Effect of habitat fragmentation on rural house invasion by sylvatic triatomines: A multiple landscape-scale approach

After the decrease of the relative importance of Triatoma infestans, a number of studies reported the occurrence of sylvatic triatomines dispersing actively to domestic environments in the dry western Chaco Region of Argentina. Anthropic modification of the landscape is mentioned as one of the main causes of the increase in domicile invasion. The aim of this study was to describe the occurrence and frequency of sylvatic triatomines invading rural houses, and to evaluate the effect of habitat fragmentation and other ecological factors on the invasion of rural houses in central Argentina. We hypothesized that the decrease in food sources and the loss of wild ecotopes, as a consequence of habitat fragmentation, increase the chances of invasion by triatomines. The entomological data was collected by community-based vector surveillance during fieldwork carried out between 2017–2020, over 131 houses located in fourteen rural communities in the northwest of Córdoba Province (central Argentina). We used generalized linear models to evaluate the effect of (i) the environmental anthropic disturbance in the study area, (ii) the composition and configuration of the landscape surrounding the house, (iii) the spatial arrangement of houses, (iv) and the availability of artificial refuges and domestic animals in the peridomicile, on house invasion by triatomines. We report the occurrence of seven species of triatomines invading rural houses in the study area -T. infestans, T. guasayana, T. garciabesi, T. platensis, T. delpontei, T. breyeri and P. guentheri-. Study data suggest that invasion by triatomines occurs with higher frequency in disturbed landscapes, with houses spatially isolated and in proximity to subdivided fragments of forest. The availability of domestic refuges in the peridomestic structures as well as the presence of a higher number of domestic animals increase the chances of invasion by triatomines.     

New scenarios of Trypanosoma cruzi transmission in the Orinoco region of Colombia

Rhodnius prolixus, a blood-sucking triatomine with domiciliary anthropophilic habits, is the main vector of Chagas disease. The current paradigm of Trypanosoma cruzi transmission in Columbia includes a sylvatic and domiciliary cycle co-existing with domestic and sylvatic populations of reservoirs. The aim of this study is to evaluate the population densities and relative abundance of triatomines and mammals that may be involved in the sylvatic cycle of Chagas disease to clarify the epidemiological scenario in an endemic area in the province of Casanare. Insect vectors on Attalea butyracea palms were captured using both manual searches and bait traps. The capture of mammals was performed using Sherman and Tomahawk traps. We report an infestation index of 88.5% in 148 palms and an index of T. cruzi natural infection of 60.2% in 269 dissected insects and 11.9% in 160 captured mammals. High population densities of triatomines were observed in the sylvatic environment and there was a high relative abundance of reservoirs in the area, suggesting a stable enzootic cycle. We found no evidence of insect domiciliation. Taken together, these observations suggest that eco-epidemiological factors shape the transmission dynamics of T. cruzi, creating diverse scenarios of disease transmission.     

Differentiation and genetic analysis of Rhodnius prolixus and Rhodnius colombiensis by rDNA and RAPD amplification.

Domiciliated Rhodnius prolixus and sylvatic R. colombiensis were analyzed in order to confirm their genetic divergence and verify the risk that the latter represents in the domiciliation process, and to provide tools for identifying the sources of possible reinfestation by triatomines in human dwellings allowing control programs to be undertaken. Comparison of random amplified polymorphic DNA amplification patterns and cluster analysis suggests reproductive discontinuity between the two species. The calculated statistical F value of 0.24 and effective migration rate of 0.6 individuals per generation are insufficient to maintain genetic homogeneity between them and confirm the absence of present genetic flow. R. colombiensis presents higher intrapopulation variability. Polymerase chain reaction of ribosomal DNA supports these findings. The low genetic flow between the two species implies that R. colombiensis do not represent an epidemiological risk for the domiciliary transmission of Trypanosoma cruzi in the Tolima Department. The lower variability of the domiciliated R. prolixus could result in greater susceptibility to the use of pesticides in control programs.     

