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Single sensillum recording on different types of olfactory sensilla in the common bed bug, C. lectularius . ( A ) Schematic image of single sensillum recording in the olfactory sensilla on bed bug antennae. ( B ) SEM photo (modified from Liu et al. , 2014) showing the different types of olfactory sensilla on bed bug antennae. The scale bar indicates 20 μ M. ( C ) The highest neural responses for each type of olfactory sensillum to different human odorants.
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The common bed bug Cimex lectularius is a temporary ectoparasite on humans and currently resurgent in many developed countries. The ability of bed bugs to detect human odorants in the environment is critical for their host-seeking behavior. This study deciphered the chemical basis of host detection by investigating the neuronal response of olfactor...
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Citations
... In an intriguing article published in the food journal Gastronomica, Helen Leach highlights how for several centuries those who found coriander leaf unpleasant would describe it as having a bug-like odour. She goes on to note that during this period, the internal heating of homes improved, meaning that far more people were likely exposed to the smell of bed bugs than ever before (see Liu and Liu, 2015, on the human odour perception of bed bugs). At the same time, however, Leach also identifies and traces the longstanding etymological confusion related to whether the term for coriander may have been derived from, or the same as, the word for bug (see several of the above quotes for evidence on this very theme). ...
... On the other hand, several old OR lineages of single genes previously identified in R. prolixus (RproOr1, RproOr2, RproOr101-105, RproOr107, and RproOr112) [41] were also found in T. infestans and other heteropterans (Additional file 6: Supplementary Figure S2). Functional information for some of these old OR lineages has been generated in C. lectularius [90,91]. For instance, ClecOr5 (related to TinfOr103 and RproOr103) responds to nonanal and octanal; and ClecOr9 (related to TinfOr105 and RproOr105) detects decanal. ...
Background
Triatoma infestans is the main vector of Chagas disease in the Americas, currently transmitting it in Argentina, Paraguay, and Bolivia. Many T. infestans populations present insecticide resistance, reducing the efficiency of control campaigns. Alternative vector control methods are needed, and molecular targets mediating fundamental physiological processes can be a promising option to manipulate kissing bug behavior. Therefore, it is necessary to characterize the main sensory targets, as well as to determine whether they are modulated by physiological factors. In order to identify gene candidates potentially mediating host cue detection, the antennal transcripts of T. infestans fifth instar larvae were sequenced and assembled. Besides, we evaluated whether a blood meal had an effect on transcriptional profiles, as responsiveness to host-emitted sensory cues depends on bug starvation.
Results
The sensory-related gene families of T. infestans were annotated (127 odorant receptors, 38 ionotropic receptors, 11 gustatory receptors, 41 odorant binding proteins, and 25 chemosensory proteins, among others) and compared to those of several other hemipterans, including four triatomine species. Several triatomine-specific lineages representing sensory adaptations developed through the evolution of these blood-feeding heteropterans were identified. As well, we report here various conserved sensory gene orthogroups shared by heteropterans. The absence of the thermosensor pyrexia, of pickpocket receptor subfamilies IV and VII, together with clearly expanded takeout repertoires, are revealed features of the molecular bases of heteropteran antennal physiology. Finally, out of 2,122 genes whose antennal expression was significantly altered by the ingestion of a blood meal, a set of 41 T. infestans sensory-related genes (9 up-regulated; 32 down-regulated) was detected.
Conclusions
We propose that the set of genes presenting nutritionally-triggered modulation on their expression represent candidates to mediate triatomine host-seeking behavior. Besides, the triatomine-specific gene lineages found represent molecular adaptations to their risky natural history that involves stealing blood from an enormously diverse set of vertebrates. Heteropteran gene orthogroups identified may represent unknown features of the sensory specificities of this largest group of hemipteroids. Our work is the first molecular characterization of the peripheral modulation of sensory processes in a non-dipteran vector of human disease.
... On the other hand, several old OR lineages of single genes previously identi ed in R. prolixus (RproOr1, RproOr2, RproOr101-105, RproOr107, and RproOr112) [32] were also found in T. infestans and other heteropterans (Additional le 6: Supplementary Figure S2). Functional information for some of these old OR lineages has been generated in C. lectularius [72,73]. For instance, ClecOr5 (related to TinfOr103 and RproOr103) responds to nonanal and octanal; and ClecOr9 (related to TinfOr105 and RproOr105) detects decanal. ...
