Competition between vectors of Chagas disease, Triatoma infestans and T. sordida: effects on fecundity and mortality

Abstract. Interspecific competition between two species of triatomine bugs (Hemiptera: Reduviidae), vectors of Chagas disease, was assessed for 16 months through comparative fecundity and mortality of experimental populations in chicken nests, maintained indoors with ambient conditions. Triatoma sordida (Stål), the secondary vector in north‐eastern Argentina, was compared with Triatoma infestans (Klug) the more widespread domestic vector in the southern cone of South America. Both species populations originated from females collected in 1995 from the community of Empedrado, Corrientes, Argentina. Three population units were monitored: T. infestans alone, T. sordida alone and both species together in equal proportions. Each population started with six male and six female adults, 116 eggs, and nymphal instars I to V numbering 82, 48, 16, 11 and 19, respectively. Numbers and weight of individual bugs were recorded monthly (August 1995 to December 1996). The pure populations of T. infestans and T. sordida showed temporal changes in abundance, rising in summer and falling in winter, similar to the typical trends under normal field conditions. In the mixed population, however, T. sordida fell to extinction after 6 months, whereas T. infestans reached similar abundance to the pure (control) population. For each nymphal instar of T. sordida, the mean body weight was significantly less and mortality rate was higher in the mixed population compared to the pure population, but there were no significant differences of adult longevity or fecundity between the pure and mixed populations of T. sordida. The apparent competitive displacement of T. sordida by T. infestans was attributed to the latter species having better ability to obtain bloodmeals. This might explain the rarity of mixed populations where these two species occur in sympatry.     

Peridomestic distribution of Triatoma garciabesi and Triatoma guasayana in north-west Argentina

The Reduviid bugs Triatoma garciabesi Carcavallo et al. (Hemiptera: Reduviidae: Triatominae), previously known as T. sordida Ståhl in the semi‐arid chaco region, and T. guasayana Wygodzinsky & Abalos, vectors of Trypanosoma cruzi Chagas (Kinetoplastida: Trypanosomatidae), were found to occupy wide but different ranges of ecotopes in the peridomestic environment. At Amamá and nearby rural villages in north‐western Argentina, a combined total of 1233 specimens were collected from 325/2314 (14%) sites surveyed at 6‐monthly intervals from November 1994 to November 1996. Triatoma garciabesi and T. guasayana displayed a significantly different distribution among peridomestic ecotopes. Triatoma garciabesi predominated over T. guasayana in the prevalence of infested sites, the number of colonies and the number of bugs collected. For T. garciabesi, the predominant ecotopes most likely to yield T. garciabesi repeatedly were the rugged bark of Prosopis alba or P. nigra (Fabaceae) trees, where chickens roosted, and chicken coops. For T. guasayana the main ecotopes were goat or sheep corrals, piled materials and orchard fences. Triatoma garciabesi and T. guasayana were collected concurrently from the same site on 9/2314 (0.4%) occasions, and on different dates at the same site on 12 (0.5%) occasions. The observed low frequency of mixed populations (< 1%) was not significantly different from that expected from a hypothesis of independence. Triatoma garciabesi clearly outnumbered T. guasayana in four of the nine mixed populations, none of which persisted as such. Neither T. garciabesi nor T. guasayana colonized human habitations, even in the absence of T. infestans (formerly the predominant domestic vector of T. cruzi in this area), a situation that apparently has not changed in the last 50 years in northern Argentina.     

Risk factors associated with house infestation by the Chagas disease vector Triatoma pallidipennis in Cuernavaca metropolitan area, Mexico

