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Physiological Characterization of the Hematophagy of Ornithodoros

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Physiological Characterization of the Hematophagy of Ornithodoros © 2016. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2016) 219, 3656-3664 doi:10.1242/jeb.144246 RESEARCH ARTICLE Physiological characterization of the hematophagy of Ornithodoros rostratus (Acari: Argasidae) on live hosts Gabriel Cerqueira Alves Costa1,*, Adriana Coelho Soares1,*, Marcos Horácio Pereira1,2, Nelder Figueiredo Gontijo1,2, Maurıció Roberto Viana Sant’Anna1 and Ricardo Nascimento Araujo1,2,‡ ABSTRACT humans and other animals (Almeida et al., 2012; Hoogstraal, 1985). Ornithodoros rostratus is an argasid tick and its importance is based on Ornithodoros rostratus has been reported in four countries in South its hematophagy and the resulting transmission of pathogens such as America: Argentina, Bolivia, Brazil and Paraguay (Barros-Battesti Rickettsia rickettsii and Coxiella burnetii to its vertebrate hosts. In the et al., 2006; Guglielmone et al., 2003). face of a lack of physiological studies related to hematophagy in During its life cycle, O. rostratus has one larval and six nymphal argasid ticks, this paper aims to identify and characterize the events instars, in addition to the adult stage. The tick is an obligatory that occur throughout the feeding by O. rostratus on live hosts. hematophage in all stages and remains in contact with its host for Electrical signals and alterations on the feeding site were monitored varying periods, from a few minutes or hours (nymphal instars and using intravital microscopy and electromyography. The analyses adults) to days (larvae) (Costa et al., 2015; Lavoipierre and Riek, allowed for the characterization of four distinct events: suction, 1955; Ribeiro et al., 2013). Although contact with their host is for a salivation, chelicerae movements and inactivity. Feeding was divided short period of time, it is crucial because their success in obtaining into two distinct phases: (1) penetration of mouthparts (when only blood will affect their survival, development and reproduction salivation and chelicerae movements occurred) and the formation of (Anderson and Magnarelli, 2008); moreover, the short period of the feeding pool (salivation and chelicerae movements with the first contact also reduces the risk of being perceived and killed by the signs of suction) and (2) engorgement, during which chelicerae host (Rossignol et al., 1985). In addition, it is during blood feeding movements ceased and blood intake took place in feeding complexes that pathogens circulate between vectors and their hosts, thus (salivation followed by suction). Variations in patterns of the electrical interfering with the epidemiology of vector-borne diseases. signals, suction frequency and salivation showed four distinct sub- Owing to the obvious importance of hematophagy, some phases: (2a) suction with electrical signals of irregular shape, techniques, such as intravital microscopy and electronic increased suction frequency and decreased salivation frequency monitoring systems, have been developed to study the physiology throughout blood feeding; (2b) suction with electrical signals of of the feeding process. Intravital microscopy consists of visualizing symmetrical shape, high suction rates (3.8 Hz on average) and the feeding site on live hosts, allowing the evaluation of events that ’ feeding complexes lasting for 7.7 s; (2c) suction with electrical occur throughout the blood feeding from the arthropod s point of signals of irregular shape, high suction frequency and feeding view (e.g. visualization of movements of their mouthparts) as well ’ complex lasting 11.5 s; and (2d) electrical signals with no profile and as the host s (e.g. visualizing modifications that occur in their skin, the longest feeding complexes (14.5 s). Blood feeding ended with the microcirculation and tissues on the feeding site) (Soares et al., withdrawal of the mouthparts from the host’sskin. 2014). Although very informative, intravital microscopy misses many processes taking place inside the bloodsucking arthropod. KEY WORDS: Ornithodoros rostratus, Blood feeding, Pharyngeal This problem is addressed by the use of electronic monitoring pump, Intravital microscopy, Electromyogram systems: the electrical penetration graph (Backus, 1994) and electromyogram (Araujo et al., 2011) monitor the electrical INTRODUCTION signals (variation of resistance or voltage) generated at the Ornithodoros rostratus Aragão 1911 is an argasid tick that uses an arthropod–host interface. The electromyogram records signals eclectic array of food sources, including dogs, pigs, cows, peccaries generated by the arthropods’ muscles. Because bloodsucking and humans (Cançado et al., 2008; Hoogstraal, 1985; Ribeiro et al., arthropods are