Dynamics of Sylvatic Chagas Disease Vectors in Coastal Ecuador Is Driven by Changes in Land Cover

Background

Chagas disease is a serious public health problem in Latin America where about ten million individuals show Trypanosoma cruzi infection. Despite significant success in controlling domiciliated triatomines, sylvatic populations frequently infest houses after insecticide treatment which hampers long term control prospects in vast geographical areas where vectorial transmission is endemic. As a key issue, the spatio-temporal dynamics of sylvatic populations is likely influenced by landscape yet evidence showing this effect is rare. The aim of this work is to examine the role of land cover changes in sylvatic triatomine ecology, based on an exhaustive field survey of pathogens, vectors, hosts, and microhabitat characteristics'' dynamics.

Methodology and Principal Findings

The study was performed in agricultural landscapes of coastal Ecuador as a study model. Over one year, a spatially-randomized sampling design (490 collection points) allowed quantifying triatomine densities in natural, cultivated and domestic habitats. We also assessed infection of the bugs with trypanosomes, documented their microhabitats and potential hosts, and recorded changes in landscape characteristics. In total we collected 886 individuals, mainly represented by nymphal stages of one triatomine species Rhodnius ecuadoriensis. As main results, we found that 1) sylvatic triatomines had very high T. cruzi infection rates (71%) and 2) densities of T. cruzi-infected sylvatic triatomines varied predictably over time due to changes in land cover and occurrence of associated rodent hosts.

Conclusion

We propose a framework for identifying the factors affecting the yearly distribution of sylvatic T. cruzi vectors. Beyond providing key basic information for the control of human habitat colonization by sylvatic vector populations, our framework highlights the importance of both environmental and sociological factors in shaping the spatio-temporal population dynamics of triatomines. A better understanding of the dynamics of such socio-ecological systems is a crucial, yet poorly considered, issue for the long-term control of Chagas disease.     

Frequent House Invasion of Trypanosoma cruzi-Infected Triatomines in a Suburban Area of Brazil

Background

The demographic transition of populations from rural areas to large urban centers often results in a disordered occupation of forest remnants and increased economic pressure to develop high-income buildings in these areas. Ecological and socioeconomic factors associated with these urban transitions create conditions for the potential transmission of infectious diseases, which was demonstrated for Chagas disease.

Methodology/Principal Findings

We analyzed 930 triatomines, mainly Triatoma tibiamaculata, collected in artificial and sylvatic environments (forests near houses) of a suburban area of the city of Salvador, Bahia State, Brazil between 2007 and 2011. Most triatomines were captured at peridomiciles. Adult bugs predominated in all studied environments, and nymphs were scarce inside houses. Molecular analyses of a randomly selected sub-sample (n=212) of triatomines showed Trypanosoma cruzi infection rates of 65%, 50% and 56% in intradomestic, peridomestic and sylvatic environments, respectively. We detected the T. cruzi lineages I and II and mixed infections. We also showed that T. tibiamaculata fed on blood from birds (50%), marsupials (38%), ruminants (7%) and rodents (5%). The probability of T. cruzi infection was higher in triatomines that fed on marsupial blood (odds ratio (OR) = 1.95, 95% confidence interval (CI) = 1.22-3.11). Moreover, we observed a protective effect against infection in bugs that fed on bird blood (OR = 0.43, 95% CI = 0.30-0.73).

Conclusions/Significance

The frequent invasion of houses by infected triatomines indicates a potential risk of T. cruzi transmission to inhabitants in this area. Our results reinforce that continuous epidemiological surveillance should be performed in areas where domestic transmission is controlled but enzootic transmission persists.     

Sex, subdivision, and domestic dispersal of Trypanosoma cruzi lineage I in southern Ecuador

Background

Molecular epidemiology at the community level has an important guiding role in zoonotic disease control programmes where genetic markers are suitably variable to unravel the dynamics of local transmission. We evaluated the molecular diversity of Trypanosoma cruzi, the etiological agent of Chagas disease, in southern Ecuador (Loja Province). This kinetoplastid parasite has traditionally been a paradigm for clonal population structure in pathogenic organisms. However, the presence of naturally occurring hybrids, mitochondrial introgression, and evidence of genetic exchange in the laboratory question this dogma.

