Invasion speeds of Triatoma dimidiata, vector of Chagas disease: An application of orthogonal polynomials method.

Demographic processes and spatial dispersal of Triatoma dimidiata, a triatomine species vector of Chagas disease, are modeled by integrodifference equations to estimate invasion capacity of this species under different ecological conditions. The application of the theory of orthogonal polynomials and the steepest descent method applied to these equations, allow a good approximation of the abundance of the adult female population and the invasion speed. We show that: (1) under the same mean conditions of demography and dispersal, periodic spatial dispersal results in an invasion speed 2.5 times larger than the invasion speed when spatial dispersal is continuous; (2) when the invasion speed of periodic spatial dispersal is correlated to adverse demographic conditions, it is 34.7% higher as compared to a periodic dispersal that is correlated to good demographic conditions. From our results we conclude, in terms of triatomine population control, that the invasive success of T. dimidiata may be most sensitive to the probability of transition from juvenile to adult stage. We discuss our main theoretical predictions in the light of observed data in different triatomines species found in the literature.

Global Climate Change Effects on Venezuela's Vulnerability to Chagas Disease is Linked to the Geographic Distribution of Five Triatomine Species.

We analyzed the possible effects of global climate change on the potential geographic distribution in Venezuela of five species of triatomines (Eratyrus mucronatus (Stal, 1859), Panstrongylus geniculatus (Latreille, 1811), Rhodnius prolixus (Stål, 1859), Rhodnius robustus (Larrousse, 1927), and Triatoma maculata (Erichson, 1848)), vectors of Trypanosoma cruzi, the etiological agent of Chagas disease. To obtain the future potential geographic distributions, expressed as climatic niche suitability, we modeled the presences of these species using two IPCC (Intergovernmental Panel on Climate Change) future emission scenarios of global climate change (A1B and B1), the Global Climate model CSIRO Mark 3.0, and three periods of future projections (years 2020, 2060, and 2080). After estimating with the MaxEnt software the future climatic niche suitability for each species, scenario, and period of future projections, we estimated a series of indexes of Venezuela's vulnerability at the county, state, and country level, measured as the number of people exposed due to the changes in the geographical distribution of the five triatomine species analyzed. Despite that this is not a measure of the risk of Chagas disease transmission, we conclude that possible future effects of global climate change on the Venezuelan population vulnerability show a slightly decreasing trend, even taking into account future population growth; we can expect fewer locations in Venezuela where an average Venezuelan citizen would be exposed to triatomines in the next 50-70 yr.

Life History Traits and Demographic Parameters of Triatoma infestans (Hemiptera: Reduviidae) Fed on Human Blood.

Triatoma infestans (Klug, 1834) (Hemiptera: Reduviidae), the main vector of Chagas disease in South America, feeds primarily on humans, but ethical reasons preclude carrying out demographical studies using people. Thus, most laboratory studies of T. infestans are conducted using bird or mammal live hosts that may result in different demographic parameters from those obtained on human blood. Therefore, it is of interest to determine whether the use of an artificial feeder with human blood would be operational to rear triatomines and estimate population growth rates. We estimated life history traits and demographic parameters using an artificial feeder with human blood and compared them with those obtained on live hens. Both groups of T. infestans were kept under constant conditions [28 ± 1°C, 40 ± 5% relative humidity, a photoperiod of 12:12 (L:D) h] and fed weekly. On the basis of age-specific survival and age-specific fecundity, we calculated the intrinsic rate of natural increase (r), the finite rate of population growth (λ), the net reproductive rate (Ro), and the mean generation time (Tg). Our results show differences in life history traits between blood sources, resulting in smaller population growth rates on human blood than on live hens. Although demographic growth rate was smaller on human blood than on hens, it still remains positive, so the benefit/cost ratio of this feeding method seems relatively attractive. We discuss possibility of using the artificial feeder with human blood for both ecological and behavioral studies.

American triatomine species occurrences: updates and novelties in the DataTri database.

The causative agent of Chagas disease (Trypanosoma cruzi) is transmitted to mammals, including humans, mainly by insect vectors of the subfamily Triatominae (Hemiptera: Reduviidae). Also known as "kissing bugs", the subfamily currently includes 157 validated species (154 extant and three extinct), in 18 genera and five tribes. Here, we present a subdataset (7852 records) of American triatomine occurrences; an update to the most complete and integrated database available to date at a continental scale. New georeferenced records were obtained from a systematic review of published literature and colleague-provided data. New data correspond to 101 species and 14 genera from 22 American countries between 1935 and 2022. The most important novelties refer to (i) the inclusion of new species, (ii) synonymies and formal transferals of species, and (iii) temporal and geographical species records updates. These data will be a useful contribution to entomological surveillance implicated in Chagas disease.

