraction to bugs and potential dispersal capabilities are discussed in the paper in the context of infestation/re-infestation of rural houses by sylvan T. dimidiata flying adults. The triatomine bugs (Hemiptera: Reduviidae: Triatominae) are the main vectors of the parasite Trypanosoma cruzi (Chagas) which is the causative agent of Chagas disease. It is thought that in the Americas, approximately 100 million people are at risk and that potentially 10 million could be infected (World Health Organization 1991, Schofield et al. 2006). In Mexico, the prevalence infection rate has been reported to be almost 2 million persons with an estimated incidence rate of ≈70,000 per year (Ramsey and Schofield 2003, Ramsey et al. 2003). Although T. cruzi infections can be acquired during blood transfusions, it is believed that most human infections are due to vectorial transmission involving 27 different species of triatomine bugs (Ramsey et al. 2003). With regard to the causative parasite in Mexico, Bosseno et al. (2002) analyzed 56 T. cruzi stocks isolated from different geographic regions of the country, finding a dominance of occurrence of T. cruzi lineage I and only two isolates that were clustered with lineage II. This suggests that T. cruzi parasites circulating in Mexico are significantly different from those of South American origin, which essentially belong to lineage II. Regionally in the Yucatan Peninsula (YP), the first studies on triatomine bugs were carried out by Mazzotti (1940), and years later it was demonstrated that bugs were naturally infected with T. cruzi (Tay and Biagi 1964). The main vector species in the YP is Triatoma dimidiata (Latreille) which possesses a large distribution area throughout Mexico and Central America (Martínez-Campos 2003). Due to its large distribution range, there have been reports on variability of size, morphology, and body pigmentation (Lent and Wygodzinsky 1979). Nonetheless, it is currently recognized in Mexico that T. dimidiata is composed of at least two subspecies or clades; one occurring in the central states of Mexico (clade 2) and the other in southeast Yucatan (clade 1) (Marcilla et al. 2001). Other authors such as Tamay-Segovia et al. (2008), using the internal transcriber spacer-2 (ITS-2), characterized specimens from seven locations of the state of Campeche in the YP, finding that T. dimidiata clade 1 was found mainly in the tropical rain forest areas, whereas clade 2 was found in the coastal areas. Recent studies with T. dimidiata have also detected a very large intraspecific variation within the complex in Central America, suggesting that T. dimidiata members may exhibit different vectorial capacities (Bargues et al. 2008, Dorn et al. 2009). Control of the disease still depends largely on the control of the vector, so it is necessary to understand how sylvan populations may affect domestic and peri-domestic T. dimidiata populations and thus the efficacy of vector control schemes. Dumonteil et al. (2002) had hypothesized that due to seasonal abundance, T. dimidiata flying adults were likely to invade domestic and peri-domestic environments from the sylvan habitat. This phenomenon was indeed shown to occur by Dumonteil et al. (2004) who studied re-infestation patterns of T. dimidiata in domestic houses that had been insecticide-sprayed. On the other hand, an examination of other published studies carried out in the YP (González-Angulo and Ryckman 1967, Quintal and Polanco 1977, Guzmán-Marín et al. 1991, Dumonteil et al, 2002; Ruiz-Piña and Cruz-Reyes 2002; Guzmán-Tapia et al. 2005) shows that all of them have focused on the domestic/peri-domestic populations of T. dimidiata and, with the exception of the work of Dumonteil et al. (2007), the sylvan population has rarely been collected and analyzed. Hence, in this study we sought to document the nightly activity patterns of male and female T. dimidiata from the sylvan populations in a selected site of the Yucatan as well as to assess the reproductive status and the T. cruzi infection rate of adults during the sampling period. The study was conducted in the ejido San Pedro Chacabal, Motul, Yucatan (N 21°07′53″ and W 89°12′00″), which is located 55 km northeast from the city of Mérida at an altitude of 19 m above sea level (masl). The weather in the region is classified as hot-humid with a marked drought season from January to May followed by a rainy season. The main sources of income for the inhabitants of the village (known as ejido in Spanish) are agriculture-based activities with other employment, especially among