Water temperature and microenvironmental factors predict the presence and detection of the snail host of Fasciola hepatica in Andean Patagonia.

The transmission of Fasciola hepatica occurs only where there are -or recently were- aquatic or amphibious snails of the Lymnaeidae family, the intermediate host of this parasite. Direct detection of these snails is time-consuming and imprecise, hindering accurate and detailed mapping of transmission risk. To identify which microenvironmental factors could be used as proxies for the occurrence of the lymnaeid snail Galba viator, a major intermediate host in South America, a total of 183 1-m2 quadrants across diverse water bodies in an endemic area in Andean Patagonia were manually timed-searched for snails and microenvironmental variables were registered. Data was analyzed using a Bayesian hierarchical occupancy model that assessed the effects of the microenvironmental variables on the presence of snails while considering imperfect snail detection. The model estimated that G. viator predominantly inhabits shallow aquatic environments, in the presence of grasses, where snails of the genus Biomphalaria are also detected, and with scarce tree canopy cover. Physical factors affecting occupancy presumably act as proxies for the average water temperature, while the temperature at the time of sampling was found to affect snail detectability. The identified variables are easy, fast, and inexpensive to measure, and can complement management decisions and risk maps based on coarser remote-sensing data, particularly relevant in a context of growing resistance to anthelminthic drugs.

Key source habitats and potential dispersal of triatoma infestans populations in Northwestern Argentina: implications for vector control.

BACKGROUND: Triatoma infestans -the principal vector of the infection that causes Chagas disease- defies elimination efforts in the Gran Chaco region. This study identifies the types of human-made or -used structures that are key sources of these bugs in the initial stages of house reinfestation after an insecticide spraying campaign. METHODOLOGY AND PRINCIPAL FINDINGS: We measured demographic and blood-feeding parameters at two geographic scales in 11 rural communities in Figueroa, northwest Argentina. Of 1,297 sites searched in spring, 279 (21.5%) were infested. Bug abundance per site and female fecundity differed significantly among habitat types (ecotopes) and were highly aggregated. Domiciles (human sleeping quarters) had maximum infestation prevalence (38.7%), human-feeding bugs and total egg production, with submaximal values for other demographic and blood-feeding attributes. Taken collectively peridomestic sites were three times more often infested than domiciles. Chicken coops had greater bug abundance, blood-feeding rates, engorgement status, and female fecundity than pig and goat corrals. The host-feeding patterns were spatially structured yet there was strong evidence of active dispersal of late-stage bugs between ecotopes. Two flight indices predicted that female fliers were more likely to originate from kitchens and domiciles, rejecting our initial hypothesis that goat and pig corrals would dominate. CONCLUSIONS AND SIGNIFICANCE: Chicken coops and domiciles were key source habitats fueling rapid house reinfestation. Focusing control efforts on ecotopes with human-fed bugs (domiciles, storerooms, goat corrals) would neither eliminate the substantial contributions to bug population growth from kitchens, chicken coops, and pig corrals nor stop dispersal of adult female bugs from kitchens. Rather, comprehensive control of the linked network of ecotopes is required to prevent feeding on humans, bug population growth, and bug dispersal simultaneously. Our study illustrates a demographic approach that may be applied to other regions and triatomine species for the design of innovative, improved vector control strategies.

Domestic animal hosts strongly influence human-feeding rates of the Chagas disease vector Triatoma infestans in Argentina.

