Mosquitoes Use Vision to Associate Odor Plumes with Thermal Targets

感觉线索 吸引力 生物 感觉系统 气味 羽流 神经科学 计算机视觉 计算机科学 物理 语言学 热力学 哲学
作者
Floris van Breugel,Jeff Riffell,Adrienne L. Fairhall,Michael H. Dickinson
出处
期刊:Current Biology [Elsevier BV]
卷期号:25 (16): 2123-2129 被引量:272
标识
DOI:10.1016/j.cub.2015.06.046
摘要

All moving animals, including flies [1van Breugel F. Dickinson M.H. Plume-tracking behavior of flying Drosophila emerges from a set of distinct sensory-motor reflexes.Curr. Biol. 2014; 24: 274-286Abstract Full Text Full Text PDF PubMed Scopus (124) Google Scholar, 2Budick S.A. Dickinson M.H. Free-flight responses of Drosophila melanogaster to attractive odors.J. Exp. Biol. 2006; 209: 3001-3017Crossref PubMed Scopus (158) Google Scholar, 3Barrows W.M. The reactions of the Pomace fly, Drosophila ampelophila loew, to odorous substances.J. Exp. Zool. 1907; 4: 515-537Crossref Scopus (75) Google Scholar], sharks [4Johnsen P.B. Teeter J.H. Behavioral responses of bonnethead sharks (Sphyrna tiburo) to controlled olfactory stimulation.Mar. Freshwat. Behav. Physiol. 1985; 11: 283-291Crossref Google Scholar], and humans [5Porter J. Craven B. Khan R.M. Chang S.-J. Kang I. Judkewitz B. Volpe J. Settles G. Sobel N. Mechanisms of scent-tracking in humans.Nat. Neurosci. 2007; 10: 27-29Crossref PubMed Scopus (233) Google Scholar], experience a dynamic sensory landscape that is a function of both their trajectory through space and the distribution of stimuli in the environment. This is particularly apparent for mosquitoes, which use a combination of olfactory, visual, and thermal cues to locate hosts [6McMeniman C.J. Corfas R.A. Matthews B.J. Ritchie S.A. Vosshall L.B. Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans.Cell. 2014; 156: 1060-1071Abstract Full Text Full Text PDF PubMed Scopus (259) Google Scholar, 7Ditzen M. Pellegrino M. Vosshall L.B. Insect odorant receptors are molecular targets of the insect repellent DEET.Science. 2008; 319: 1838-1842Crossref PubMed Scopus (257) Google Scholar, 8DeGennaro M. McBride C.S. Seeholzer L. Nakagawa T. Dennis E.J. Goldman C. Jasinskiene N. James A.A. Vosshall L.B. orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET.Nature. 2013; 498: 487-491Crossref PubMed Scopus (266) Google Scholar, 9Turner S.L. Li N. Guda T. Githure J. Cardé R.T. Ray A. Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes.Nature. 2011; 474: 87-91Crossref PubMed Scopus (122) Google Scholar, 10Bidlingmayer W.L. How mosquitoes see traps: role of visual responses.J. Am. Mosq. Control Assoc. 1994; 10: 272-279PubMed Google Scholar]. Mosquitoes are thought to detect suitable hosts by the presence of a sparse CO2 plume, which they track by surging upwind and casting crosswind [11Dekker T. Cardé R.T. Moment-to-moment flight manoeuvres of the female yellow fever mosquito (Aedes aegypti L.) in response to plumes of carbon dioxide and human skin odour.J. Exp. Biol. 2011; 214: 3480-3494Crossref PubMed Scopus (67) Google Scholar]. Upon approach, local cues such as heat and skin volatiles help them identify a landing site [12Eiras A.E. Jepson P.C. Responses of female Aedes aegypti (Diptera: Culicidae) to host odours and convection currents using an olfactometer bioassay.Bull. Entomol. Res. 1994; 84: 207-211Crossref Scopus (54) Google Scholar, 13Davis E. Sokolove P. Temperature responses of antennal receptors of the mosquito, Aedes aegypti.J. Comp. Physiol. 1975; 96: 223-236Crossref Scopus (70) Google Scholar, 14Wang G. Qiu Y.T. Lu T. Kwon H.-W. Pitts R.J. Van Loon J.J. Takken W. Zwiebel L.J. Anopheles gambiae TRPA1 is a heat-activated channel expressed in thermosensitive sensilla of female antennae.Eur. J. Neurosci. 2009; 30: 967-974Crossref PubMed Scopus (72) Google Scholar, 15Lacey E.S. Ray A. Cardé R.T. Close encounters: contributions of carbon dioxide and human skin odour to finding and landing on a host in Aedes aegypti.Physiol. Entomol. 2014; 39: 60-68Crossref PubMed Scopus (33) Google Scholar]. Recent evidence suggests that thermal attraction is gated by the presence of CO2 [6McMeniman C.J. Corfas R.A. Matthews B.J. Ritchie S.A. Vosshall L.B. Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans.Cell. 2014; 156: 1060-1071Abstract Full Text Full Text PDF PubMed Scopus (259) Google Scholar], although this conclusion was based experiments in which the actual flight trajectories of the animals were unknown and visual cues were not studied. Using a three-dimensional tracking system, we show that rather than gating heat sensing, the detection of CO2 actually activates a strong attraction to visual features. This visual reflex guides the mosquitoes to potential hosts where they are close enough to detect thermal cues. By experimentally decoupling the olfactory, visual, and thermal cues, we show that the motor reactions to these stimuli are independently controlled. Given that humans become visible to mosquitoes at a distance of 5–15 m [16Bidlingmayer W.L. Hem D.G. The range of visual attraction and the effect of competitive visual attractants upon mosquito (Diptera: Culicidae) flight.Bull. Entomol. Res. 1980; 70: 321-342Crossref Scopus (38) Google Scholar], visual cues play a critical intermediate role in host localization by coupling long-range plume tracking to behaviors that require short-range cues. Rather than direct neural coupling, the separate sensory-motor reflexes are linked as a result of the interaction between the animal’s reactions and the spatial structure of the stimuli in the environment.
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