Vector competence and feeding-excretion behavior of Triatoma rubrovaria (Blanchard, 1843) (Hemiptera: Reduviidae) infected with Trypanosoma cruzi TcVI

Abstract

Several studies addressed changes on the insect vector behavior due to parasite infection, but little is known for triatomine bugs, vectors of Trypanosoma cruzi, the etiological agent of Chagas disease. We assessed infection rates and metacyclogenesis of T. cruzi (TcVI) in fifth-instar nymphs of Triatoma rubrovaria comparing with the primary vector Triatoma infestans. Also, biological parameters related to feeding-excretion behavior were evaluated aiming to identify which variables are most influenced by T. cruzi infection. Fifth-instar nymphs of T. rubrovaria and T. infestans were fed on mice infected with T. cruzi (TcVI). We compared the presence and the number of parasite evolutive forms in excreta of both triatomine species at 30, 60 and 90 days post-infection (dpi) with traditional statistical analyses. Moreover, both species were analyzed through generalized linear models and multinomial logistic regression hypotheses for seven behavioral parameters related to host-seeking and feeding-excretion. Triatoma rubrovaria and T. infestans had similar overall infection and metacyclogenesis rates of T. cruzi TcVI in laboratory conditions. Regarding vector behavior, we confirmed that the triatomine’s tendency is to move away from the bite region after a blood meal, probably to avoid being noticed by the vertebrate host. Interspecific differences were observed on the volume of blood ingested and on the proportion of individuals that excreted after the blood meal, revealing the higher feeding efficiency and dejection rates of T. infestans. The amount of ingested blood and the bite behavior of T. rubrovaria seems to be influenced by TcVI infection. Infected specimens tended to ingest ~25% more blood and to bite more the head of the host. Noteworthy, in two occasions, kleptohematophagy and coprophagy behaviors were also observed in T. rubrovaria. Laboratory infections revealed similar rate of T. cruzi TcVI trypomatigotes in excreta of T. rubrovaria and T. infestans, one of the most epidemiological important vectors of T. cruzi. Therefore, TcVI DTU was able to complete its life cycle in T. rubrovaria under laboratory conditions, and this infection changed the feeding behavior of T. rubrovaria. Considering these results, T. rubrovaria must be kept under constant entomological surveillance in Rio Grande do Sul, Brazil. Chagas disease is caused by the etiological agent Trypanosoma cruzi and is mainly transmitted through the excreta of triatomine vectors. It is endemic in Latin America and the Caribbean, affecting ~8 million people. Control programs are based on the elimination of domestic vectors through insecticide-spraying indoors, since there is no vaccine or efficient treatment for chronic patients. However, this strategy is not sustainable where native triatomine species are capable of colonizing peridomestic structures and reinvading human dwellings. Since the ‘virtual’ elimination of Triatoma infestans in Brazil (residual foci remain in Rio Grande do Sul and Bahia), specimens of the native Triatoma rubrovaria have been constantly collected inside human dwellings and peridomiciliary ecotopes in Rio Grande do Sul, southern Brazil, which might represent a real risk for human infections. Here we analyzed a unique and large dataset through classical and modern statistical methods to evaluate T. cruzi infection in T. rubrovaria and to identify host-seeking, and also feeding/excretion behavioral traits that could be influenced by the parasite. Our results indicated that the parasite infection caused changes in T. rubrovaria feeding behavior that could increase T. cruzi TcVI transmission. Moreover, this vector species had similar infection rate to one of the main important Chagas disease vectors in South America, T. infestans. Therefore, T. rubrovaria must be kept under constant entomological surveillance in Rio Grande do Sul, Brazil.