BACKGROUND: The host species composition in a household and their relative availability affect the host-feeding choices of blood-sucking insects and parasite transmission risks. We investigated four hypotheses regarding factors that affect blood-feeding rates, proportion of human-fed bugs (human blood index), and daily human-feeding rates of Triatoma infestans, the main vector of Chagas disease. METHODS: A cross-sectional survey collected triatomines in human sleeping quarters (domiciles) of 49 of 270 rural houses in northwestern Argentina. We developed an improved way of estimating the human-feeding rate of domestic T. infestans populations. We fitted generalized linear mixed-effects models to a global model with six explanatory variables (chicken blood index, dog blood index, bug stage, numbers of human residents, bug abundance, and maximum temperature during the night preceding bug catch) and three response variables (daily blood-feeding rate, human blood index, and daily human-feeding rate). Coefficients were estimated via multimodel inference with model averaging. FINDINGS: Median blood-feeding intervals per late-stage bug were 4.1 days, with large variations among households. The main bloodmeal sources were humans (68%), chickens (22%), and dogs (9%). Blood-feeding rates decreased with increases in the chicken blood index. Both the human blood index and daily human-feeding rate decreased substantially with increasing proportions of chicken- or dog-fed bugs, or the presence of chickens indoors. Improved calculations estimated the mean daily human-feeding rate per late-stage bug at 0.231 (95% confidence interval, 0.157-0.305). CONCLUSIONS AND SIGNIFICANCE: Based on the changing availability of chickens in domiciles during spring-summer and the much larger infectivity of dogs compared with humans, we infer that the net effects of chickens in the presence of transmission-competent hosts may be more adequately described by zoopotentiation than by zooprophylaxis. Domestic animals in domiciles profoundly affect the host-feeding choices, human-vector contact rates and parasite transmission predicted by a model based on these estimates.

Heterogeneities in the ecoepidemiology of Trypanosoma cruzi infection in rural communities of the Argentinean Chaco.

We conducted a cross-sectional survey of Trypanosoma cruzi infection of Triatoma infestans as well as dogs and cats in 327 households from a well-defined rural area in northeastern Argentina to test whether the household distribution of infection differed between local ethnic groups (Tobas and Creoles) and identify risk factors for host infection. Overall prevalence of infection of bugs (27.2%; 95% confidence interval = 25.3-29.3%), dogs (26.0%; 95% confidence interval = 23.3-30.1%), and cats examined (28.7%; 95% confidence interval = 20.2-39.0%) was similar. A multimodel inference approach showed that infection in dogs was associated strongly with the intensity and duration of local exposure to infected bugs and moderately with household ethnic background. Overall, Toba households were at a substantially greater risk of infection than Creole households. The strong heterogeneities in the distribution of bug, dog, and cat infections at household, village, and ethnic group levels may be used for targeted vector and disease control.

Origins of house reinfestation with Triatoma infestans after insecticide spraying in the Argentine Chaco using wing geometric morphometry.

Identifying the origins of insect vectors collected after community-wide residual insecticide applications is a relevant challenge in the Gran Chaco region where the main vector of Chagas disease Triatoma infestans usually reinfests human dwellings. Wing geometric morphometry was used to compare the right wings of 63 males and 54 females collected at 4 months post-spraying (MPS) with those from 165 males and 111 females collected before full-coverage spraying with pyrethroids in a well-defined rural area in Northeastern Argentina. Male and female wing centroid size resulted significantly larger at 4MPS than before interventions, but no significant changes in shape were detected. Metric disparity (variance of shape) varied significantly in males but not in females. Using shape variables, a relatively large fraction of post-spraying males (70%) and females (54%) could not be differentiated from those collected at the same source house or at the nearest infested house before interventions. Bugs collected at 4 and 8MPS in a persistently infested house were mainly assigned to the source house. These results support the hypothesis of persistent bug populations that survived the insecticide application at local spatial scales, and are consistent with the occurrence of vector control failures most likely related to moderate pyrethroid resistance. Wing geometric morphometry is a useful tool for identifying sources of reinfestation, but it is limited by the spatial structure found in the reference populations. Combined with field and genetic data, this approach may contribute to the understanding of the reinfestation process and improvement of vector control strategies.

Intensified surveillance and insecticide-based control of the Chagas disease vector Triatoma infestans in the Argentinean Chaco.