the young people, in factories located in the city of Motul. One of the agriculture practices concerns the cultivation and exploitation of henequen plants, and in fact some areas around the village are allocated to this activity, whereas other areas are characterized by the presence of secondary vegetation, thus creating a fragmented landscape. The collection points were selected on the basis of road accessibility and the presence of vegetation patches with no influence from nearby agriculture-oriented patches. Following a dirt road from the village, we selected the two collection points at 1.5 km and 2.5 km from the closest dwelling. Collection points were geo-referenced using a hand-held global position system (GPS) (Magellan Explorist 200, San Dimas, CA). Adult T. dimidiata were collected by fluorescent white light traps consisting of a white cloth (1.5 × 1.5 m) suspended by the upper points from nearby tree branches and anchored to the ground by attaching the lower points to heavy rocks (Figure 1). Illumination was provided by a 6-V rechargeable lamp (Truper Herramientas™, S.A. de C. V., Estado de México), which usually lasted for two continuous hours of illumination, and thereafter a new charged lamp was switched on. Catches were conducted on eight sampling dates beginning in late March and ending in late July, 2007. We selected these collection dates based on previous reports of T. dimidiata abundance in domestic catches (Dumonteil et al. 2002, Ruiz-Piña and Cruz-Reyes 2002, Guzmán-Tapia et al. 2005) which had shown that population peaked during the dry hot season. On every collecting date, we set traps at the two sampling points before the sunset, and just when light conditions changed from dim-light to darkness, the lamps were switched on. From that moment and regardless of the clock time, we began to measured the time elapsed from that “zero minute interval” until the arrival of light conditions at dawn, so time was expressed as periods or intervals in minutes after dusk: 0–60, 61–120, 121–180…and so forth, until the tenth period of 540–600. Adult triatomines were captured directly from the white-square cloth (Figure 1) if they landed on the illuminated screen. In addition, we collected all bugs that were observed walking in a four to five m perimeter around the illuminated trap. Catches were performed by two teams composed of at least three persons and each team was deployed at each collection point. Because the collection of bugs was meant to be carried on throughout the night, the catching teams were scheduled to undergo duty shifts of roughly three to four hours followed by a one to two hour sleep break. Collectors were requested to record the exact minute after dusk every time a bug was caught and to record the temperature and humidity every 30 min. All adult bugs were carefully caught either by using a pair of rounded-tip forceps or by placing a disposable 100 ml plastic container up-side-down over the bug. Then, with a gentle pencil push, they were introduced into the container and a plastic lid was quickly added. On collection, all bugs were sexed and placed individually in disposable containers that had previously been lined on the bottom with a round piece of white paper and a small piece of corrugated paper placed vertically. For transportation to the laboratory facilities in Mérida, containers were stacked in polystyrene ice-boxes. Bugs were maintained in a fan-ventilated room until they were processed. A white square cloth (1.5 × 1.5 m) used as an illuminated screen to attract adult T. dimidiata. Only unfed females were dissected within a week of the collection date. Our goal was to dissect 20% of the total female catches. However, we were only able to examine 14.4% to assess reproductive status. Bugs were chilled for at least 10 min before being placed ventral side up on a standard Petri dish filled with non-toxic plasticine. Legs were held down with standard pins and the abdomen was gently and carefully side-opened in order to extract and count the number of eggs in the ovaries (Figures 2A, 2B). Likewise, the spermathecas were teased apart and were placed onto a microscope slide with a drop of PBS. A cover slip was added and it was gently pushed down to squeeze the spermatheca and release the sperm. Insemination status was inspected under a light microscope, and no attempts were made to assess whether or not sparmathecas were partially or fully filled with sperm. We only recorded females as inseminated if sperm was visible (regardless of amount) or uninseminated if no sperm was