Methodology/Principal Findings

Eighty-one parasite isolates from domiciliary, peridomiciliary, and sylvatic triatomines and mammals were genotyped across 10 variable microsatellite loci. Two discrete parasite populations were defined: one predominantly composed of isolates from domestic and peridomestic foci, and another predominantly composed of isolates from sylvatic foci. Spatial genetic variation was absent from the former, suggesting rapid parasite dispersal across our study area. Furthermore, linkage equilibrium between loci, Hardy-Weinberg allele frequencies at individual loci, and a lack of repeated genotypes are indicative of frequent genetic exchange among individuals in the domestic/peridomestic population.

Conclusions/Significance

These data represent novel population-level evidence of an extant capacity for sex among natural cycles of T. cruzi transmission. As such they have dramatic implications for our understanding of the fundamental genetics of this parasite. Our data also elucidate local disease transmission, whereby passive anthropogenic domestic mammal and triatomine dispersal across our study area is likely to account for the rapid domestic/peridomestic spread of the parasite. Finally we discuss how this, and the observed subdivision between sympatric sylvatic and domestic/peridomestic foci, can inform efforts at Chagas disease control in Ecuador.     

Invasion of rural houses by wild Triatominae in the arid Chaco

Triatomines are the vectors of Trypanosoma cruzi, the etiologic agent of Chagas disease, the main endemic disease affecting five to seven million people in Latin America. Besides Triatoma infestans, the most important T. cruzi vector in the Gran Chaco region, other triatomine species associated with sylvatic birds and mammals are responsible for the maintenance of the wild cycle of T. cruzi. The present study aimed at evaluating the house invasion by sylvatic triatomine species in rural communities of the Los Llanos region (La Rioja, Argentina) and its association with environmental variables. House invasion by flying adult triatomines was recorded by trained collectors that surveyed over 377 houses distributed over 73 localities in a 56,600 km² study region, between October, 2014 and February, 2015. The result of the study showed the frequent house invasion by adult triatomines: 26.3% houses were infested in 53% of the localities. Seven sylvatic triatomine species were collected, with T. guasayana and T. garciabesi among the most abundant. House invasion by triatomine species showed no spatial aggregation and was not associated with temperature, precipitation, or vegetation cover at the spatial scale considered in the present study. House invasion by the epidemiologically important T. infestans is a concern of rural communities. Besides constituting a latent, although low, risk, the presence of these species negatively interferes with the vigilance activities of the provincial Chagas disease program.     

Intrusive versus domiciliated triatomines and the challenge of adapting vector control practices against Chagas disease

Chagas disease prevention remains mostly based on triatomine vector control to reduce or eliminate house infestation with these bugs. The level of adaptation of triatomines to human housing is a key part of vector competence and needs to be precisely evaluated to allow for the design of effective vector control strategies. In this review, we examine how the domiciliation/intrusion level of different triatomine species/populations has been defined and measured and discuss how these concepts may be improved for a better understanding of their ecology and evolution, as well as for the design of more effective control strategies against a large variety of triatomine species. We suggest that a major limitation of current criteria for classifying triatomines into sylvatic, intrusive, domiciliary and domestic species is that these are essentially qualitative and do not rely on quantitative variables measuring population sustainability and fitness in their different habitats. However, such assessments may be derived from further analysis and modelling of field data. Such approaches can shed new light on the domiciliation process of triatomines and may represent a key tool for decision-making and the design of vector control interventions.     

Peridomiciliary colonies of Triatoma vitticeps (Stal, 1859) (Hemiptera, Reduviidae, Triatominae) infected with Trypanosoma cruzi in rural areas of the state of Espírito Santo, Brazil