Background
Triatoma infestans is the main vector of Chagas disease in the Americas, currently transmitting it in Argentina, Paraguay, and Bolivia. Many T. infestans populations present insecticide resistance, reducing the efficiency of control campaigns. Alternative vector control methods are needed, and molecular targets mediating fundamental physiological processes can be a promising option to manipulate kissing bug behavior. Therefore, it is necessary to characterize the main sensory targets, as well as to determine whether they are modulated by physiological factors. In order to identify gene candidates potentially mediating host cue detection, the antennal transcripts of T. infestans fifth instar larvae were sequenced and assembled. Besides, we evaluated whether a blood meal had an effect on transcriptional profiles, as responsiveness to host-emitted sensory cues depends on bug starvation.
Results
The sensory-related gene families of T. infestans were annotated (127 odorant receptors, 38 ionotropic receptors, 11 gustatory receptors, 41 odorant binding proteins, and 25 chemosensory proteins, among others) and compared to those of several other hemipterans, including four triatomine species. Several triatomine-specific lineages representing sensory adaptations developed through the evolution of these blood-feeding heteropterans were identified. As well, we report here various conserved sensory gene orthogroups shared by heteropterans. The absence of the thermosensor pyrexia, of subfamily IV and VII pickpocket receptors, together with clearly expanded takeoutrepertoires, are revealed features of the molecular bases of heteropteran antennal physiology. Finally, out of 2122 genes whose antennal expression was significantly altered by the ingestion of a blood meal, a set of 41 T. infestans sensory-related genes (9 up-regulated; 32 down-regulated) is detected.
Conclusions
We propose that the set of genes presenting nutritionally-triggered modulation on their expression represent candidates to mediate triatomine host-seeking behavior. Besides, the triatomine-specific gene lineages found represent molecular adaptations to their risky natural history that involves stealing blood from an enormously diverse set of vertebrates. Heteropteran gene orthogroups identified represent an unknown feature of the sensory specificities of this largest group of hemipteroids. Our work is the first molecular characterization of the peripheral modulation of sensory processes in a non-dipteran vector of human disease.
... Bed bugs detect cues (mostly volatile) using sensilla on the antennae and other sensory appendages. The distal tip of each antenna houses seven different sensilla, with type-Ds shown to be responsible for human odorant reception [35][36][37] . A more detailed single sensillum electrophysiology study is needed to investigate the roles of various sensilla in detecting TAGs. ...
Bed bugs (Cimex lectularius) have proliferated globally and have become one of the most challenging pests to control indoors. They are nocturnal and use multiple sensory cues to detect and orient towards their human hosts. After feeding, usually on a sleeping human, they return to a shelter on or around the sleeping surface, but not directly on the host. We hypothesized that although human skin odors attract hungry bed bugs, human skin compounds may also prevent arrestment on hosts. We used arrestment assays to test human skin swabs, extracts from human skin swabs, and pure compounds identified from human skin swabs. When given a choice, bed bugs preferred to arrest on substrates not previously conditioned by humans. These responses were consistent among laboratory-reared and apartment-collected bed bugs. The compounds responsible for this behavior were found to be extractable in hexane, and bed bugs responded to such extracts in a dose-dependent manner. Bioassay-guided fractionation paired with thin-layer chromatography, GC-MS, and LC-MS analyses suggested that triglycerides (TAGs), common compounds found on human skin, were preventing arrestment on shelters. Bed bugs universally avoided sheltering in TAG-treated shelters, which was independent of the number of carbons or the number of double bonds in the TAG. These results provide strong evidence that the complex of human skin compounds serve as multifunctional semiochemicals for bed bugs, with some odorants attracting host-seeking stages, and others (TAGs and possibly other compounds) preventing bed bug arrestment. Host chemistry, environmental conditions and the physiological state of bed bugs likely influence the dual nature behavioral responses of bed bugs to human skin compounds.
... Although trichoid, grooved peg and smooth peg sensilla are putative sensors of olfactory, thermal and hydric cues, only detection of olfactory cues was reported in functional studies (Table 1). Trichoid sensilla, smooth peg sensilla and grooved pegs were demonstrated to respond to both host odours and alarm pheromones (Harraca et al., 2010a(Harraca et al., , 2010b(Harraca et al., , 2012Levinson et al., 1974;Liu and Liu, 2015). The unserrated bristles and the third type of E sensillum (E 3 ) were implied in gustatory functions whereas the immersed cones in thermo-hygroreception (Levinson et al., 1974;Olson et al., 2014). ...