Abstract. Chagas disease caused by infection with Trypanosoma cruzi Chagas (Kinetoplastida: Trypanosomatidae) is widespread in Mexico, transmitted by various triatomine bugs (Hemiptera: Reduviidae). The only domestic vector in Cuernavaca (population 650 000) is Triatoma pallidipennis (Ståhl) with T. cruzi seroprevalence ranging from 1% to 9% in the resident human population. We surveyed possible risk factors for T. pallidipennis infestation at Cuernavaca (altitude 1200–2200 m) on south-western slopes of the Sierra Madre Occidental. This metropolitan area (with five administrative counties) has rapid urbanization, forested environs and proliferation of ‘weekend housing’ for visitors from Mexico City, 60 km to the north. To assess factors associated with T. pallidipennis infestation, we first stratified Cuernavaca by altitude and by socio-economic status of population catchment units (PCUs). Within each PCU, one to three blocks were chosen for cluster sampling (three houses/block) and information about Chagas disease was distributed. After obtaining signed consent from householders, representative houses were routinely and opportunistically inspected for T. pallidipennis and surveyed for demographic, economic, physical and other potential risk factors. Of the 1129 houses assessed, T. pallidipennis was found in 4.1% (range 3.0–6.8% per county) and the T. cruzi infection rate was ∼50% in bugs. Rates of house infestation in poor PCUs were double those in higher socio-economic strata (odds ratio 2.12, confidence interval 1.03–4.3), with >4-fold greater crowding index of T. pallidipennis. The bug density index was inversely correlated with PCU altitude and socio-economic category (altitude of homes being associated with prosperity), while the bug colonization index (presence of nymphs indicating breeding) did not vary significantly across the PCU categories, but did vary according to altitude. Multivariate regression analysis showed that the most significant risk factors associated with T. pallidipennis infestation were lower altitude (linked with lower socio-economic status), garden area >80 m², dogs at liberty to enter the house, occurrence of squirrels and opossums around the house, presence of pigs in the surrounding area and having at least one of the adjacent lots empty (unconstructed). Householders who had received information about Chagas disease comprised 33% from infested houses (14/42) but only 15% from non-infested houses (148/984). Hence, the awareness of Chagas disease was significantly associated with having a bug-free house (P < 0.01). When shown specimens of T. pallidipennis, the proportions of householders who recognized them were 78% from infested houses but only 29% of those with uninfested houses. Given the low infestation rates and the high capacity of the population to act appropriately once they have received information regarding this disease and its vector, relevant health education is expected to have a significant impact on triatomine control in this metropolitan area.     

Prevalence and distribution of parasites and pathogens of Triatominae from Argentina, with emphasis on Triatoma infestans and Triatoma virus TrV

Chagas’ disease is the most important endemic arthropod-zoonosis in Argentina with an estimated 1.6 million people infected with the causative agent Trypanosoma cruzi. Triatoma infestans is the main vector of Chagas’ disease in Argentina. A survey for parasites and pathogens of Triatominae was conducted from August 2002 to February 2005. Collections of insects were made in domiciles, peridomiciles, and in the natural habitats of the Triatominae. Insects from these collections were dissected and their organs and tissues examined for flagellates. Frass from these insects was collected and examined for detection of the entomopathogenic virus Triatoma virus (TrV) using AC-ELISA and PCR. Triatominae belonging to four species, T. infestans (n = 1646), Triatoma guasayana (n = 4), Triatoma platensis (n = 1) and Triatoma sordida (n = 5) were collected from 62 sites located in 13 provinces of Argentina. Triatoma virus and two protozoan species, Blastocrithidia triatomae and T. cruzi, the etiological agent of Chagas disease, were found infecting Triatominae. The total prevalence of TrV in 1646 T. infestans analyzed by ELISA was 9.66% (159/1646) from 7 to 13 provinces where collections were made. Triatoma virus positive triatomines were found in 17 of 62 populations when examined by AC-ELISA but in 38 of 62 populations when PCR was used for detection. The prevalence of B. triatomae in T. infestans was 0.43% (7/1646), while the prevalence of T. cruzi was 1.3% (21/1646). This is the first study on the diversity, distribution and prevalence of flagellated protozoa and TrV of Triatominae in endemic Chagas’ disease regions of Argentina.     