In Brazil, the colonization of human dwellings by triatomines occurs in areas with native vegetation of the caatinga or cerrado types. In areas of Atlantic forest such as in the Brazilian state of Espírito Santo, there are no species adapted to live in human habitations. The few autochthonous cases of Chagas disease encountered in Espírito Santo have been attributed to adult specimens of Triatoma vitticeps that invade houses from forest remnants. In recent years, the entomology unit of the Espírito Santo State Health Secretariat has recorded nymphs infected with flagellates similar to Trypanosoma cruzi in rural localities. Entomological surveys were carried out in the residences and outbuildings in which the insects were found, and serological examinations for Chagas disease performed on the inhabitants. Four colonies were found, all associated with nests of opossums (Didelphis aurita), 111 specimens of T. vitticeps, and 159 eggs being collected. All the triatomines presented flagellates in their frass. Mice inoculated with the faeces presented trypomastigotes in the circulating blood and groups of amastigotes in the cardiac muscle fibres. Serological tests performed on the inhabitants were negative for T. cruzi. Even with the intense devastation of the forest in Espírito Santo, there are no indications of change in the sylvatic habits of T. vitticeps. Colonies of this insect associated with opossum nests would indicate an expansion of the sylvatic environment into the peridomicile.     

Population dynamics of Triatoma vitticeps (Stål, 1859) in Itanhomi, Minas Gerais, Brazil

Taxonomic markers (head structure morphometry, isoenzymes and randon amplified polymorphism of DNA - RAPD) were used to understand the population dynamics of Triatoma vitticeps, predominant triatomine species in Itanhomi district, using samples obtained from domestic, peridomiciliary and sylvatic habitats. Morphometric analysis revealed sexual dimorphism within the three samples although specimens could not be separated according to the habitat in which they were captured. Forty-two bands were analyzed from RAPD profiles generated using four primers. A dendrogram constructed from Dice's similarity coefficient values showed that migration of the insects between the habitats has occurred, without structuring of populations. Moreover, the dendrogram obtained from the genetic distance values showed an important gene flow between the sylvatic and domestic habitats. No polymorphism was found in the electrophoretic mobility of proteins for the ten enzymes studied. Our results revealed movement of triatomines between the three habitats, suggesting that the presence of T. vitticeps in houses should not be ignored. As invasion of houses by sylvatic insects is frequent and the natural infection indices of this species are among the highest known, epidemiological vigilance studies may reveal possible changes in T. vitticeps behaviour which could present future risks to public health.     

Gypsy moth response to landscape structure differs from neutral model predictions: implications for invasion monitoring

Simulations of dispersal across computer-generated neutral landscapes have generated testable predictions about the relationship between dispersal success and landscape structure. Models predict a threshold response in dispersal success with increasing habitat fragmentation. A threshold is defined as an abrupt, disproportionate decline in dispersal success at a certain proportion of habitat in the landscape. To identify potential empirical threshold responses in invasion success to landscape structure, we quantified the relationship between progression of the gypsy moth (Lymantria dispar) invasion wavefront across Michigan (1985–1996) and the structure of the Michigan landscape using two indices of invasion success and six landscape metrics. We also examined the effect of scale of analysis and choice of land cover characterization on our results by repeating our analysis at three scales using two different land cover maps. Contrary to simulation model predictions, thresholds in invasion success did not correspond closely with thresholds in landscape structure metrics. Increased variation in invasion success indices at smaller scales of analysis also suggested that invasion success should be studied at larger spatial extents (≥75 km²) than would be appropriate for characterizing individual dispersal events. The predictions of individual dispersal models across neutral landscapes may have limited applications for the monitoring and management of vagile species with excellent dispersal capabilities such as the gypsy moth.     

Updated geographical distribution and ecoepidemiology of the triatomine fauna (Reduviidae: Triatominae) in Colombia

Information concerning triatomine records from provinces and municipalities was accumulated-including data indicating natural infections with trypanosomatides-that has been previously published or reported by Colombian provincial health services and research institutes. Altitude appeared to be the main factor responsible for the distribution of the insects. Illustrations summarize the information provided by the above records. A triatomine fauna classification is presented that corresponds to the eco-epidemiological conditions of the country, considering altitude as the factor determining the geographical distribution of these vectors. Rhodnius prolixus, Triatoma dimidiata, Triatoma maculata and Triatoma venosa are considered the major transmission risk species in Colombia, according to the frequency in which they are reported inside dwellings and peridomiciliary areas. Entomological surveillance providess a necessary tool to reinforce the control strategies for Chagas disease. This also allows the evaluation of transmission risk that the sylvatic triatomines represent in Colombia.     