... ClOrco expression was characterized in several sensory tissues (Hansen et al., 2014). Functional experiments performed by Liu and Liu (2015) addressed the detection of host-related odours such as nonanal and decanal by ClOR1 and ClOR2. The intermediately sized sensory repertoire of bed bugs is in accordance with the moderate complexity of its chemical ecology, but having a broader host range than the human louse (Benoit et al., 2016). ...
Many hematophagous insects acquire medical and veterinary relevance because they transmit disease causing pathogens to humans. Hematophagy is only fulfilled once a blood feeder successfully locates a vertebrate host by means of fine sensory systems. In nature, blood-sucking insects can exploit environments with differential association with their hosts. Given the relevance of the sensory systems during host searching, we review the current state of knowledge of the sensory machinery of four blood-sucking insects: human lice, bed bugs, kissing bugs and mosquitoes. Each one is representative of highly anthropophilic behaviours and a different degree of association with human hosts. We compare the number, arrangement and functional type of cuticular sensory structures dispersed on the main sensory organs. We also compare the genetic machinery potentially involved in the detection of host stimuli. Finally, we discuss the sensory diversity of the insects studied here.
... The E1 and E2 type sensillae at the terminal antennal segment of C. lectularius have been demonstrated playing a key role in alarm pheromone perception (Levinson et al. 1974). All the 9 grooved peg sensillae located at the distal tip of antennae are involved in the perception of ammonia in C. lectularius (Harraca et al. 2010); and the D-type sensillae on C. lectularius antennae has been demonstrated playing a vital role for perceiving human odorants (Liu and Liu 2015). In Experiment III, male C. hemipterus could not respond to CO 2 once their antennae or mouthparts or both antennae and mouthparts were removed, which suggest that the sensillae located on antennae and mouthparts were involved in the CO 2 perception of C. hemipterus. ...
Bed bugs (Cimex spp.) (Hemiptera: Cimicidae) are obligatory blood-sucking insects. Research on their behavioral response to host-derived olfactory cues will be helpful for designing more effective management tools. However, previous studies mainly focused on Cimex lectularius L., while the related studies on Cimex hemipterus (F.) have been rarely reported. In this study, we evaluated the behavioral responses of C. hemipterus to one of the crucial host-derived cues - carbon dioxide (CO2), at various concentrations. Pitfall traps baited with CO2 captured significantly more C. hemipterus (72%) than unbaited ones (28%). In the Y-tube test, bed bugs' exploratory activity (response rate) gradually decreased (from 70 to 27%) as the CO2 concentration increased (from 0.9 to 14.5%); and bed bugs exhibited a significant attraction to CO2 when the tested CO2 concentrations were between 0.9 and 7.3%. Cimex hemipterus were no longer attracted to CO2 after their antennae or mouthparts or both antennae and mouthparts were removed. In conclusion, C. hemipterus are attracted to CO2, and both antennae and mouthparts are important for CO2 perception.
... Electrophysiological studies have shown that bed bugs can sense 104 human skin volatiles. 67 There is a need for techniques like those used in pheromone research by Gries et al. 30 to be applied in the identification of host kairomones that could potentially be used to improve trap lures. ...
Bed bugs, Cimex lectularius L. and C. hemipterus (F.) (Hemiptera: Cimicidae) are hematophagous ectoparasites of humans. Since the resurgence of bed bugs in the late 1990s there has been a corresponding emphasis on development and implementation of integrated pest management (IPM) programs to manage infestations. One critical requirement of IPM is the ability to detect and monitor the target pest. We outline and describe the majority of all known existing devices and technologies developed for bed bug detection and monitoring as well as much of the underlying science. Almost 40 detection and monitoring products have flooded the marketplace, but for various reasons, including price, size, complexity and lack of independent scientific evaluation, they have not been widely adopted for IPM in structures. One product, the ClimbUp® Insect Interceptor, has nine competitors that utilize a similar design. This review also discloses many other technologies and products that are either too expensive or too impractical for use as either consumer or industrial products. We conclude that there is a critical need for inexpensive and effective detection and monitoring traps and lures suitable for widespread adoption by the urban pest control industry. © 2021 Society of Chemical Industry.