Infestation of arboreal nests of coatis by triatomine species,vectors of Trypanosoma cruzi,in a large Neotropical wetland

The coati (Nasua nasua, Carnivora) is a medium‐sized mammal common in the Pantanal of Brazil. Unlike most mammals, coatis construct arboreal nests used for resting and reproduction. In this region, the coati is an important host of Trypanosoma cruzi, the causative agent of Chagas disease. There are two possible routes through coatis can be infected by T. cruzi: the oral route or the vectorial route. However, the relative importance of each of these routes in the infection of coatis and its role in the sylvatic cycle of the parasite are unknown. Our objectives were to investigate: (i) whether coati nests were infested by triatomine bugs, (ii) what species were frequent in the nests, (iii) whether the triatomines in nests were infected by T. cruzi, and (iv) what were the food resources of these triatomines. Eight of the 24 nests sampled were infested with triatomines, a total of 37 specimens of at least two species (Rhodnius stali and Triatoma sordida). In one nest, R. stali and T. sordida co‐occurred and both fed on multiple resources, including coatis. This is the first report of triatomines occurring in arboreal nests of coatis. The co‐occurrence of two different genera of triatomine vectors and coatis within the limited space of the coati nests provide multiple opportunities for the exchange of the protozoan parasite through both the vectorial and oral transmission routes.     

Insecticide resistance in Brazilian Triatoma infestans and Venezuelan Rhodnius prolixus

Resistance levels to insecticides used in control of Chagas Disease vectors were assessed in two species of bugs (Hemiptera: Reduviidae): Triatoma infestans (Klug) from Brazil and Rhodnius prolixus Stål from Venezuela. The resistance ratios, compared to susceptible laboratory strains, were determined by topical application bioassays. The T. infestans PA strain exhibited resistance ratios of 7× to deltamethrin, 3.6× to β‐cyfluthrin and 3.3× to cypermethrin, but was susceptible to β‐cypermethrin and lambda‐cyhalothrin. Rhodnius prolixus CA strain showed resistance to all the pyrethroids evaluated, the resistance ratios ranging between 4.5× to lambda‐cyhalothrin and 12.4× to cypermethrin. Deltamethrin resistance in both strains was decreased by piperonyl butoxide, suggesting oxidative metabolism as cause of resistance.     

Laboratory and field studies for the control of Chagas disease vectors using the fungus Metarhizium anisopliae

Chagas disease is one of the most important insect-vectored diseases in Brazil. The entomopathogenic fungus Metarhizium anisopliae was evaluated against nymphs and adults of Panstrongylus megistus, Triatoma infestans, and T. sordida. Pathogenicity tests at saturated humidity demonstrated high susceptibility to fungal infection. The shortest estimates of 50% lethal time (LT₅₀) for P. megistus varied from 4.6 (isolate E9) to 4.8 days (genetically modified strain 157p). For T. infestans, the shortest LT₅₀ was 6.3 (E9) and 7.3 days (157p). For T. sordida, the shortest LT₅₀ was 8.0 days (157p). The lethal concentration sufficient to kill 50% of T. infestans (LC₅₀) was 1.9 × 10⁷ conidia/ml for strain 157p. In three chicken coops that were sprayed with M. anisopliae, nymphs especially were well controlled, with a great population reduction of 38.5% after 17 days. Therefore M. anisopliae performed well, controlling Triatominae in both laboratory and field studies.     

Effect of ectoparasitic <Emphasis Type="Italic">Pimeliaphilus plumifer</Emphasis> mites (Acari: Pterygosomatidae) on <Emphasis Type="Italic">Meccus pallidipennis</Emphasis> (Hemiptera: Reduviidae) and several other Chagas’ disease vectors under laboratory conditions

Several biological parameters were evaluated to determine the capacity of Pimeliaphilus plumifer as biological control agent of Triatominae bugs. When P. plumifer and bugs of a variety of triatomine species were forced together in cages in the laboratory, the incidence of mite infestation was the following: Meccus pallidipennis > M. bassolsae > Triatoma rubida > M. longipennis > M. picturatus, and practically no mites were found on T. infestans and Rhodnius prolixus. Adults and hexapod larvae of P. plumifer were the only stages found to parasitize on M. pallidipennis. Fourth and fifth instar nymphs of this bug appeared most susceptible to mite infestation. P. plumifer mites located preferably on the coxae, ventral abdomen and pronotum of M. pallidipennis bugs. The number of blood meals, amount of ingested blood, and resistance to starvation of M. pallidipennis were similar in both the control and the mite infested groups. On the other hand, mite infection reduced molting rate in nymphs and longevity in adults, increased mortality in third-fifth instar nymphs, and fewer viable eggs were laid by females infected with P. plumifer. These effects could be related with nutritional deficiencies. Our results support the use of P. plumifer mites as control agents of host Triatominae species.     