visible. Photographs depicting a T. dimidiata female before dissection (A) and after dissection showing eggs in the abdomen (B). The last abdominal segment of each individual triatomine bug was removed with a sterile scalpel and placed in a sterile glass mortar for maceration. A lysis solution (200mM Tris-HCl pH 7.5, 250mM NaCl, 25mM EDTA y 0.5% SDS) was then added and processed as previously described (Edwards et al. 1991). After re-suspension in the lysis solution, the homogenate was left for >1 h at room temperature and then centrifuged at 10,000 g. Three-hundred μl were added to a clean mirocentrifuge tube and an equal volume of isopropilic alcohol was aggregated and gently mixed by inversion of the tube. Later, this homogenate was centrifuged for 10 min as above; then the supernatant was discarded, the pellet was dried under vacuum in a Savant DNA desiccator system (Savant, Inc. U.S.A.). Finally the pellet was re-suspended in 50 μl of double-distilled sterile water. The reaction mix for the PCR procedure was prepared using a GoTaq Green Master Mix PCR mix from Promega (Promega Corp. U.S.A.) as proposed by the manufacturer. The mix had the 1× master mix (2× Green GoTaq reaction buffer pH 8.5 containing 400 μM of each dNTP, Taq DNA polymerase and 3 mM MgCl2), 10 pmol of each primer (Tc1: 5′-TTGAACGGCCCTCCCAAAAC-3′ and Tc2 5′-GATTGGGGTTGGTGAAATATA-3′) and about 10 ng of DNA in a final volume of 20 μl. The cycling temperatures were used as in Dorn et al. (1997) as follows: a denaturing step at 94° C for 2 min, followed by 35 repetitions of 94, 55, and 72° C 1 min each, and then a final extension step of 10 min at 72° C. Diagnosis of infection was carried out by identification of a 235 bp fragment after the electrophoresis of an aliquot of PCR product in a 1.5% agarose-TBE stained with ethidium bromide (10 μg/ml) and further documentation in an EDAS 290 gel documentation system (Kodak, Rochester, NY). Since the nightly abundance of T. dimidiata per collection site showed a similar pattern, we pooled those data for each sampling date so that activity during each time interval after dusk is expressed as a separate mean for males and females. Patterns of activity were correlated with temperature and humidity using linear regression analysis and Pearson's coefficient (Minitab™ version 10.2, Clecom, UK). Regressions and correlations were considered significant if p< 0.05. In order to analyze the rate of activity between males and females, we regressed the accumulated mean observed data points against the time intervals after dusk for males and females. The regression equation Y =α+β ln(X) was adjusted by the least square method for data of both sexes separately, whereas the Pearson correlation coefficient also was computed for each sex. Both analyses were conducted with Excel™ (Liengme 1997). A total of 544 adult T. dimidiata (225 males and 319 females) were collected during eight sampling nights from March to July, 2007. Most adult bugs were found to be unfed at the time of collection. The highest collection occurred on May 11th, when we captured 159 adults (66 males and 93 females). Both male and female T. dimidiata exhibited a unimodal daily activity pattern during the night, reaching its highest point towards the time interval of minutes after dusk of 121–180 with a lower peak around 421–480 (Figure 3). Even though females were more abundant than males, in general terms the activity pattern displayed by both sexes followed the same trend. We found significant correlations between the mean number of male and female T. dimidiata with temperature and humidity recorded at each time interval after dusk. For example, female T. dimidiata were significantly affected by the variables [Y= -17-4 + 0.898 (temperature); F = 7.03; d.f= 1,9; p=0.03; r= 0.684] and [Y= 20.4 – 0.199 (humidity); F= 10.51; d.f= 1,9; p=0.012; r= .0754], whereas males were found to be very significantly regressed [Y= -14-7 + 0.734 (temperature); F = 22.5; d.f. = 1,9; p = 0.000; r = 0.860] and [Y = 15.3 – 0.152 (humidity); F = 28.35; d.f.