BACKGROUND: The elimination of Triatoma infestans, the main Chagas disease vector in the Gran Chaco region, remains elusive. We implemented an intensified control strategy based on full-coverage pyrethroid spraying, followed by frequent vector surveillance and immediate selective insecticide treatment of detected foci in a well-defined rural area in northeastern Argentina with moderate pyrethroid resistance. We assessed long-term impacts, and identified factors and procedures affecting spray effectiveness. METHODS AND FINDINGS: After initial control interventions, timed-manual searches were performed by skilled personnel in 4,053 sites of 353-411 houses inspected every 4-7 months over a 35-month period. Residual insecticide spraying was less effective than expected throughout the three-year period, mainly because of the occurrence of moderate pyrethroid resistance and the limited effectiveness of selective treatment of infested sites only. After initial interventions, peridomestic infestation prevalence always exceeded domestic infestation, and timed-manual searches consistently outperformed householders' bug detection, except in domiciles. Most of the infestations occurred in houses infested at baseline, and were restricted to four main ecotopes. Houses with an early persistent infestation were spatially aggregated up to a distance of 2.5 km. An Akaike-based multi-model inference approach showed that new site-level infestations increased substantially with the local availability of appropriate refugia for triatomine bugs, and with proximity to the nearest site found infested at one or two preceding surveys. CONCLUSIONS AND SIGNIFICANCE: Current vector control procedures have limited effectiveness in the Gran Chaco. Selective insecticide sprays must include all sites within the infested house compound. The suppression of T. infestans in rural areas with moderate pyrethroid resistance requires increased efforts and appropriate management actions. In addition to careful, systematic insecticide applications, housing improvement and development policies that improve material conditions of rural villagers and reduce habitat suitability for bugs will contribute substantially to sustainable vector and disease control in the Gran Chaco.

Unexpected failures to control Chagas Disease vectors with pyrethroid spraying in northern Argentina.

Effectiveness of the elimination efforts against Triatoma infestans (Klug) in South America through residual application of pyrethroid insecticides has been highly variable in the Gran Chaco region. We investigated apparent vector control failures after a standard community-wide spraying with deltamethrin SC in a rural area of northeastern Argentina encompassing 353 houses. Insecticide spraying reduced house infestation less than expected: from 49.5% at baseline to 12.3 and 6.7% at 4 and 8 mo postspraying, respectively. Persistent infestations were detected in 28.4% of houses, and numerous colonies with late-stage bugs were recorded after the interventions. Laboratory bioassays showed reduced susceptibility to pyrethroids in the local bug populations. Eleven of 14 bug populations showed reduced mortality in diagnostic dose assays (range, 35 +/- 5% to 97 +/- 8%) whereas the remainder had 100% mortality. A fully enclosed residual bug population in a large chicken coop survived four pyrethroid sprays, including two double-dose applications, and was finally suppressed with malathion. The estimated resistance ratio of this bug population was 7.17 (range, 4.47-11.50). Our field data combined with laboratory bioassays and a residual foci experiment demonstrate that the initial failure to suppress T. infestans was mainly because of the unexpected occurrence of reduced susceptibility to deltamethrin in an area last treated with pyrethroid insecticides 12 yr earlier. Our results underline the need for close monitoring of the impact of insecticide spraying to provide early warning of possible problems because of enhanced resistance or tolerance and determine appropriate responses.

Factors affecting infestation by Triatoma infestans in a rural area of the humid Chaco in Argentina: a multi-model inference approach.