Publishing data to support the fight against human vector-borne diseases.

Vector-borne diseases are responsible for more than 17% of human cases of infectious diseases. In most situations, effective control of debilitating and deadly vector-bone diseases (VBDs), such as malaria, dengue, chikungunya, yellow fever, Zika and Chagas requires up-to-date, robust and comprehensive information on the presence, diversity, ecology, bionomics and geographic spread of the organisms that carry and transmit the infectious agents. Huge gaps exist in the information related to these vectors, creating an essential need for campaigns to mobilise and share data. The publication of data papers is an effective tool for overcoming this challenge. These peer-reviewed articles provide scholarly credit for researchers whose vital work of assembling and publishing well-described, properly-formatted datasets often fails to receive appropriate recognition. To address this, GigaScience's sister journal GigaByte partnered with the Global Biodiversity Information Facility (GBIF) to publish a series of data papers, with support from the Special Programme for Research and Training in Tropical Diseases (TDR), hosted by the World Health Organisation (WHO). Here we outline the initial results of this targeted approach to sharing data and describe its importance for controlling VBDs and improving public health.

Machine-learning model led design to experimentally test species thermal limits: The case of kissing bugs (Triatominae).

Species Distribution Modelling (SDM) determines habitat suitability of a species across geographic areas using macro-climatic variables; however, micro-habitats can buffer or exacerbate the influence of macro-climatic variables, requiring links between physiology and species persistence. Experimental approaches linking species physiology to micro-climate are complex, time consuming and expensive. E.g., what combination of exposure time and temperature is important for a species thermal tolerance is difficult to judge a priori. We tackled this problem using an active learning approach that utilized machine learning methods to guide thermal tolerance experimental design for three kissing-bug species: Triatoma infestans, Rhodnius prolixus, and Panstrongylus megistus (Hemiptera: Reduviidae: Triatominae), vectors of the parasite causing Chagas disease. As with other pathogen vectors, triatomines are well known to utilize micro-habitats and the associated shift in microclimate to enhance survival. Using a limited literature-collected dataset, our approach showed that temperature followed by exposure time were the strongest predictors of mortality; species played a minor role, and life stage was the least important. Further, we identified complex but biologically plausible nonlinear interactions between temperature and exposure time in shaping mortality, together setting the potential thermal limits of triatomines. The results from this data led to the design of new experiments with laboratory results that produced novel insights of the effects of temperature and exposure for the triatomines. These results, in turn, can be used to better model micro-climatic envelope for the species. Here we demonstrate the power of an active learning approach to explore experimental space to design laboratory studies testing species thermal limits. Our analytical pipeline can be easily adapted to other systems and we provide code to allow practitioners to perform similar analyses. Not only does our approach have the potential to save time and money: it can also increase our understanding of the links between species physiology and climate, a topic of increasing ecological importance.

Demographic and dispersal constraints for domestic infestation by non-domicilated chagas disease vectors in the Yucatan Peninsula, Mexico.

Chagas disease is one of the most important diseases in Latin America. Insecticides have been sprayed to control domiciliated vectors. However, some triatomine species are not strictly domiciliated, and the transmission risk posed by immigrants is identified as a major challenge. The design of new control strategies requires disentangling the importance of demography and immigration in vector occurrence inside houses. Using a population dynamics model, we confirmed that dispersal can explain satisfactorily the domestic abundance of Triatoma dimidiata in Yucatan, Mexico. A surprisingly low fecundity was also required (no more than one to two female offspring per female per trimester). A wide range of survival probabilities was possible, although the best fit was obtained for a very low immature survival (< or = 0.01/trimester). Our model predicted that domestic populations are not sustainable, and up to 90% of the individuals found in houses are immigrants. We discuss the potential of different strategies to control the transmission of Chagas disease by non-domiciliated vectors.

DataTri, a database of American triatomine species occurrence.

Trypanosoma cruzi, the causative agent of Chagas disease, is transmitted to mammals - including humans - by insect vectors of the subfamily Triatominae. We present the results of a compilation of triatomine occurrence and complementary ecological data that represents the most complete, integrated and updated database (DataTri) available on triatomine species at a continental scale. This database was assembled by collecting the records of triatomine species published from 1904 to 2017, spanning all American countries with triatomine presence. A total of 21815 georeferenced records were obtained from published literature, personal fieldwork and data provided by colleagues. The data compiled includes 24 American countries, 14 genera and 135 species. From a taxonomic perspective, 67.33% of the records correspond to the genus Triatoma, 20.81% to Panstrongylus, 9.01% to Rhodnius and the remaining 2.85% are distributed among the other 11 triatomine genera. We encourage using DataTri information in various areas, especially to improve knowledge of the geographical distribution of triatomine species and its variations in time.

