Feeding Performance of Triatoma brasiliensis (Hemiptera: Reduviidae) on Habitual Hosts: Thrichomys laurentius (Rodentia: Echimyidae) and Humans

Abstract

Triatoma brasiliensis is an important vector of Trypanosoma cruzi in the semiarid zones of Northeastern Brazil where it is commonly found in human dwellings, peridomiciliary areas, and the wild environments. To better understand features that may be influencing the interaction of T. brasiliensis with its hosts, in the present work we compared the feeding performance of sylvatic and domestic populations of T. brasiliensis on humans and on Thrichomys laurentius, a wild rodent found in the natural ecotopes of T. brasiliensis. The analyses were performed using the electronic monitoring of the cibarial pump. The blood sources considerably affected the feeding parameters. Insects fed on T. laurentius had lower ingestion rate, gained less weight, had longer interruption time, remained less time in contact with the host, and had the contractions of the pump in a lower frequency during the feeding process in comparison to insects fed on humans. These results indicate that humans are better blood sources for T. brasiliensis than T. laurentius. The fact that there was no difference between the feeding performance of sylvatic and domestic insects suggests that feeding is not a barrier for the domiciliation. Together, these findings suggest that shelter and faster blood meals are qualities of human dwellings that facilitate the domiciliation of T. brasiliensis.

Introduction

T riatoma brasiliensis (Hemiptera: Reduviidae) is one of the most important vectors of Trypanosoma cruzi in the semiarid zones of Northeastern Brazil where it is able to colonize wild, peridomiciliary, and domiciliary environments (Costa et al. 1998, Goncalves et al. 2009). In wild, the species has extensive ecotopes, especially among rocky crevices in the arid region of the northeast where it takes blood from rodents, opossums, birds, and bats (Alencar 1987). In areas of human dwellings and their surroundings, T. brasiliensis has been associated with peridomiciliary structures and human activities, taking blood from humans and their domestic animals (Alencar 1987, Costa et al. 1998). Sylvatic populations can serve as sources of reinfestations in areas where they had been controlled by insecticide spraying campaigns (Diotaiuti et al. 2000).

The punarè Thrichomys laurentius (Rodentia, Echimyidae) is a caviomorph rodent associated to xeric and rocky environments with frequent incursions into human dwellings and has an ample distribution in the Northeast. It was the most abundant rodent species captured in the Brazilian states of Ceará and Piauí with infection rates varying from 0.7% to 45% for T. cruzi (Alencar 1987, Herrera et al. 2005).

Since T. brasiliensis circulate among different environments, taking blood from wild and domestic hosts, in the present work, we evaluated the feeding performance of two populations on T. laurentius and human hosts.

Materials and Methods

Insects

The T. brasiliensis specimens belonged to the second generation of a colony derived from insects collected in human dwellings (domestic population) or among rock piles (sylvatic population) in Novo Oriente, Ceará, Brazil. The insects were reared under semicontrolled conditions (28°C ± 2°C and 65% ± 10% relative humidity) and fed weekly on mice or chickens according to ethical principles of animal care (CEUA-FIOCRUZ, license number L-058/08).

Hosts

T. laurentius specimens were captured from rock piles in Crateús, Ceará, Brazil, using live traps baited with fresh vegetables. The animals were captured and transported under permission from IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis–licence n. 076/2000-DIFAS/DIREC) and were sedated (Diazepam, 4 mg/kg body wt) by intraperitoneal injection before the assays. Human volunteers were three of the authors (A.A.G., N.F.G., M.H.P).

Feeding performance by the electronic monitoring of cibarial pump

The electronic monitoring of cibarial pump was performed according to Guarneri et al. (2003). T. brasiliensis fifth instar nymphs starving for 14 days were allowed to feed on the ventral surface of T. laurentius or on the forearm of human volunteers. The following feeding parameters were compared between groups: initial weight (IW, mg), cumulative probing time (PT, s), total ingestion rate (IR, mg/min), pump frequency (F, Hz), quantity of blood ingested per cibarial pump contraction (QLC, μg of blood/contraction), interruptions during the engorgement phase (I, measured as the the percentage of time without food intake), total contact time (TT, min), and the normalized weight gain (WG, ratio WG/IW). Variables were initially checked by normality using the Kolmogorov-Smirnov test. To examine whether feeding performance was affected by the host used, a one-way analysis of variance with host used as a single factor was performed. Since the IW was significantly different between the two groups of insects, a second analysis included a correlation matrix among IW, IR, F, QLC, TT, and PT. The variables that were positively correlated with IW were submitted to a two-way analysis of covariance (ANCOVA) with host and population used as main component and IW as covariate. The differences were considered to be significant when p < 0.05.