= 1,9; p = 0.000; r = 0.883]. Analyzing the rate of recruitment of the mean number of T. dimidiata adults in relation with the time intervals after dusk, we found that both sexes were significantly regressed to a logarithmic regression model (Figure 4), which had an almost perfect fit with observed data points. Nightly activity pattern of adult T. dimidiata collected in a sylvan habitat near the village San Pedro Chacabal, Motul, Yucatan, in Mexico. The y-axis represents the mean number of bugs collected per time interval after dusk (x-axis). Circles in the plot represent the observed data on female activity, whereas open triangles represent the observed activity for males. Nightly capture distribution of T. dimidiata adults (females = filled triangles, males = open triangles). Each point is the accumulated mean of insects (y-axis) collected at that time interval after dusk (x-axis). Dissection revealed that 43.5% (n= 20) of females had fully-formed eggs in their abdomens (Figure 2B). In all females that had eggs in their abdomens, we observed a total of 102 eggs (average 2.22 per female). On the other hand, out of those 46 females that were dissected, we found only two females (4.4%) that had visible and still motile sperm within the spermatheca. Regarding the natural infection rate among adult T. dimidiata, we observed that only eight (five males and three females) out of 215 (3.7%) bugs had detectable amounts of T. cruzi's DNA as revealed by a PCR protocol. Infected bugs were found scattered from April (n=1), May (n = 3), June (n = 3), and July (n = 2). To the best of our knowledge, this is the first field observation of the nightly activity of the sylvan population of adult T. dimidiata in Mexico. Our results were similar to other studies with triatomines (e.g., Sjogren and Ryckman 1966, Noireau and Dujardin 2001), in which night activity was reported as unimodal. Sjogren and Ryckman (1966) reported that Triatoma protracta (Uhler) was more abundant in temperature ranges of 21.6 to 23.6° C and with humidity levels of 51–60 and 61–70%, respectively. Compared with our data with T. dimidiata, we also found that both climatic variables possibly are correlated with or had an influence on the nightly activity of adults. Other variables such as atmospheric pressure, wind direction, wind speed, and phase of the moon could also be involved in the activity patterns observed in T. dimidiata. Nevertheless, none of the above-mentioned variables was measured in our study, and for this reason it is highly recommended that in future studies they are recorded in order to gain a better understanding on how these external factors may interact with the nightly activity behavior displayed by T. dimidiata. Collection of triatomine bugs with illuminated traps has been successfully employed by others (Sjogren and Ryckman 1966, Lehane and Schofield 1982, Noireau and Dujardin 2001, Vazquez-Prokopec et al. 2004), showing their importance to an understanding of flight activity patterns of triatomines. Flying adults are commonly reported to be attracted to light sources in the domestic/peri-domestic environment. Nocturnal insects such as triatomines have eyes adapted to low-light intensity conditions, and at least for Triatoma infestans (Klug), it has been reported that movements of the visual pigments of the ommatidia are controlled by an endogenous circadian oscillator, which allows insects to gather more light in their peripheral rhabdomeres, thereby increasing eye sensitivity at night (Reisenman et al. 2002). Flight initiation in triatomines has partially been explained as a result of a light stimulus. For example, Minoli and Lazzari (2006) evaluated the effect of different light sources on the take-off activity of T. infestans and Rhodnius prolixus (Stål). Their findings revealed different degrees of take-off activity among the two studied species, but also of sexes, with females being more frequently active than males. Minoli and Lazzari (2006) demonstrated that white light actually lures bugs to initiate flight, and the authors also suggested that perhaps the use of non-attractive lights in the domestic/peri-domestic environment could reduce the number of invading bugs from the sylvan habitat. In our field study, the catches of T. dimidiata were not influenced by any light source other than the 6-V lamp. The fact that we collected more females than males throughout our study may confirm the experimental results of Minoli and Lazzari (2006) who found females more eagerly attracted to light. With regard to the overall effect of light on the T. dimidiata collections, we cannot rule out the possibility that some adults were attracted in response to our body odor profiles or to the combination of light plus human odors. On a few occasions we actually noticed that some adults were landing directly upon us, however at this stage we cannot distinguish whether or not they were attracted soley to the light or by the combination of human kairomones emitted by ourselves in addition to the light stimulus. In addition to light, flight initiation and