A two-sex matrix population model to represent harem structure.

Population dynamic models often include males in the calculation of population change, but even in those cases males have rarely been introduced to represent polygyny (harem social structure), where it is particularly important to include males in the reproductive performance of the population. In this article we develop an adaptable matrix population modeling framework for species that have a harem-like social structure under an assumption that the transitions from newborn to juvenile and juvenile to adult both take one time step. We are able to calculate not only the growth rates and stable stage distributions, but also the mathematical expressions for harem size for this model. We then provide applications of this model to two mammal species with slightly different harem behavior.

The impact of climate change on the geographical distribution of two vectors of Chagas disease: implications for the force of infection.

Chagas disease, caused by the parasite Trypanosoma cruzi, is the most important vector-borne disease in Latin America. The vectors are insects belonging to the Triatominae (Hemiptera, Reduviidae), and are widely distributed in the Americas. Here, we assess the implications of climatic projections for 2050 on the geographical footprint of two of the main Chagas disease vectors: Rhodnius prolixus (tropical species) and Triatoma infestans (temperate species). We estimated the epidemiological implications of current to future transitions in the climatic niche in terms of changes in the force of infection (FOI) on the rural population of two countries: Venezuela (tropical) and Argentina (temperate). The climatic projections for 2050 showed heterogeneous impact on the climatic niches of both vector species, with a decreasing trend of suitability of areas that are currently at high-to-moderate transmission risk. Consequently, climatic projections affected differently the FOI for Chagas disease in Venezuela and Argentina. Despite the heterogeneous results, our main conclusions point out a decreasing trend in the number of new cases of Tr. cruzi human infections per year between current and future conditions using a climatic niche approach.

Biological Control of the Chagas Disease Vector Triatoma infestans with the Entomopathogenic Fungus Beauveria bassiana Combined with an Aggregation Cue: Field, Laboratory and Mathematical Modeling Assessment.

BACKGROUND: Current Chagas disease vector control strategies, based on chemical insecticide spraying, are growingly threatened by the emergence of pyrethroid-resistant Triatoma infestans populations in the Gran Chaco region of South America. METHODOLOGY AND FINDINGS: We have already shown that the entomopathogenic fungus Beauveria bassiana has the ability to breach the insect cuticle and is effective both against pyrethroid-susceptible and pyrethroid-resistant T. infestans, in laboratory as well as field assays. It is also known that T. infestans cuticle lipids play a major role as contact aggregation pheromones. We estimated the effectiveness of pheromone-based infection boxes containing B. bassiana spores to kill indoor bugs, and its effect on the vector population dynamics. Laboratory assays were performed to estimate the effect of fungal infection on female reproductive parameters. The effect of insect exuviae as an aggregation signal in the performance of the infection boxes was estimated both in the laboratory and in the field. We developed a stage-specific matrix model of T. infestans to describe the fungal infection effects on insect population dynamics, and to analyze the performance of the biopesticide device in vector biological control. CONCLUSIONS: The pheromone-containing infective box is a promising new tool against indoor populations of this Chagas disease vector, with the number of boxes per house being the main driver of the reduction of the total domestic bug population. This ecologically safe approach is the first proven alternative to chemical insecticides in the control of T. infestans. The advantageous reduction in vector population by delayed-action fungal biopesticides in a contained environment is here shown supported by mathematical modeling.

Seroprevalence of Triatoma virus (Dicistroviridae: Cripaviridae) antibodies in Chagas disease patients.

BACKGROUND: Chagas disease is caused by Trypanosoma cruzi, and humans acquire the parasite by exposure to contaminated feces from hematophagous insect vectors known as triatomines. Triatoma virus (TrV) is the sole viral pathogen of triatomines, and is transmitted among insects through the fecal-oral route and, as it happens with T. cruzi, the infected insects release the virus when defecating during or after blood uptake. METHODS: In this work, we analysed the occurrence of anti-TrV antibodies in human sera from Chagas disease endemic and non-endemic countries, and developed a mathematical model to estimate the transmission probability of TrV from insects to man, which ranged between 0.00053 and 0.0015. RESULTS: Our results confirm that people with Chagas disease living in Bolivia, Argentina and Mexico have been exposed to TrV, and that TrV is unable to replicate in human hosts. CONCLUSIONS: We presented the first experimental evidence of antibodies against TrV structural proteins in human sera.