BACKGROUND: Transmission of Trypanosoma cruzi by Triatoma infestans remains a major public health problem in the Gran Chaco ecoregion, where understanding of the determinants of house infestation is limited. We conducted a cross-sectional study to model factors affecting bug presence and abundance at sites within house compounds in a well-defined rural area in the humid Argentine Chaco. METHODOLOGY/PRINCIPAL FINDINGS: Triatoma infestans bugs were found in 45.9% of 327 inhabited house compounds but only in 7.4% of the 2,584 sites inspected systematically on these compounds, even though the last insecticide spraying campaign was conducted 12 years before. Infested sites were significantly aggregated at distances of 0.8-2.5 km. The most frequently infested ecotopes were domiciles, kitchens, storerooms, chicken coops and nests; corrals were rarely infested. Domiciles with mud walls and roofs of thatch or corrugated tarred cardboard were more often infested (32.2%) than domiciles with brick-and-cement walls and corrugated metal-sheet roofs (15.1%). A multi-model inference approach using Akaike's information criterion was applied to assess the relative importance of each variable by running all possible (17,406) models resulting from all combinations of variables. Availability of refuges for bugs, construction with tarred cardboard, and host abundance (humans, dogs, cats, and poultry) per site were positively associated with infestation and abundance, whereas reported insecticide use showed a negative association. Ethnic background (Creole or Toba) adjusted for other factors showed little or no association. CONCLUSIONS/SIGNIFICANCE: Promotion and effective implementation of housing improvement (including key peridomestic structures) combined with appropriate insecticide use and host management practices are needed to eliminate infestations. Fewer refuges are likely to result in fewer residual foci after insecticide spraying, and will facilitate community-based vector surveillance. A more integrated perspective that considers simultaneously social, economic and biological processes at local and regional scales is needed to attain effective, sustainable vector and disease control.

Temporal dynamics of flight muscle development in Triatoma infestans (Hemiptera: Reduviidae).

Triatoma infestans Klug is dimorphic for flight muscles. This dimorphism may affect flight dispersal, reinfestation patterns, and transmission risk. To understand the contributions of genes and environment to morph determination, it is first necessary to characterize the temporal dynamics of flight muscle development. Field-collected T. infestans adults were dissected 20 or 100 d after collection, and those collected as nymphs were dissected at approximately 4, 15, or 44 d after the imaginal molt. The occurrence of flight muscles was additionally assessed by minimally invasive, repeated observations through the scutum of live bugs. Overall, 33.5% of 179 males and 7.8% of 179 females had no flight muscles. Neither dissections nor repeated observations evidenced changes in morph type during adult life, suggesting that the occurrence of flight muscles is mostly irreversible within the time span of observations and is determined before or during final ecdysis. Flight muscles were detectable at 4 d after emergence and achieved complete development within 4-15 d after emergence. The repeated observation of thoracic contents through the scutum showed very high sensitivity and specificity and apparently had minor effects on mortality. In another bug population located 360 km away, 16.4% of 177 males and 6.7% of 149 females had no flight muscles. Current results show that the sex-biased flight muscle dimorphism is a regionally widespread character in T. infestans. This character should be considered in field population studies that seek to measure reinfestation risk and dispersal in T. infestans and other Triatominae.

Variability in the encoding of spatial information by dancing bees.

A honeybee's waggle dance is an intriguing example of multisensory convergence, central processing and symbolic information transfer. It conveys to bees and human observers the position of a relatively small area at the endpoint of an average vector in a two-dimensional system of coordinates. This vector is often computed from a collection of waggle phases from the same or different dancers. The question remains, however, of how informative a small sample of waggle phases can be to the bees, and how the spatial information encoded in the dance is actually mapped to the followers' searches in the field. Certainly, it is the variability of a dancer's performance that initially defines the level of uncertainty that followers must cope with if they were to successfully decode information in the dance. Understanding how a dancer's behaviour is mapped to that of its followers initially relies on the analysis of both the accuracy and precision with which the dancer encodes spatial information in the dance. Here we describe within-individual variations in the encoding of the distance to and direction of a goal. We show that variations in the number of a dancer's wagging movements, a measure that correlates well with the distance to the goal, do not depend upon the dancer's travelled distance, meaning that there is a constant variance of wagging movements around the mean. We also show that the duration of the waggle phases and the angular dispersion and divergence of successive waggle phases co-vary with a dancer's orientation in space. Finally, using data from dances recorded through high-speed video techniques, we present the first analysis of the accuracy and precision with which an increasing number of waggle phases conveys spatial information to a human observer.

Flight muscle dimorphism and heterogeneity in flight initiation of field-collected Triatoma infestans (Hemiptera: Reduviidae).