... For example, the total number of trichoidea sensilla varies dramatically between Triatoma (400-800) and Rhodnius A B C D FIGURE 1 | Olfactory mechanism of the peripheral olfactory system in bed bugs and kissing bugs. (A) Scanning electronic microscope images show six functional types of olfactory sensillum (Dα, Dβ, Dγ, E1, E2, and C) for bed bugs (left; Liu and Liu, 2015) and two types (Basiconica and grooved peg) for kissing bugs (right; adapted from Guerenstein and Guerin, 2001, with the permission from Dr. Guerin). (B) The olfactory receptor neurons housed in each olfactory sensillum are responsible for detecting the attractive cues and increasing the firing frequency of the action potentials. ...
... Potent sensitivities of the kissing bug olfactory sensillum to host odor plumes and a few unitary aldehyde and acid compounds have been described (Guerenstein and Guerin, 2001), while the bed bug olfactory sensilla are particularly sensitive to several chemical classes of odors in human emanation, especially aldehydes, alcohols, aromatics, and ketones (Liu and Liu, 2015), as well as plant-sourced terpenes and terpenoids (Liu et al., 2014). Similar patterns have also been reported for two mosquitoes, Culex quinquefasciatus and Aedes aegypti (Liu et al., 2013;Ye et al., 2016;Chen et al., 2018Chen et al., , 2019. ...
... According to the various models that have been proposed, an OR may be activated either by the odorant molecule itself or the OBP(CSP)/odorant complex (Leal, 2013). For instance, knockdown of OBP1 in the southern house mosquito Levinson et al., 1974;[2] Steinbrecht and Müller, 1976;[3] Singh et al., 1996;[4] Harraca et al., 2010;[5] Liedtke et al., 2011;[6] Olson et al., 2014;[7] Liu et al., 2014;[8] Liu and Liu, 2015;[9] Wigglesworth and Gillett, 1934; [10] Mayer, 1968;[11] Bernard, 1974;[12] Mciver and Siemicki, 1985;[13] Lazzari, 1990;[14] Catalá and Schofield, 1994;[15] Lazzari and Wicklein, 1994;[16] Catalá, 1997;[17] Taneja and Guerin, 1997;[18] Guerenstein and Guerin, 2001;[19] Carbajal De La Fuente and Catalá, 2002;[20] Diehl et al., 2003;[21] Catalá et al., 2004;[22] Villela et al., 2005; [23] Moreno et al., 2006;[24] Pontes et al., 2014. C. quinquefasciatus results in reduced EAG responses to mosquito oviposition pheromones (Pelletier et al., 2010) and silencing OBP1 leads to a failure to sense indole, a key component of human sweat, in the malaria mosquito Anopheles gambiae (Biessmann et al., 2010). ...
As one of the most abundant insect orders on earth, most Hemipteran insects are phytophagous, with the few hematophagous exceptions falling into two families: Cimicidae, such as bed bugs, and Reduviidae, such as kissing bugs. Many of these blood-feeding hemipteran insects are known to be realistic or potential disease vectors, presenting both physical and psychological risks for public health. Considerable researches into the interactions between hemipteran insects such as kissing bugs and bed bugs and their human hosts have revealed important information that deepens our understanding of their chemical ecology and olfactory physiology. Sensory mechanisms in the peripheral olfactory system of both insects have now been characterized, with a particular emphasis on their olfactory sensory neurons and odorant receptors. This review summarizes the findings of recent studies of both kissing bugs (including Rhodnius prolixus and Triatoma infestans) and bed bugs (Cimex lectularius), focusing on their chemical ecology and peripheral olfactory systems. Potential chemosensation-based applications for the management of these Hemipteran insect vectors are also discussed.
... The process of taking a bloodmeal and finding the blood vessels quickly without disturbing the host is a key feature for the adaption of hematophagy in insects (Ferreira et al. 2007). Previous research showed that removal of terminal segments elicits no behavioral response to stimuli usually driven by olfactory cues (Harraca et al. 2010, Liu andLiu 2015). Female kissing bug antennae have sensilla between E type hairs with increased surface area of antennae structure. ...