Parameters of Leishmania braziliensis transmission by indoor Lutzomyia ovallesi in Venezuela.

We developed a mathematical model of cutaneous leishmaniasis (CL) transmission predicting CL incidence based on field data of number of positive sand flies, new CL cases, and number of susceptible people. We estimated the following parameters: a CL incubation period of one month, the overall susceptibility (Phi = 0.793), the serologic force of infection (lambda(m) = 0.108 /person/year, SD = 0.014), the clinical force of infection (lambda(l)= 0.114/year), the proportion of infections that result in skin lesions (alpha = 1.056), and the instantaneous reversal rate of Montenegro skin test-positive (MST(+)) people to MST(-) (rho= 0.124/year, SD = 0.021). We also provide the first field estimate of the transmission efficiency (epsilon = 0.0045, SD = 0.0009). The model predictions conform well with the observed new cases except for some small departures in the peaks and in some depressions (D(max) = 0.1494, P < 0.2). We discuss possible sources of error of our estimate of epsilon, and compare our parameter estimates with those obtained in Peru.

Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruzi in the Yucatan peninsula of Mexico.

Chagas disease represents a major public health concern in most of Latin America, and its control is currently based on vector control and blood bank screening. We investigated the geographic distribution and seasonal variations in triatomine populations in the Yucatan peninsula of Mexico to obtain entomologic data for the optimization of potential control programs. We collected domiciliated and peri-domiciliated Triatoma dimidiata from 115 houses in 23 villages distributed throughout most of the peninsula. A high abundance of bugs was observed in the northern part of the peninsula, indicating a prioritary area for vector control. Part of this distribution could be attributed to the type of vegetation. We also documented strong seasonal variations in T. dimidiata populations, with a higher abundance during the hot and dry season in April-June. These variations, associated with reduced year-round colonization of houses and the analysis of developmental stage structure, suggest that flying adults seasonally invading houses may play a larger role than domiciliated bugs in transmission of Trypanosoma cruzi to humans. The importance of this transmission dynamics may not be limited to the Yucatan peninsula, but may be a general mechanism contributing to natural transmission that should be taken into account in other regions for the design and optimization of control strategies.

Mortality profiles of Rhodnius prolixus (Heteroptera: Reduviidae), vector of Chagas disease.

Life table data of Rhodnius prolixus (Heteroptera: Reduviidae) kept at laboratory conditions were analysed in search for mortality patterns. Gompertz and Weibull mortality models seem adequate to explain the sigmoid shape of the survivorship curve. A significant fit was obtained with both models for females (R(2) = 0.70, P < 0.0005 for the Gompertz model; R(2) = 0.78, P < 0.0005 for the Weibull model) and for males (R(2) = 0.39, P < 0.0005 for the Gompertz model; R(2) = 0.48, P < 0.0005 for the Weibull model). The mortality parameter (b) is higher for females in Gompertz and Weibull models, using smoothed and non-smoothed data (P < 0.05), revealing a significant sex mortality differential. Given the particular life history of this insect, the non-linear relationship between the force of mortality and age may have an important impact in the vectorial capacity of R. prolixus as Chagas disease vector, and its consideration should be included as an important factor in the transmission of Trypanosoma cruzi by triatomines.

Bayesian inference on the effect of density dependence and weather on a guanaco population from Chile.

Understanding the mechanisms that drive population dynamics is fundamental for management of wild populations. The guanaco (Lama guanicoe) is one of two wild camelid species in South America. We evaluated the effects of density dependence and weather variables on population regulation based on a time series of 36 years of population sampling of guanacos in Tierra del Fuego, Chile. The population density varied between 2.7 and 30.7 guanaco/km2, with an apparent monotonic growth during the first 25 years; however, in the last 10 years the population has shown large fluctuations, suggesting that it might have reached its carrying capacity. We used a Bayesian state-space framework and model selection to determine the effect of density and environmental variables on guanaco population dynamics. Our results show that the population is under density dependent regulation and that it is currently fluctuating around an average carrying capacity of 45,000 guanacos. We also found a significant positive effect of previous winter temperature while sheep density has a strong negative effect on the guanaco population growth. We conclude that there are significant density dependent processes and that climate as well as competition with domestic species have important effects determining the population size of guanacos, with important implications for management and conservation.

Density but not climate affects the population growth rate of guanacos ( Lama guanicoe) (Artiodactyla, Camelidae).