dispersal have also been proposed as the result of a hunger drive (Sjoren and Ryckman 1966, Lehane and Schofield 1982, McEwen and Lehane 1993, Noireau and Dujardin 2001). Schofield (1980) proposed that starvation was the main cause for triatomines to initiate flight and therefore dispersal. Based on the body weight/wing length (W/L), the same author showed that domestic T. infestans bugs had a significantly greater W/L ratio than flying adults. This pattern was not observed by Noireau and Dujardin (2001) with T. guasayana Wygodzinsky and Abalos or T. sordida (Stål). In our study with T. dimidiata, we did not measure the ratio (W/L), however, we believe that most of the captured adults (both males and females) were undernourished at the time of the collection as we did not observe any bugs with blood in their abdomens. Furthermore, the fact that females had low counts of eggs in their abdomens may reflect the fact that the adult sylvan population was mainly unfed, although the actual reasons remain unknown. Triatoma dimidiata possess a long life cycle from egg to adults of approximately 11 months under laboratory conditions and perhaps longer in the wild due to blood feeding frequency (Zeledon et al. 1970a). Furthermore, adults have a prolonged life span that in the wild may be up two years (Zeledon et al. 1970b), and it has been reported that all nymphal stages and adults are capable of withstanding starvation and that perhaps this mechanism helps individuals survive when hosts are not commonly available, as suggested by Noireau and Dujardin (2001). Studies on population dynamics, foraging behavior, and spatial distribution of potential hosts in the area are needed to estimate the density and activity patterns of the potential blood sources. These studies may hold the key to understanding the dynamics of blood-feeding, reproduction, and dispersal of T. dimidiata in the YP. Invasion of the sylvan population into the domestic/peri-domestic environment is likely to occur as shown by Dumonteil et al. (2004, 2007) during the season of high abundance of T. dimidiata in Mexico. Re-infestation of houses from the wild population has also been reported to occur in Colombia (Ramírez et al. 2005). Risk factors for T. dimidiata infestation have been reported as a combination of variables such as houses with tile roofs, dirt floors, accumulated firewood indoors, and bad sanitary conditions (Starr et al. 1991). In addition, it has been reported that T. dimidiata has increasingly been found in man-made habitats and that the presence of domestic animals in the peri-domestic environment offers suitable conditions for bugs who seek shelter and a blood meal. In the YP, the presence of some of the risk infestation factors mentioned above is commonly found in rural communities and may be associated with the establishment of T. dimidiata adults that arrived actively or passively to the domestic environment. Our study shows that T. dimidiata are capable of flying towards a light source and that in most cases those bugs were found unfed. In the Yucatan, most dwellers usually use incandescent bulbs to illuminate the inside and outside of their homes, and the outside bulbs are frequently left switched on throughout the night. The idea of Minoli and Lazzari (2006) that employing less attractive lights in the domestic environment would reduce the invasion of sylvan bugs sounds interesting, although the main challenge to implementing this strategy would be to produce light bulbs inexpensively enough to compete in cost with traditional incandescent bulbs. Control efficacy of triatomine bugs in Mexico will be reduced if continuous re-infestation from the sylvan population occurs in the domestic environment. Apart from reducing (modifying) all potential suitable places for breeding and/or feeding for T. dimidiata, control actions would also benefit if the dispersal patterns, temporality, and flight behavior activity of bugs are also considered to be key components for domestic infestation. We thank the inhabitants of San Pedro Chacabal, Motul, Yucatan, for facilities provided to conduct field work. We are also obliged to Angel Polanco-Rodríguez and a group of enthusiastic students that eagerly participated in and committed themselves to each field trip." @default.
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W4249357159 title "Abundance and Nightly Activity Behavior of a Sylvan Population ofTriatoma dimidiata(Hemiptera: Reduviidae: Triatominae) from the Yucatan, México" @default.
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