Predicting Microstegium vimineum invasion in natural plant communities of the southern Blue Ridge Mountains, USA

Shade-tolerant non-native invasive plant species may make deep incursions into natural plant communities, but detecting such species is challenging because occurrences are often sparse. We developed Bayesian models of the distribution of Microstegium vimineum in natural plant communities of the southern Blue Ridge Mountains, USA to address three objectives: (1) to assess local and landscape factors that influence the probability of presence of M. vimineum; (2) to quantify the spatial covariance error structure in occurrence that was not accounted for by the environmental variables; and (3) to synthesize our results with previous findings to make inference on the spatial attributes of the invasion process. Natural plant communities surrounded by areas with high human activity and low forest cover were at highest risk of M. vimineum invasion. The probability of M. vimineum presence also increased with increasing native species richness and soil pH, and decreasing basal area of ericaceous shrubs. After accounting for environmental covariates, evaluation of the spatial covariance error structure revealed that M. vimineum is invading the landscape by a hierarchical process. Infrequent long-distance dispersal events result in new nascent sub-populations that then spread via intermediate- and short-distance dispersal, resulting in 3-km spatial aggregation pattern of sub-populations. Containment or minimisation of its impact on native plant communities will be contingent on understanding how M. vimineum can be prevented from colonizing new suitable habitats. The hierarchical invasion process proposed here provides a framework to organise and focus research and management efforts.     

Geometric morphometric differences between Panstrongylus geniculatus from field and laboratory

The finding of Panstrongylus geniculatus nymphs inside a house in northeastern Antioquia, Colombia, and the reports related to their increasing presence in homes suggest the need for surveillance methods for monitoring the invasion processes. We analyzed the morphological differences between a wild population and its laboratory descendants, using the techniques of geometric morphometry, with the idea that such differences might parallel those between sylvatic and synanthropic populations. The analyses over five generations showed differences in size but not in shape. Head size and wing size were both reduced from sylvatic to laboratory populations, but the decrease in head size occurred only up to the second generation while the decrease in wing size proceeded up to the fifth generation. In contrast, although a decrease in sexual size dimorphism has been proposed as a marker of colonization in human dwellings, we did not detect any significant loss of dimorphism between sexes of P. geniculatus over the five generations studied. We conclude that size changes may have a physiological origin in response to a change of ecotopes, but more than five generations may be required for the expression of permanent morphological markers of human dwellings colonization.     

Dispersal polymorphism and the speed of biological invasions

The speed at which biological range expansions occur has important consequences for the conservation management of species experiencing climate change and for invasion by exotic organisms. Rates of dispersal and population growth are known to affect the speed of invasion, but little is known about the effect of having a community of dispersal phenotypes on the rate of range expansion. We use reaction-diffusion equations to model the invasion of a species with two dispersal phenotypes into a previously unoccupied landscape. These phenotypes differ in both their dispersal rate and population growth rate. We find that the presence of both phenotypes can result in faster range expansions than if only a single phenotype were present in the landscape. For biologically realistic parameters, the invasion can occur up to twice as fast as a result of this polymorphism. This has implications for predicting the speed of biological invasions, suggesting that speeds cannot just be predicted from looking at a single phenotype and that the full community of phenotypes needs to be taken into consideration.     

Isoenzyme profiles of Trypanosoma cruzi stocks from different areas of Paraguay

Twenty one Trypanosoma cruzi stocks from humans, domiciliary triatomines and one sylvatic animal of different areas of Paraguay were subjected to isoenzyme analysis. Thirteen enzyme systems (15 loci in total) were studied. MN cl2 (clonets 39) and SO34 cl4 (clonets 20) were used as references. Relationships between stocks were depicted by an UPGMA dendrogram constructed using the Jaccard's distances matrix. Among the Paraguayan stocks 14 zymodemes were identified (Par1 to Par14), Par 5 being the most frequent. Polymorphism rate and clonal diversity were 0.73 and 0.93, respectively. Average number of alleles per polymorphic locus was 2.5 (range 2-4). These measurements show a high diversity, which is confirmed by the dendrogram topology. All stocks belong to the same lineage, as MN cl2 reference strain (T. cruzi II). Moreover three distinct subgroups were identified and two of them correspond to Brazilian and Bolivian zymodemes, respectively. The third subgroup, the most common in Paraguay, is related to Tulahuen stock. The large geographical distribution of some zymodemes agrees with the hypothesis of clonality for T. cruzi populations. However sample size was not adequate to detect genetic recombination in any single locality.     