We analyzed the effects of population density and climatic variables on the rate of population growth in the guanaco ( Lama guanicoe), a wild camelid species in South America. We used a time series of 36 years (1977-2012) of population sampling in Tierra del Fuego, Chile. Individuals were grouped in three age-classes: newborns, juveniles, and adults; for each year a female population transition matrix was constructed, and the population growth rate (λ) was estimated for each year as the matrix highest positive eigenvalue. We applied a regression analysis with finite population growth rate (λ) as dependent variable, and total guanaco population, sheep population, annual mean precipitation, and winter mean temperature as independent variables, with and without time lags. The effect of guanaco population size was statistically significant, but the effects of the sheep population and the climatic variables on guanaco population growth rate were not statistically significant.

Influence of vectors' risk-spreading strategies and environmental stochasticity on the epidemiology and evolution of vector-borne diseases: the example of Chagas' disease.

Insects are known to display strategies that spread the risk of encountering unfavorable conditions, thereby decreasing the extinction probability of genetic lineages in unpredictable environments. To what extent these strategies influence the epidemiology and evolution of vector-borne diseases in stochastic environments is largely unknown. In triatomines, the vectors of the parasite Trypanosoma cruzi, the etiological agent of Chagas' disease, juvenile development time varies between individuals and such variation most likely decreases the extinction risk of vector populations in stochastic environments. We developed a simplified multi-stage vector-borne SI epidemiological model to investigate how vector risk-spreading strategies and environmental stochasticity influence the prevalence and evolution of a parasite. This model is based on available knowledge on triatomine biodemography, but its conceptual outcomes apply, to a certain extent, to other vector-borne diseases. Model comparisons between deterministic and stochastic settings led to the conclusion that environmental stochasticity, vector risk-spreading strategies (in particular an increase in the length and variability of development time) and their interaction have drastic consequences on vector population dynamics, disease prevalence, and the relative short-term evolution of parasite virulence. Our work shows that stochastic environments and associated risk-spreading strategies can increase the prevalence of vector-borne diseases and favor the invasion of more virulent parasite strains on relatively short evolutionary timescales. This study raises new questions and challenges in a context of increasingly unpredictable environmental variations as a result of global climate change and human interventions such as habitat destruction or vector control.

Adaptive developmental delay in Chagas disease vectors: an evolutionary ecology approach.

BACKGROUND: The developmental time of vector insects is important in population dynamics, evolutionary biology, epidemiology and in their responses to global climatic change. In the triatomines (Triatominae, Reduviidae), vectors of Chagas disease, evolutionary ecology concepts, which may allow for a better understanding of their biology, have not been applied. Despite delay in the molting in some individuals observed in triatomines, no effort was made to explain this variability. METHODOLOGY: We applied four methods: (1) an e-mail survey sent to 30 researchers with experience in triatomines, (2) a statistical description of the developmental time of eleven triatomine species, (3) a relationship between development time pattern and climatic inter-annual variability, (4) a mathematical optimization model of evolution of developmental delay (diapause). PRINCIPAL FINDINGS: 85.6% of responses informed on prolonged developmental times in 5(th) instar nymphs, with 20 species identified with remarkable developmental delays. The developmental time analysis showed some degree of bi-modal pattern of the development time of the 5(th) instars in nine out of eleven species but no trend between development time pattern and climatic inter-annual variability was observed. Our optimization model predicts that the developmental delays could be due to an adaptive risk-spreading diapause strategy, only if survival throughout the diapause period and the probability of random occurrence of "bad" environmental conditions are sufficiently high. CONCLUSIONS/SIGNIFICANCE: Developmental delay may not be a simple non-adaptive phenotypic plasticity in development time, and could be a form of adaptive diapause associated to a physiological mechanism related to the postponement of the initiation of reproduction, as an adaptation to environmental stochasticity through a spreading of risk (bet-hedging) strategy. We identify a series of parameters that can be measured in the field and laboratory to test this hypothesis. The importance of these findings is discussed in terms of global climatic change and epidemiological consequences.

Re-infestation of houses by Triatoma dimidiata after intra-domicile insecticide application in the Yucatán peninsula, Mexico.

In most countries, Chagas disease transmission control remains based on domestic insecticide application. We thus evaluated the efficacy of intra-domicile cyfluthrin spraying for the control of Triatoma dimidiata, the only Chagas disease vector in the Yucatán peninsula, Mexico, and monitored potential re-infestation every 15 days for up to 9 months. We found that there was a re-infestation of houses by adult bugs starting 4 months after insecticide application, possibly from sylvatic/peridomicile areas. This points out the need to take into account the potential dispersal of sylvatic/peridomestic adult bugs into the domiciles as well as continuity action for an effective vector control.