Influence of blood meal source on the biological parameters of Triatoma pallidipennis (Heteroptera: Reduviidae) from Mexico

Chagas disease is one of the most important vector-borne diseases in Latin America, including Mexico. Triatoma pallidipennis (Stål) (Hemiptera: Reduviidae) is a Mexican triatomine vector commonly associated with different hosts. The influence of six blood meals (rabbits, rats, mice, dogs, cats and chickens) on six biological parameters of the biology of T. pallidipennis was evaluated. A significant difference was found in the period of egg-to-adult development between the five mammalian feeds (mean 195 days) and the chicken feed (221 days). The probability of survival was significantly lower in the chicken cohort (0.285). The total number of blood meals to moult from the first instar to the adult stage was the highest in the chicken cohort (10–15). This cohort had the significantly highest rate of females at the end cycle. The mean number of eggs laid per female and the egg eclosion rate were similar among the six food sources. Most results seemed to be influenced by the higher nutritional quality of the mammalian blood compared to the bird's blood and the increased energy expenditure required for the digestion of bird blood. These results clearly show that T. pallidipennis, unlike other triatomine species, has a high reproductive capacity when feeding on different hosts.     

Scanning Electron Microscopic Studies of Blastocrithidia triatomae (Trypanosomatidae) in the Rectum of Triatoma infestans (Reduviidae)12

ABSTRACT. The morphology of Blastocrithidia triatomae, when colonizing the rectum of Triatoma infestans, was studied by scanning electron microscopy. The posterior end of the epimastigote's body is tapered and often rolled up. The “straphangers” (cyst stages) are connected with the flagellum by “cytoplasmic bridges”; after “straphanger” detachment these bridges persist as remnants. A comparison of colonization densities of B. triatomae and Trypanosoma cruzi shows that both prefer to colonize the rectal gland, but minor density differences are apparent for B. triatomae in other rectal regions. The colonization density in established infections of B. triatomae is always greater than that of T. cruzi, especially near the midgut exit.     

Cannibalism and Coprophagy Are Modes of Transmission of Blastocrithidia triatomae (Trypanosomatidae) between Triatomines

Transovarial transmission was not detectable among Blastocrithidia triatomae- infected Triatoma infestans . Rather, B. triatomae was transmitted directiy between triatomines by cannibalism and coprophagy. Cannibalism conditions that excluded coprophagy always resulted in an infection of Dipetalogaster maxima . The efficiency of transmission was not influenced by the blood source—mice or chickens—fed to the infected donor bugs although chicken blood lyses the epimastigotes of the stomach population. Triatoma infestans was infected by coprophagy only if fed, not if unfed. Blastocrithidia triatomae in dry feces was taken up only if the feces were redissolved in fresh feces. Infections also appeared in groups of bugs fed on chickens previously used for feeding infected bugs.     

Enhancing fitness in offspring of crosses between two triatomine species

Chagas disease is one of the main vector‐borne diseases in Latin America, including Mexico. Understanding the biological parameters of the triatomine species is a crucial first step in estimating the epidemiologic importance of each group. The aim of this study was to compare the biological fitness of Meccus pallidipennis (Stål), M. bassolsae (Alejandre, Nogueda, Cortez, Jurberg, Galvão, Carcavallo) (Hemiptera: Reduviidae: Triatominae) and their laboratory hybrids, by estimating six biological parameters in order to increase the knowledge of the potential role of triatomine hybrids in the transmission of Trypanosoma cruzi to reservoir hosts. Biological parameters related to lifespan, number of blood meals to molt, mortality for each instar, percentage of females at the end of the cycle, number of eggs laid, and hatching of eggs in four cohorts of 100 specimens of M. pallidipennis, M. bassolsae, and their laboratory hybrids were evaluated and compared. In four of the six studied parameters (accumulative mortality, the percentage of females, mean number of laid eggs, and egg hatching), the hybrid cohorts had better fitness results than the parental cohorts. The increase in hybrid fitness found in our study could lead to an increase in the epidemiologic risks caused by transmission of T. cruzi to humans.     