Ecological Connectivity of Trypanosoma cruzi Reservoirs and Triatoma pallidipennis Hosts in an Anthropogenic Landscape with Endemic Chagas Disease

Traditional methods for Chagas disease prevention are targeted at domestic vector reduction, as well as control of transfusion and maternal-fetal transmission. Population connectivity of Trypanosoma cruzi-infected vectors and hosts, among sylvatic, ecotone and domestic habitats could jeopardize targeted efforts to reduce human exposure. This connectivity was evaluated in a Mexican community with reports of high vector infestation, human infection, and Chagas disease, surrounded by agricultural and natural areas. We surveyed bats, rodents, and triatomines in dry and rainy seasons in three adjacent habitats (domestic, ecotone, sylvatic), and measured T. cruzi prevalence, and host feeding sources of triatomines. Of 12 bat and 7 rodent species, no bat tested positive for T. cruzi, but all rodent species tested positive in at least one season or habitat. Highest T. cruzi infection prevalence was found in the rodents, Baiomys musculus and Neotoma mexicana. In general, parasite prevalence was not related to habitat or season, although the sylvatic habitat had higher infection prevalence than by chance, during the dry season. Wild and domestic mammals were identified as bloodmeals of T. pallidipennis, with 9% of individuals having mixed human (4.8% single human) and other mammal species in bloodmeals, especially in the dry season; these vectors tested >50% positive for T. cruzi. Overall, ecological connectivity is broad across this matrix, based on high rodent community similarity, vector and T. cruzi presence. Cost-effective T. cruzi, vector control strategies and Chagas disease transmission prevention will need to consider continuous potential for parasite movement over the entire landscape. This study provides clear evidence that these strategies will need to include reservoir/host species in at least ecotones, in addition to domestic habitats.     

What shapes giant hogweed invasion? Answers from a spatio-temporal model integrating multiscale monitoring data

In this study we simulated the invasion of Heracleum mantegazzianum with a spatiotemporal model that combined a life-cycle matrix model with mechanistic local and corridor dispersal and a stochastic long-distance dispersal in a cellular automaton. The model was applied to the habitat configuration and invader distribution of eight 1?km2 study areas. Comparing the simulations with monitoring data collected over 7?years (2002?C2009) yielded a modelling efficiency of 0.94. We tested the significance of different mechanisms of invasion by omitting or modifying single model components one at a time. Thus we found that the extent of H. mantegazzianum invasion at landscape level depends on both landscape-scale processes and local processes which control recruitment success and population density. Limiting recruitment success (100????30?%) and successionally decreasing the carrying capacity of habitats (max????0) over 30?years significantly improved the projections of the invasion at the landscape level. Local dispersal reached farther than 10?m, i.e. farther than previously assumed, but appeared to be unaffected by wind directions. Long-distance dispersal together with local dispersal dominated the invasion quantitatively. Dispersal through corridors accounted for less invasive spread. Its importance, with respect to invasion speed (number of colonised model grid cells) is probably limited over short periods of time (7?years). Only dispersal along rivers made a significant quantitative contribution to invasion of H. mantegazzianum. We suggest that biotic heterogeneity of suitable habitats is responsible for varying invasion success and that successionally increasing competition leads to declining population densities of H. mantegazzianum over several decades slowing down the spread on the landscape scale.     

基于景观格局与过程的云南省典型地区道路网络生态效应

利用概率连接度指数的量化分析方法,分析了云南省典型地区道路网络对景观格局、生态过程以及景观功能的影响.结果表明：研究区道路网络加剧了区域景观的破碎化程度;道路网络对不同生态过程的迁移路径结构、数目以及分布的影响有所不同,影响程度随迁移扩散能力的增加而增加;道路网络总体上降低了景观维持生态过程连续性的功能（不同情景平均下降超过10%）,使各个斑块在景观中的功能退化（平均下降超过40%）,影响程度随迁移扩散能力的增加而增加.