Physiological characterization of the hematophagy ofOrnithodoros rostratus(Acari: Argasidae) on live hosts

Abstract

Ornithodoros rostratus is an argasid tick and its importance is based on its hematophagy and the resulting transmission of pathogens such as Rickettsia rickettsii and Coxiella burnetii to its vertebrate hosts. In the face of a lack of physiological studies related to hematophagy in argasid ticks, this paper aims to identify and characterize the events that occur throughout the feeding by O. rostratus on live hosts. Electrical signals and alterations on the feeding site were monitored using intravital microscopy and electromyography. The analyses allowed for the characterization of four distinct events: suction, salivation, chelicerae movements and inactivity. Feeding was divided into two distinct phases: (1) penetration of mouthparts (when only salivation and chelicerae movements occurred) and the formation of the feeding pool (salivation and chelicerae movements with the first signs of suction) and (2) engorgement, during which chelicerae movements ceased and blood intake took place in feeding complexes (salivation followed by suction). Variations in patterns of the electrical signals, suction frequency and salivation showed four distinct subphases: (2a) suction with electrical signals of irregular shape, increased suction frequency and decreased salivation frequency throughout blood feeding; (2b) suction with electrical signals of symmetrical shape, high suction rates (3.8 Hz on average) and feeding complexes lasting for 7.7 s; (2c) suction with electrical signals of irregular shape, high suction frequency and feeding complex lasting 11.5 s; and (2d) electrical signals with no profile and the longest feeding complexes (14.5 s). Blood feeding ended with the withdrawal of the mouthparts from the host's skin.

AC–DC electropenetrography unmasks fine temporal details of feeding behaviors for two tick species on unsedated hosts

“…Electronic instruments have previously been used to record the feeding behavior of blood-feeding arthropods (~ 20 publications), including with argasid ticks 33,34 . Recent instrument designs use high-sensitivity electromyography (EMG) amplifiers, like those used by electrophysiologists.…”

“…These include: (i) electrical resistance from opening/closing of valves/pumps in the foregut as well as mouthpart movements/depth; and, (ii) electrical conductivity related to biochemical composition of saliva 20,22 . While a few EMG papers have identified trace salivation and mouthpart movement biopotentials 33,34 , their electrical resistance information is likely incomplete. In addition, a major benefit of AC-DC EPG is the far wider range of selectable amplifier sensitivities, to detect all signal types from resistance-only to biopotential-only and mixtures of both 19,22 .…”

“…The latter often encompasses a variable window of time rather than a specific time 10,15,28,[36][37][38] . Previous studies examining specific tick tissue functions are www.nature.com/scientificreports/ rarer, and commonly require: (i) interruption of tick feeding, with or without dissection of the tissue target; (ii) adaptation of ticks to artificial feeding systems; (iii) use of sedated hosts (argasid tick studies); or, (iv) significant host discomfort 33,34,[39][40][41] . Studies on real-time expression of precise on-host ixodid feeding behaviors are lacking, largely due to absence of tools to investigate them.…”

Soft ticks perform evaporative cooling during blood-feeding

“…During its life cycle, this species has one larval and three to six nymphal instars, and adults can arise from 3 rd to 6 th -instar nymphs (Costa et al 2015). This species is an obligatory hematophagous arthropod in all stages and remains in contact with its host for a period varying from a few minutes to hours (nymphal instars and adults), or even days (larvae) (Costa et al, 2015(Costa et al, , 2016Lavoipierre and Riek, 1955;Ribeiro et al, 2013). Although contact with their host is for a short period of time as compared to hard ticks, it remains crucial as their success in obtaining blood will then affect their survival, development and reproduction (Anderson and Magnarelli, 2008).…”