The cuticular hydrocarbons of the Triatoma sordida species subcomplex (Hemiptera: Reduviidae)

The cuticular hydrocarbons of the Triatoma sordida subcomplex (Hemiptera: Reduviidae: Triatominae) were ana-lysed by gas chromatography and their structures identified by mass spectrometry. They comprised mostly n-alkanes and methyl-branched alkanes with one-four methyl substitutions. n-alkanes consisted of a homologous series from C21-C33 and represented 33-45% of the hydrocarbon fraction; n-C29 was the major component. Methyl-branched alkanes showed alkyl chains from C24-C43. High molecular weight dimethyl and trimethylalkanes (from C35-C39) represented most of the methyl-branched fraction. A few tetramethylalkanes were also detected, comprising mostly even-numbered chains. Several components such as odd-numbered 3-methylalkanes, dimethylalkanes and trimethylalkanes of C37 and C39 showed patterns of variation that allowed the differentiation of the species and populations studied. Triatoma guasayana and Triatoma patagonica showed the most distinct hydrocarbon patterns within the subcomplex. The T. sordida populations from Brazil and Argentina showed significantly different hydrocarbon profiles that posed concerns regarding the homogeneity of the species. Triatoma garciabesi had a more complex hydrocarbon pattern, but it shared some similarity with T. sordida. The quantitative and qualitative variations in the cuticular hydrocarbons may help to elucidate the relationships between species and populations of this insect group.     

Trypanosomatidae Isolated from Zelus leucogrammus (Perty, 1834) (Hemiptera,Reduviidae), with a Discussion on Flagellates of Insectivorous Bugs*

The insectivorous bug Zelus leucogrammus (Perty, 1834) (Hemiptera, Reduviidae) was found to harbor several species of trypanosomatids of the genera Leptomonas, Crithidia, Herpetomonas and Blastocrithidia. However, laboratory bred nymphs given sterile food were infected only by Blastocrithidia, the other flagellates appearing in their intestinal tract when they were fed on other insects. The Blastocrithidia was thought to belong to a single species and to be a parasite proper of Z. leucogrammus (and possibly other Hemiptera), producing luxuriant infections in the intestinal tract of the bugs captured in nature and spreading easily among isolated populations through cannibalism and ingestion of cysts; it was also abundant in the genital tract of gravid females but transovarian transmission was not proved. This Blastocrithidia experimentally infected Triatoma infestans and is very close to B. triatomae Cerisola, del Prado, Rohwedder and Bozzini, 1971. The other trypanosomatids, never numerous in naturally infected Z. leucogrammus, are acquired by the bug from many different insects, chiefly Diptera, on which it was seen to feed. Herpetomonas muscarum and C. luciliae, the common trypanosomatids among several muscoid Diptera, were isolated both from flies and from the bugs fed on them.     

Triatominae in furnariid nests of the Argentine Gran Chaco

Triatomines (Hemiptera, Reduviidae) are bloodsucking insects involved in the transmission of Trypanosoma cruzi, the causative agent of Chagas disease, an important public health problem in Latin America. The triatomine species found in sylvatic habitats generally play a limited epidemiological role compared to domestic species, but they may act as a reinfestation source of dwellings after insecticide spraying and have to be carefully considered in control strategies of Chagas disease transmission. The objectives of this work were to carry out a survey of the sylvatic triatomine species colonizing Furnariidae nests in a typical area of the Chaco region of Argentina during the winter and to study the parasites and natural enemies associated with the collected triatomines. Sixty‐three triatomine specimens were collected from Furnariidae nests (Coryphistera alaudina and Phacellodomus sibilatrix) randomly selected within the study area. Fifty‐four were identified as Psammolestes coreodes, seven as Triatoma platensis, and two as Triatoma infestans. Specimens of T. infestans and T. platensis were found in one nest. The first finding of instar nymphs of T. infestans x T. platensis in a sylvatic habitat is reported. For the first time, sylvatic collected specimens of T. platensis were found infected by T. cruzi. Triatoma virus was found in one Ps. coreodes specimen.     

The peri-urban interface and house infestation with Triatoma infestans in the Argentine Chaco: an underreported process?

