Diurnal and nocturnal mosquitoes escape looming threats using distinct flight strategies

Cribellier, Antoine; Straw, Andrew; Spitzen, Jeroen; Pieters, R.P.M.; Leeuwen, J.L. van; Muijres, Florian T.

doi:10.1016/j.cub.2022.01.036

Cited by 24 publications

(29 citation statements)

References 60 publications

(74 reference statements)

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“…aegypti lose interest in their hosts [ 13 , 40 , 43 ]. The bar avoidance in our blood-fed group could be a defensive strategy to avoid hosts when the priority is ovipositing, which could be further explored in free-flight assays [ 44 ]. Testing whether mosquitoes recover their bar tracking ability after laying eggs could provide additional evidence that visual attention depends on the female reproductive stage.…”

Section: Discussionmentioning

confidence: 99%

Carbon dioxide and blood-feeding shift visual cue tracking during navigation in Aedes aegypti mosquitoes

et al. 2022

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Haematophagous mosquitoes need a blood meal to complete their reproductive cycle. To accomplish this, female mosquitoes seek vertebrate hosts, land on them and bite. As their eggs mature, they shift attention away from hosts and towards finding sites to lay eggs. We asked whether females were more tuned to visual cues when a host-related signal, carbon dioxide, was present, and further examined the effect of a blood meal, which shifts behaviour to ovipositing. Using a custom, tethered-flight arena that records wing stroke changes while displaying visual cues, we found the presence of carbon dioxide enhances visual attention towards discrete stimuli and improves contrast sensitivity for host-seeking Aedes aegypti mosquitoes. Conversely, intake of a blood meal reverses vertical bar tracking, a stimulus that non-fed females readily follow. This switch in behaviour suggests that having a blood meal modulates visual attention in mosquitoes, a phenomenon that has been described before in olfaction but not in visually driven behaviours.

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Section: Discussionmentioning

confidence: 99%

Carbon dioxide and blood-feeding shift visual cue tracking during navigation in Aedes aegypti mosquitoes

et al. 2022

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“…In contrast to pheromone tracking in male moths, which is mostly limited to the horizontal plane (Cardé, 2021), mosquitoes zigzag in both horizontal and vertical crosswind direction . While this basic cast-and-surge host-seeking mechanism is common to all mosquito species, details may vary speciesspecifically, e.g., due to differences in host spectrum, light conditions during the circadian host-seeking peak, or weighing of the input of other sensory modalities (e.g., Klowden, 2007b;Cribellier et al, 2022).…”

Section: Odour-mediated Optomotor Anemotaxis: Cast-and-surgementioning

confidence: 99%

“…The 3D tracking of mosquito flight has been used to, e.g., understand the host-seeking mechanism of different mosquito species, the integration of other modalities, escape dynamics, as well as to optimise mosquito control methods, such as baited traps and insecticide-treated nets Lacey and Cardé, 2011;Spitzen et al, 2013Spitzen et al, , 2014McMeniman et al, 2014;Parker et al, 2015;van Breugel et al, 2015;Angarita-Jaimes et al, 2016;Cribellier et al, , 2022Amos et al, 2020). The recently established wind tunnel setup, 3D tracking and custom analysis pipeline allows for the study of different aspects of mosquito host seeking by analysing their flight manoeuvres in a climate-controlled environment in the absence of odour contamination by the observer (figure 1; paper I / Hinze et al, 2021).…”

Section: Tracking and Analysing Mosquito Flightmentioning

confidence: 99%

Odour-mediated host seeking and discrimination in mosquitoes : chemistry, neurobiology and behaviour

Hinze¹

2022

Acta Universitatis Agriculturae Sueciae

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The majority of the world’s population is at risk of one or more mosquito-borne diseases that are transmitted by blood-feeding female mosquitoes, affecting both human health and economic development. Especially Anopheles gambiae, the principal malaria vector, and Aedes aegypti, the vector of dengue and yellow fever, are of primary concern due to their strong specialisation on human hosts, and the high number of casualties caused by the pathogens they transmit. Host seeking and discrimination are crucial for disease transmission, and are predominantly mediated by olfaction. Using a wind tunnel system and a custom analysis pipeline, this thesis confirms that the two mosquito species use volatile host cues, derived from breath and body, differentially, as carbon dioxide on its own drives host seeking in Ae. aegypti, but not in An. gambiae (paper I). To discriminate between host and nonhost species (paper V), Ae. aegypti encode human identity by the relative activation of two glomeruli within the antennal lobe, the primary olfactory centre, of which one is tuned to long-chain aldehydes enriched in human odour. A synthetic blend mimicking the glomerular activation elicited host seeking in Ae. aegypti (paper II). Next to preferring human over non-human hosts, Ae. aegypti also prefer some human individuals to others, which was demonstrated to be affected by the ABO blood type and pregnancy or menstrual cycle phase. Analysis of the volatiles associated with individual volunteers, identified 1-octen-3-ol to be significantly associated with very high attractiveness (paper III). The molecular regulation of host seeking acquisition during An. gambiae female adult maturation was independent of odorant receptor gene AgamOR39 expression (paper IV). The results presented in this thesis contribute to the understanding of mosquito host seeking and discrimination from multiple perspectives, which is a prerequisite to ultimately develop novel tools for mosquito monitoring and control.

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“…In free flight, both Ae. aegypti and the nocturnal malaria vector Anopheles coluzzii , displayed rapid escape maneuvers when stimulated with an artificial swatter that induces both airflow and visual cues 22 , 23 , hinting at the role of visual cues in signaling threats. Furthermore, some mosquito species display a “pre-biting” rest 24 or “pre-attack” resting 25 behavior when the mosquito density increases around a target host 26 , which is known to heighten host defensive behaviors 27 , 28 .…”

Section: Introductionmentioning

confidence: 99%

Visual threats reduce blood-feeding and trigger escape responses in Aedes aegypti mosquitoes

Wynne

Chandrasegaran

Fryzlewicz

et al. 2022

Sci Rep

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The diurnal mosquitoes Aedes aegypti are vectors of several arboviruses, including dengue, yellow fever, and Zika viruses. To find a host to feed on, they rely on the sophisticated integration of olfactory, visual, thermal, and gustatory cues emitted by the hosts. If detected by their target, this latter may display defensive behaviors that mosquitoes need to be able to detect and escape in order to survive. In humans, a typical response is a swat of the hand, which generates both mechanical and visual perturbations aimed at a mosquito. Here, we used programmable visual displays to generate expanding objects sharing characteristics with the visual component of an approaching hand and quantified the behavioral response of female mosquitoes. Results show that Ae. aegypti is capable of using visual information to decide whether to feed on an artificial host mimic. Stimulations delivered in a LED flight arena further reveal that landed Ae. aegypti females display a stereotypical escape strategy by taking off at an angle that is a function of the direction of stimulus introduction. Altogether, this study demonstrates that mosquitoes landed on a host mimic can use isolated visual cues to detect and avoid a potential threat.

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Diurnal and nocturnal mosquitoes escape looming threats using distinct flight strategies

Cited by 24 publications

References 60 publications

Carbon dioxide and blood-feeding shift visual cue tracking during navigation in Aedes aegypti mosquitoes

Carbon dioxide and blood-feeding shift visual cue tracking during navigation in Aedes aegypti mosquitoes

Odour-mediated host seeking and discrimination in mosquitoes : chemistry, neurobiology and behaviour

Visual threats reduce blood-feeding and trigger escape responses in Aedes aegypti mosquitoes

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