... To follow up with the current assays, a modified arena that allows for monitoring of bedbugs not only on direction but also velocity and intensity of attraction to heat, CO 2 , and moisture would be a strong future direction. Questions remain about how chemical cues and heated stimuli activate bed bug host selection behavior (Liu and Liu 2015). Behavioral responses are hard to study without proper visual equipment in place to observe nightly activities of bed bugs. ...
The bed bug, Cimex lectularius L., is a common ectoparasite found to live among its vertebrate hosts. Antennal segments in bugs are critical for sensing multiple cues in the environment for survival. To determine whether the thermo receptors of bed bugs are located on their antennae; innovative bioassays were created to observe the choice between heated and unheated stimuli and to characterize the response of bugs to a heat source. Additionally, the effect of complete antenectomized segments on heat detection were evaluated. Heat, carbon dioxide, and moisture are cues that are found to activate bed bug behavior; a temperature at 38°C was used to assess the direction/degree at which the insect reacts to the change in distance from said stimulus. Using a lightweight spherical ball suspended by air through a vacuum tube, bed bugs and other insects are able to move in 360° while on a stationary point. Noldus EthoVision XT was used to capture video images and to track the bed bugs during 5-min bioassays. A bioassay was created using four Petri dish arenas to observe bed bug attraction to heat based on antennae segments at 40°C. The purpose of this study was to evaluate the effects of heat on complete antenectomized segments of the antennae. The results in this experiment suggest that bed bugs detect and are attracted to heat modulated by nutritional status. Learning the involvement of antennae segments in heat detection will help identify the location and role of thermoreceptors for bed bug host interaction.
... In addition, despite the importance of heat in bed bug host location and feeding (Rivnay 1932, DeVries et al. 2016, the sensory structures responsible for heat detection have not been characterized. Previous studies on bed bugs have shown that receptors responsible for human odor detection and chemical communication are located in the antennae (Herraca et al. 2010, Herraca et al. 2012, Liu and Liu 2015. Based on morphological assessments of bed bugs (Levinson et al. 1974, Steinbrecht andMuller 1976) and other closely related species (Barrozo et al. 2017), the antenna is likely responsible for heat detection, although this has yet to be shown. ...
... All sensilla can be found in both adult sexes and most are present in nymphs, which indicate that all life stages and both sexes can detect the cues necessary for host location and feeding (Levinson et al. 1974). Among the seven sensilla, porous sensilla (types C, D, and E) are potentially responsible for detecting different cues such as pheromones, odors, and temperature Muller 1976, Liu andLiu 2015). Levinson et al. (1974) showed that type E sensilla are responsible for the detection of alarm pheromones and Herraca et al. (2010) and Liu and Liu (2015) confirmed that D sensilla are responsible for human odorants reception. ...
... Among the seven sensilla, porous sensilla (types C, D, and E) are potentially responsible for detecting different cues such as pheromones, odors, and temperature Muller 1976, Liu andLiu 2015). Levinson et al. (1974) showed that type E sensilla are responsible for the detection of alarm pheromones and Herraca et al. (2010) and Liu and Liu (2015) confirmed that D sensilla are responsible for human odorants reception. It still remains unclear, however, which sensilla are responsible for detecting heat. ...
The common bed bug (Cimex lectularius L.) is an obligate hematophagous ectoparasite that has significant impacts on human health and well-being. All life stages of bed bugs (except eggs) feed solely on blood, which is required to molt and reproduce. Bed bugs use multiple cues to locate their hosts, including heat, CO 2 , and body odors. Of these cues, detection of heat appears limited to a short distance of <3 cm. However, it remains unclear if bed bugs can detect radiant heat, what structure(s) are responsible for heat detection, and if heat detection via the antennae is required for feeding. In this study, bed bug response to radiant heat was evaluated using the two-choice T-maze assay with the heat source either in contact with the surface (i.e., conduction) or not in contact (i.e., radiation) in nonantennectomized bed bugs. Further, we systematically ablated the bed bug's antennal segments (distal tip, first segment, and all four segments) and assessed their responses to heat and feeding in a unique two-choice T-maze assay and individual feeding assays, respectively. Our two-choice assays with contact to or no contact with the surface indicated that bed bugs cannot detect radiant heat. Later, we found that the distal tip of the terminal antennal segment is responsible for orientation toward a heat source. However, >50% of the bed bugs fed even when the entire antenna was removed, suggesting redundancy in sensory cues that drive feeding. These results will be used to better understand the role heat plays in bed bug host attraction and design of traps.