Peri-urban infestations with triatomine bugs, their sources and their dynamics have rarely been investigated. Here, we corroborated the reported occurrence of Triatoma infestans in a peri-urban area and in neighbouring rural houses in Pampa del Indio, in the Argentine Chaco, and identified its putative sources using spatial analysis and demographic questionnaires. Peri-urban householders reported that 10% of their premises had triatomines, whereas T. infestans was collected by timed manual searches or community-based surveillance in only nine (3%) houses. Trypanosoma cruzi-infected T. infestans and Triatoma sordida were collected indoors only in peri-urban houses and were infected with TcV and TcI, respectively. The triatomines fed on chickens, cats and humans. Peri-urban infestations were most frequent in a squatter settlement and particularly within the recently built mud houses of rural immigrants, with large-sized households, more dogs and cats and more crowding. Several of the observed infestations were most likely associated with passive bug transport from other sources and with active bug dispersal from neighbouring foci. Thus, the households in the squatter settlement were at a greater risk of bug invasion and colonisation. In sum, the incipient process of domestic colonisation and transmission, along with persistent rural-to-urban migratory flows and unplanned urbanisation, indicate the need for active vector surveillance and control actions at the peri-urban interface of the Gran Chaco.     

Differences in competitive ability for the occupancy of shelters in triatomines

Triatomines (Hemiptera: Reduviidae: Triatominae) are nocturnal blood‐sucking insects. During daylight hours they remain in an akinetic state inside their shelters, whereas at dusk they become active and move outside. When they are outside their shelters during the photophase, triatomines are vulnerable to diurnal predators and the period just before dawn is critical to their survival. This work analyses the existence of competitive interactions involved in the occupancy of shelters by triatomines. Behavioural assays were performed in which nymphs of different stages, nutritional status or species were released in an experimental arena containing a space‐limited artificial shelter. The proportions of individuals occupying the shelter during the photophase were quantified to estimate the competitive abilities of each stage and species. Intraspecific comparisons showed higher levels of shelter occupancy for fourth over fifth instars and fed over unfed nymphs of Triatoma infestans. Interspecific comparisons showed higher rates of shelter occupancy for Triatoma sordida in comparison with T. infestans, and for T. infestans over Rhodnius prolixus. Arrival order was also relevant to determining shelter occupancy levels: early arrival was advantageous in comparison with later arrival. The study of intra‐ and interspecific competitive interactions for shelter occupancy provides relevant information about colonization and recolonization processes in the natural environments of triatomines.     

Isolation of <Emphasis Type="Italic">Beauveria bassiana</Emphasis> (Bals.) Vuill. (Deuteromycotina: Hyphomycetes) from the Chagas disease vector, <Emphasis Type="Italic">Triatoma infestans</Emphasis> (Hemiptera: Reduviidae) in Argentina

A survey for natural entomopathogenic fungi of the Chagas disease vector Triatoma infestans was conducted in five provinces of Argentina since 2001. Nymphs (1.5%) and adults (3.3%) infected with a strain of the fungus Beauveria bassiana were found at Dean Funes, Córdoba province, Argentina. Field collected insects that died in the laboratory were maintained in moist chambers and incubated at 22 °C. Beauveria bassiana from infected insects was cultured on SDAY media. Pathogenicity tests were conducted with a conidial suspension (1 × 10⁷ conidia/ml) of this isolate on T. infestans adults. A mortality rate of 100% was obtained at 15 days post-infection. This is the first record of natural infection of T. infestans by B. bassiana.     

Could the bug Triatoma sherlocki be vectoring Chagas disease in small mining communities in Bahia,Brazil?

Searches for Chagas disease vectors were performed at the type locality from which Triatoma sherlocki Papa et al. (Hemiptera: Reduviidae: Triatominae) was described in the municipality of Gentio do Ouro, in the state of Bahia, Brazil, and in a small artisan quarry‐mining community ～13 km distant in a remote area of the same municipality. The latter site represents a new locality record for this species. Adults, nymphs and exuviae of T. sherlocki were found in 21% of human dwellings, indicating that the species is in the process of domiciliation. Prevalence of Trypanosoma cruzi infection in collected bugs was 10.8%. Simple predictive approaches based on environmental similarity were used to identify additional sites likely suitable for this species. The approach successfully predicted an additional five sites for the species in surrounding landscapes. Ecological and entomological indicators were combined to discuss whether this scenario likely represents an isolated case or an emerging public health problem.