Abstract 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.
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Bed Bug (Hemiptera: Cimicidae) Attraction to Human Odors: Validation of a Two-Choice Olfactometer
Abstract Bed bugs (Cimex lectularius L.) (Hemiptera: Cimicidae) are obligate hematophagous ectoparasites, and, therefore, must locate suitable hosts to ensure survival and reproduction. Their largely nocturnal activity suggests that chemosensory and thermosensory cues would play critical roles in host location. Yet, the importance of olfaction in host attraction of bed bugs remains unclear. We developed and validated a Y-tube, two-choice olfactometer and tested its suitability for investigating attraction to human odors (from skin swabs). Olfactometer orientation significantly affected the percentage of bed bugs that were activated by human odors, with significantly more bed bugs responding when the olfactometer was oriented vertically (bug introduced at bottom of the olfactometer) compared with all other orientations. Starved (7–10 d) adult males, mated females, and nymphs responded (47–77% moved up the olfactometer and made a choice) when human odors were present in the olfactometer, while starved, unmated females did not respond. Skin swabs from all five human participants elicited high response rates (65–82%), and bed bugs from four different populations responded to skin swabs (40–82% response rate). However, in all assays including those resulting in relatively low response rates, bed bugs exhibited >90% preference for human odors over blank controls. These results provide strong evidence that bed bugs can respond and orient towards human odors, independently of all other host cues. Furthermore, the validated olfactometer should enable rapid and efficient evaluations of bed bug behavioral responses to semiochemicals.
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- Award ID(s):
- 1754190
- NSF-PAR ID:
- 10160596
- Date Published:
- Journal Name:
- Journal of Medical Entomology
- Volume:
- 56
- Issue:
- 2
- ISSN:
- 0022-2585
- Page Range / eLocation ID:
- 362 to 367
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Reproductive fitness and survival are enhanced by adaptive behaviors that are modulated by internal physiological states and external social contexts. The common bed bug,
Cimex lectularius , is an obligate hematophagous ectoparasite that requires host blood for growth, development, and reproduction. We investigated how mating, starvation and social interactions affect host-seeking, blood feeding, oviposition, and survival of female bed bugs. The percentage of females that fed and the amount of blood they ingested were greater in mated females (90–100%) than in unmated females (48–60%). Mating state also modulated the female’s orientation towards human skin odor in an olfactometer; more mated (69%) than unmated (23%) females responded to human odors. The response rate of unmated females (60%) to skin odor increased with longer starvation period, while the opposite pattern was observed in mated females (20%). Although fecundity after a single blood meal was unaffected by long or short residence and interaction with males, females subjected to frequent copulation attempts had lower survivorship and lifespan than females housed with males for only 24 h. Taken together, these results indicate that by adaptively and coordinately expressing behaviors based on the internal physiological state, females maximize their survival and reproductive fitness. -
Appel, Arthur (Ed.)Abstract 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, CO2, 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.more » « less
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Abstract Background Widespread vector control has been essential in reducing the global incidence and prevalence of malaria, despite now stalled progress. Long-lasting insecticide-treated nets (LLINs) have historically been, and remain, one of the most commonly used vector control tools in the campaign against malaria. LLINs are effective only with proper use, adherence, retention and community adoption, which historically have relied on the successful control of secondary pests, including bed bugs. The emergence of pyrethroid-resistant bed bugs in malaria-endemic communities and failure to control infestations have been suggested to interfere with the effective use of LLINs. Therefore, the behavioral interactions of bed bugs with commonly used bed nets should be better understood.
Methods To investigate the interactions between bed bugs (
Cimex lectularius L.) and LLINs, insecticide-susceptible and pyrethroid-resistant bed bugs were challenged to pass through two commonly used LLINs in two behavioral assays, namely host (blood meal)-seeking and aggregation-seeking assays. The proportions blood-fed and aggregated bed bugs, aggregation time and mortality were quantified and analyzed in different bed bug life stages.Results Overall, both the insecticide-susceptible bed bugs and highly resistant bed bugs showed a varying ability to pass through LLINs based on treatment status and net design. Deltamethrin-treated nets significantly impeded both feeding and aggregation by the susceptible bed bugs. While none of the tested LLINs significantly impeded feeding (passage of unfed bed bugs through the nets) of the pyrethroid-resistant bed bugs, the untreated bed net, which has small mesh holes, impeded passage of fed bed bugs. Mortality was only seen in the susceptible bed bugs, with significantly higher mortality on deltamethrin-treated nets (63.5 ± 10.7%) than on permethrin-treated nets (2.0 ± 0.9%).
Conclusions Commonly used new LLINs failed to prevent the passage of susceptible and pyrethroid-resistant bed bugs in host- and aggregation-seeking bioassays. The overall low and variable mortality observed in susceptible bed bugs during both assays highlighted the potential of LLINs to impose strong selection pressure for the evolution of pyrethroid resistance. Already, the failure to control bed bug infestations has been implicated as a contributing factor to the abandonment or misuse of LLINs. For the first time to our knowledge, we have shown the potential of LLINs in selecting for resistant secondary pest populations and so their potential role in stalling malaria control programs should be further investigated.
Graphical Abstract The emergence of pyrethroid-resistant bed bugs in malaria-endemic communities may interfere with the effective use of pyrethroid-impregnated bed nets. We assessed the interactions of two bed bug strains with commonly used bed nets using two behavioral assays, namely host (blood meal)-seeking by unfed bed bugs and aggregation-seeking by freshly fed bed bugs. These assays assessed the passage of bed bugs through various bed nets in response to host cues and aggregation stimuli, respectively. Conditioned paper is a section of file folder paper that has been exposed to bed bugs and has been impregnated with feces and aggregation pheromone; it is attractive to aggregation-seeking fed bed bugs. An unconditioned ramp is a similar section of file folder paper that allows bed bugs to traverse the bed net and gain access to a blood-meal source.
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Abstract As populations differentiate across geographic or host‐association barriers, interpopulation fertility is often a measure of the extent of incipient speciation. The bed bug,
Cimex lectularius L., was recently found to form two host‐associated lineages within Europe: one found with humans (human‐associated, HA) and the other found with bats (bat‐associated, BA). No unequivocal evidence of contemporary gene flow between these lineages has been found; however, it is unclear whether this is due to an inability to produce viable “hybrid” offspring. To address this question and determine the extent of compatibility between host‐associated lineages, we set up mating crosses among populations of bed bugs based on both their host association (human—HA vs. bat—BA) and geographic origin (North America vs. Europe). Within‐population fecundity was significantly higher for all HA populations (>1.7 eggs/day) than for BA populations (<1 egg/day). However, all within‐population crosses, regardless of host association, had >92% egg hatch rates. Contrary to previous reports, in all interlineage crosses, successful matings occurred, fertile eggs were oviposited, and the F1“hybrid” generation was found to be reproductively viable. In addition, we evaluated interpopulation genetic variation inWolbachia among host‐associated lineages. We did not find any clear patterns related to host association, nor did we observe a homogenization ofWolbachia lineages across populations that might explain a breakdown of reproductive incompatibility. These results indicate that while the HA and BA populations ofC. lectularius represent genetically differentiated host‐associated lineages, possibly undergoing sympatric speciation, this is in its incipient stage as they remain reproductively compatible. Other behavioral, physiological, and/or ecological factors likely maintain host‐associated differentiation.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/jme/tjy202
