Trypanosoma cruzi-infected Rhodnius prolixus endure increased predation facilitating parasite transmission to mammal hosts

Abstract

Triatomine bugs aggregate with conspecifics inside shelters during daylight hours. At dusk, they leave their refuges searching for hosts on which to blood feed. After finding a host, triatomines face the threat of being killed, because hosts often prey on them. As it is known that many parasites induce the predation of intermediate hosts to promote transmission, and that ingestion of Trypanosoma cruzi-infected bugs represents a very effective means for mammal infection, we hypothesized that trypanosomes induce infected bugs to take increased risk, and, as a consequence, be predated when approaching a host. Therefore, we evaluated whether the predation risk and predation rates endured by Rhodnius prolixus increase when infected with T. cruzi. Assays were performed in square glass arenas offering one central refuge to infected and uninfected 5th instar nymphs. A caged mouse was introduced in each arena after a three-day acclimation interval to activate sheltered insects and induce them to approach it. As hypothesized, a significantly higher proportion of infected insects was predated when compared with uninfected ones (36% and 19%, respectively). Indeed, T. cruzi-infected bugs took higher risk (Approximation Index = 0.642) when compared with healthy ones (Approximation Index = 0.302) and remained outside the shelters when the host was removed from the arena. Our results show that infection by T. cruzi induces bugs to assume higher risk and endure higher predation rates. We reveal a hitherto unknown trypanosome-vector interaction process that increases infected bug predation, promoting increased rates of robust oral transmission. The significant consequences of the mechanism revealed here make it a fundamental component for the resilient maintenance of sylvatic, peridomestic and domestic cycles.

The Parasite Load of Trypanosoma cruzi Modulates Feeding and Defecation Patterns of the Chagas Disease Vector Triatoma infestans

“…The incongruences observed between our results and other reports, which are focused on the feeding and defecation behavior, could be associated, among others, with the different vector and parasite ( T. cruzi / T. rangeli ) combinations or genotypes, their parasite load, their starvation time, time after infection, or different pre-experimental and experimental blood sources [ 15 , 16 , 17 , 18 , 19 , 26 , 50 ]. Although these differences make direct comparisons difficult, all of these investigations confirm that T. cruzi modifies the behavior of their hosts.…”

“…Verly et al (2020) [ 59 ], observed that Triatoma rubrovaria (Blanchard, 1843) infected with T. cruzi ingested about 25% more blood than non-infected insects. Our results and others [ 17 ] show that there seems to be a taxon-specific effect of the infection, as infected T. infestans show the same tendency to increase the number of bites, but also to ingest and retain more blood, unlike other triatomine species. The amount of blood ingested seems to be positively influenced by the T. cruzi infection [ 59 ].…”

“…As proposed before by several other authors [ 6 , 17 , 21 , 52 , 53 ], a hypothesis to explain the increase in the number of bites and the decrease in host detection time, which was more evident in triatomines with a higher T. cruzi load, could be a competition between the triatomine and T. cruzi for the nutrients in the ingested blood, leading these insects to a more advanced state of starvation when compared to individuals with a lower parasite load, and those who are non-infected. Triatomines in this state may become more receptive to stimuli: They do not sit and wait until a host appears or move randomly in search of signals; instead, they orient themselves with the air streams to capture smells of interest [ 7 , 54 ].…”

“…The vectorial transmission of the parasite to vertebrates would be impaired if the vector leaves the host before defecating, so the time that the triatomine takes to excrete its first dejection is important from an epidemiological point of view [ 15 , 16 ]. Prolonged feeding increases the contact time between the host and the vector, increasing the probability of T. cruzi acquisition by the triatomine contact between the parasite and the host [ 16 ]; its downside is the enhanced chance of predation by the host of the vector, which in turn could result in oral transmission of T. cruzi [ 17 ].…”

Global characterization of gene expression in the brain of starved immature Rhodnius prolixus

“…The decision to leave a shelter and engage in foraging is risky, as triatomine hosts are often predators as well. For this reason, starved bugs mostly leave the protection of the shelters when a robust set of host clues is present [3][4][5]. Bugs of all nymphal instars and adults of both sexes feed on blood and can tolerate long starvation.…”