Results

Parameters of the feeding performance of each T. brasiliensis population on the hosts are shown in Table 1. There was no difference between the feeding performance of domestic and sylvatic specimens of T. brasiliensis (ANCOVA, not significant). However, feeding parameters from bugs fed on T. laurentius were negatively affected in comparison to the ones fed on humans. When feeding on punarè, bugs presented lower IR (ANCOVA), which was due to the longer interruption time observed for this group. The group fed on humans did not interrupt feeding after the ingestion period had begun, whereas 78.7% of the insects fed on punarè presented one or more interruptions during the course of the meal. The insects fed on T. laurentius also remained less time in contact with the host, gained less weight, and had the contractions of the pump in a lower frequency during the feeding process (ANCOVA, p < 0.001). Despite the great range of cumulative PT values, statistically significant differences were not found among groups (Kruskall-Wallis, not significant).

Table 1.

Parameters of the Feeding Performance from Domestic and Sylvatic Populations of Triatoma Brasiliensis Fed on Human and the Rodent Thrichomys Apereoides

Parameters analyzed	HD (n = 10)	HS (n = 10)	RD (n = 18)	RS (n = 16)	p-Value (statistical analysis)
Initial weight (mg) (mean ± SE)	68.0 ± 4.0	66.1 ± 5.0	55.4 ± 3.3	59.6 ± 3.0	0.01 (ANOVA) F = 6.15; df = 1
Cumulative probing time (s) (median; 1st–3rd quartile)	45 (12–99)	50 (33–90)	33 (13–92)	154 (51–270)	n.s. (Kruskall-Wallis) χ ² = 0.67; df = 1
Total ingestion rate (mg/min) (mean ± SE)	11.3 ± 0.9	11.0 ± 1.3	4.5 ± 0.7	5.5 ± 1.4	0.00004 (ANCOVA) F = 19.77; df = 1
Pump frequency (Hz) (mean ± SE)	3.0 ± 0.2	2.7 ± 0.3	2.1 ± 0.1	2.3 ± 0.2	0.04 (ANCOVA) F = 4.03; df = 1
Quantity of blood ingested per cibarial pump contraction (μg) (mean ± SE)	62.8 ± 3.4	66.3 ± 4.3	49.2 ± 5.1	51.4 ± 6.7	n.s. (ANCOVA) F = 1.16; df = 1
Interruptions (%) (median; 1st–3rd quartile)	0	0	13.5 (0–43.6)	20 (6.7–24.7)	0.0001 (Kruskall-Wallis) χ ² = 28.67; df = 1
Total contact time (min) (mean ± SE)	34.0 ± 2.3	37.6 ± 4.7	15.7 ± 2.0	23.2 ± 3.0	0.0001 (ANCOVA) F = 28.46; df = 1
Normalized weight gain (median; 1st–3rd quartile)	5.7 (4.7–6.8)	5.5 (4.5–8.2)	1.2 (0.9–1.5)	1.2 (0.8–1.9)	0.0001 (Kruskall-Wallis) χ ² = 31.72; df = 1

HD, domestic population fed on human; HS, sylvatic population fed on human; RD, domestic population fed on rodent; RS, sylvatic population fed on rodent; SE, standard error; ANOVA, analysis of variance; ANCOVA, analysis of covariance; F, frequency; df, degrees of freedom; n.s., not significant.

Discussion

Previous works using the electronic monitoring of cibarial pump have showed that triatomines have different feeding performance depending on the host (Guarneri et al. 2000, Sant'Anna et al. 2001). In general, feeding on mammals is more difficult than on birds. Recently, we showed that T. brasiliensis faced difficulties to obtain blood from T. laurentius in comparison to rats (Araujo et al. 2009a). Several hematological parameters may affect the feeding performance and may explain the findings of the present work, including the viscosity of the blood (Lehane 2005) and the diameter of the feeding vessel (Araujo et al. 2009b).

In the domestic and sylvatic insects that fed on punarè, 72.2% and 75%, respectively, interrupted feeding after starting to engorge. These interruptions forced the insects to remain in contact with the hosts for longer periods and/or stop the meal, so that they ingested less blood than those that had fed on human hosts. The ingestion of smaller meals in the wild obligates the insects to feed several times to obtain enough blood for moulting or egg laying and also increases the probability of being perceived by the host (Schofield 1985). Although the sources of blood available to T. brasiliensis in its natural environment are still not completely known, punarè are likely to be important hosts, as they are abundant in the natural shelters of T. brasiliensis (Herrera et al. 2005, Roque et al. 2008). In a recent capture of sylvatic vertebrates in an area of the State of Ceará density colonized by T. brasiliensis, at several times, specimens of this vector were captured by taking blood from T. laurentius still inside of the traps (L. Diotaiuti, pers. comm.), showing the use of this rodent as source of food in the natural conditions. Nevertheless, human dwellings offer shelters with favorable climatic conditions, low exposition to predators, and also present hosts that allow faster blood meals, favoring the adaptation of this triatomine species to the domiciliary environment. The finding that domestic and sylvatic specimens had no difference in feeding performance enforce that it is not a barrier for the domiciliation of sylvatic T. brasiliensis.

Footnotes

Acknowledgments

This study was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Centro de Pesquisas René Rachou/Fundação Oswaldo Cruz CPqRR/FIOCRUZ) and benefited from international collaboration through the European Community-Latin American Network for Research on the Biology and Control of Triatominae (ECLAT). The authors thank the valuable comments from the reviewers.

Disclosure Statement

No competing financial interests exist.

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