still during feeding, most of the electrical signals 2013). These soft ticks are of medical and veterinary importance as detected come from muscle contractions of the suction and salivary they give a painful and itchy bite (Aragão, 1936; Estrada-Pena and pumps. These muscles are responsible for the generation of negative Jongejan, 1999) and may harbor and transmit pathogens such as pressures during blood feeding, thus allowing blood to enter their Rickettsia rickettsii and Coxiella burnetii, the causative agents of the digestive system. These techniques have been used in the past to Rocky Mountain spotted fever and acute Q fever, respectively, in study blood feeding in several groups of arthropods such as aphids (McLean and Kinsey, 1964), mosquitoes (Choumet et al., 2012; 1Physiology of Hematophagous Insects Laboratory, Department of Parasitology, Griffiths and Gordon, 1952; Kashin and Wakely, 1965), tsetse flies Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais 31270-901, (Margalit et al., 1972), cimicids (Araujo et al., 2009a), triatomines Brazil. 2National Institute of Molecular Entomology, Rio de Janeiro 21941-591, (Smith and Friend, 1970; Soares et al., 2014, 2006) and ixodid ticks Brazil. *These authors contributed equally to this work (Bockenstedt et al., 2014; Gregson, 1969; Richter et al., 2013; Sweatman and Gregson, 1970; Tatchell et al., 1971; Waladde et al., ‡ Author for correspondence ([email protected]) 1979). Although they have been used for insects and ixodid ticks, R.N.A., 0000-0002-1272-4386 there is an obvious lack of information for argasid ticks, as few studies have focused on the physiology of their feeding process. Received 6 June 2016; Accepted 7 September 2016 Lavoipierre and Riek (1955) described several feeding aspects of Journal of Experimental Biology 3656 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 3656-3664 doi:10.1242/jeb.144246 different argasid species on rodents using intravital microscopy. vibration and handling of the ticks before testing. The time of the However, the authors failed to interpret and quantify some processes bite and the end of the feeding process were also visually monitored. and events that occurred during blood feeding. Recently, Zheng The ticks were weighed before and after the feeding experiment in et al. (2015) detected electrical signals produced while order to determine weight gain (calculated as final weight minus Ornithodoros turicata was feeding on artificial membranes and initial weight). Based on records of the electrical signals, the total characterized different phases of this process. However, again, contact time (TCT) was defined as the length of time the ticks feeding events were not quantified. mouthparts remained inserted into the host’s skin. Ingestion rate was In order to study in more detail the physiological processes during calculated as the ratio between weight gain and TCT. O. rostratus hematophagy on live hosts, groups of fourth instar nymphs were blood fed on mice and the feeding process was Simultaneous intravital microscopy and electromyogram monitored using electromyography and intravital microscopy Hairless Swiss mice (6- to 8-week-old males) were anesthetized and simultaneously. Such an association allowed for the identification placed on a heating pad as described above. Electromyograms were and quantification of different electrical signals generated during recorded as above, except that one electrode was fixed to the dorsal feeding in order to characterize each phase of the process. Analysis surface of the ticks using a small drop of instant adhesive and results presented here allow a better comparison between (Cyanocrylate) close to the tip and the feeding site was the convex the feeding patterns of O. rostratus and other blood-feeding dorsal surface of the mouse’s ear, which was flattened on double- arthropods. sided adhesive tape against a small Plexiglas platform. Images of the feeding site were recorded at 30 frames s−1 using a digital camera MATERIALS AND METHODS (Canon EOS Rebel T3i, Canon, Taiwan) attached to a microscope Ticks and colony rearing (Leica DM500, Leica Microsystems, HeerBrugg, Switzerland). Ticks used in the experiments were collected in Nhecolândia, Images recorded during feeding were analyzed using ImageJ located in the wetlands of Mato Grosso do Sul state, Brazil (19°03′S, software (Abramoff et al., 2004) according to Soares et al. (2014) 56°47′W), and were maintained inside an incubator under semi- and Araujo et al. (2011). The image of each movie frame was controlled conditions of temperature (28±2°C) and humidity (85± converted to a binary image (black and white), and the dark area of a 10%) (Costa et al., 2015). Ticks were fed Swiss mice (Mus selected region (containing the feeding site) was calculated after musculus) every 20–30 days. Fourth instar
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