Recent experiments demonstrated that most field-collected Triatoma infestans (Klug) (Hemiptera: Reduviidae) adults from northern Argentina either never initiated flight or did so repeatedly in both sexes. This pattern could not be explained by sex, adult age, weight, weight-to-length ratio (W/L), or chance. We examined whether bugs that never initiated flight possessed developed flight muscles, and whether flight muscle mass relative to total body mass (FMR) was related to the probability of flight initiation. Approximately half of the adults that never initiated flight had no flight muscles. The absence of flight muscles was 2.4 times more frequent in males than females. Females had significantly larger flight muscle mass than males. For both sexes, the frequency of bugs with no flight muscles was spatially heterogeneous among individual collection sites. A logistic regression model of flight initiation that included both FMR and W/L provided abetter fit than models including either one of these predictors. FMR is a novel predictor of flight initiation in Triatominae, with a stronger effect than W/L. The higher frequency of females initiating flight in our experiments may be explained by females having flight muscles more frequently than males, and having FMR and W/L values more suitable for flying. These findings demonstrate that individuals and natural populations of T. infestans can differ dramatically with regard to flight initiation.

Comparative trial of effectiveness of pyrethroid insecticides against peridomestic populations of Triatoma infestans in northwestern Argentina.

The effects of different pyrethroid insecticides, formulations, and doses on peridomestic populations of Triatoma infestans (Klug) were evaluated in 128 houses with 148 identified infested peridomestic sites in northwestern Argentina between October 2003 and March 2005. Four treatments were randomly assigned within each community: two doses of 5% suspension concentrate beta-cypermethrin in water applied with manual compression sprayers, the standard dose (S) at 50 mg and a double dose (2S) at 100 mg active ingredient (AI)/m2; and two emulsifiable concentrates diluted in diesel fuel and applied with power sprayers, 25% cypermethrin (100 mg [AI] /m2) (CF) and 10% permethrin (170 mg [AI]/m2) (DF). Infestation was assessed by timed manual collections with a dislodging agent at baseline, 5, 12, and 17 mo postspraying, and the sites found to be reinfested at 5 mo postspraying were selectively resprayed. Only 2S eliminated T. infestans from all peridomestic sites up to 12 mo postspraying, and it was significantly more effective than all other treatments. At 5 mo postspraying, more sites treated with CF or DF rather than S had bug colonies that probably represented residual foci, which they also failed in eliminating after a second spray. At 17 mo postspraying, the prevalence of reinfested peridomestic sites was 5% for 2S, 29% for S, 43% for CF, and 54% for DF. The application of suspension concentrate pyrethroids in dose twice as large as that currently in use in the attack phase produces a greater initial impact and may eliminate peridomestic populations of T. infestans.

Flight initiation of Triatoma infestans (Hemiptera: Reduviidae) under natural climatic conditions.

Flight dispersal of Triatoma infestans Klug is probably the most important mechanism for house reinfestation at a village scale after residual spraying with insecticides. The aim of the current study was to estimate the flight initiation probability of field-collected T. infestans and to assess how this probability was affected by sex, adult age, partial bloodmeal, and the presence of a host inaccessible for feeding. Four experimental series, each consisting of three to six consecutive nights and repeated measurements of flight initiation on each individually marked bug, were carried out in experimental huts inside closed cages under natural climatic conditions. We demonstrate that flight initiation probability of T. infestans is much higher than previously reported, responds to temperature in a sigmoid manner, and is higher in females than males, and that the frequency distribution of the number of flights per individual is highly aggregated in female and male bugs. The age of adults had strong effects on flight initiation, whereas the presence of an inaccessible host and a partial bloodmeal exerted no significant effects in models controlling for the effects of bug weight-to-length ratio. The high flight potential found is consistent with the rapid changes in reinfestation patterns observed in the field. The present estimates of flight probabilities and the identification of factors modifying them provide essential knowledge for modeling reinfestation patterns and for improving control strategies of T.