Hold your breath - Differential behavioral and sensory acuity of mosquitoes to acetone and carbon dioxide
Host seeking in the yellow fever mosquito, Aedes aegypti, and the African malaria mosquito, Anopheles coluzzii, relies on specific and generic host-derived odorants. Previous analyses indicate that the behavioral response of these species depends differentially on the presence of carbon dioxide (CO2...
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description | Host seeking in the yellow fever mosquito, Aedes aegypti, and the African malaria mosquito, Anopheles coluzzii, relies on specific and generic host-derived odorants. Previous analyses indicate that the behavioral response of these species depends differentially on the presence of carbon dioxide (CO2) and other constituents in human breath for activation and attraction. In this study, we use a flight tube assay and electrophysiological analysis to assess the role of acetone, a major component of exhaled human breath, in modulating the behavioral and sensory neuronal response of these mosquito species, in the presence and absence of CO2. When presented alone at ecologically relevant concentrations, acetone increases attraction in Ae. aegypti, but not in An. coluzzii. Moreover, in combination with CO2, human breath-equivalents of acetone ranging between 0.1 and 10 ppm reproduces a behavioral response similar to that observed to human breath in host-seeking Ae. aegypti, but not in An. coluzzii. Acetone does, however, reduce attraction to CO2 in An. coluzzii, when presented at a higher concentration of 10 ppm. We identify the capitate peg A neuron of the maxillary palp of both species as a dual detector of CO2 and acetone. The sensory response to acetone, or binary blends of acetone and CO2, reflects the observed behavioral output in both Ae. aegypti and An. coluzzii. We conclude that host recognition is contextual and dependent on a combination of ecologically relevant odorants at naturally occurring concentrations that are encoded, in this case, by differences in the temporal structure of the neuronal response. This information should be considered when designing synthetic blends for that optimally attract mosquitoes for monitoring and control. |
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Previous analyses indicate that the behavioral response of these species depends differentially on the presence of carbon dioxide (CO2) and other constituents in human breath for activation and attraction. In this study, we use a flight tube assay and electrophysiological analysis to assess the role of acetone, a major component of exhaled human breath, in modulating the behavioral and sensory neuronal response of these mosquito species, in the presence and absence of CO2. When presented alone at ecologically relevant concentrations, acetone increases attraction in Ae. aegypti, but not in An. coluzzii. Moreover, in combination with CO2, human breath-equivalents of acetone ranging between 0.1 and 10 ppm reproduces a behavioral response similar to that observed to human breath in host-seeking Ae. aegypti, but not in An. coluzzii. Acetone does, however, reduce attraction to CO2 in An. coluzzii, when presented at a higher concentration of 10 ppm. We identify the capitate peg A neuron of the maxillary palp of both species as a dual detector of CO2 and acetone. The sensory response to acetone, or binary blends of acetone and CO2, reflects the observed behavioral output in both Ae. aegypti and An. coluzzii. We conclude that host recognition is contextual and dependent on a combination of ecologically relevant odorants at naturally occurring concentrations that are encoded, in this case, by differences in the temporal structure of the neuronal response. This information should be considered when designing synthetic blends for that optimally attract mosquitoes for monitoring and control.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0226815</identifier><identifier>PMID: 31887129</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acetone ; Acetone - pharmacology ; Acuity ; Aedes - physiology ; Aedes aegypti ; Animals ; Anopheles - physiology ; Aquatic insects ; Aroma compounds ; Attraction ; Behavior ; Behavior, Animal - drug effects ; Bioassays ; Biological assays ; Biology ; Biology and Life Sciences ; Carbon dioxide ; Carbon Dioxide - pharmacology ; Chemical ecology ; Culicidae ; Culicidae - physiology ; Disease ; Earth Sciences ; Ecology and Environmental Sciences ; Entomology ; Exhalation ; Experiments ; Host-Seeking Behavior - drug effects ; Human behavior ; Humans ; Malaria ; Malaria - transmission ; Medicine and Health Sciences ; Mosquitoes ; Odorants ; Physical Sciences ; Polymer blends ; Smell ; Social Sciences ; Species ; Tropical diseases ; Vector-borne diseases ; Yellow fever ; Yellow Fever - transmission</subject><ispartof>PloS one, 2019-12, Vol.14 (12), p.e0226815-e0226815</ispartof><rights>2019 Ghaninia et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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This information should be considered when designing synthetic blends for that optimally attract mosquitoes for monitoring and control.</description><subject>Acetone</subject><subject>Acetone - pharmacology</subject><subject>Acuity</subject><subject>Aedes - physiology</subject><subject>Aedes aegypti</subject><subject>Animals</subject><subject>Anopheles - physiology</subject><subject>Aquatic insects</subject><subject>Aroma compounds</subject><subject>Attraction</subject><subject>Behavior</subject><subject>Behavior, Animal - drug effects</subject><subject>Bioassays</subject><subject>Biological assays</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Carbon dioxide</subject><subject>Carbon Dioxide - pharmacology</subject><subject>Chemical ecology</subject><subject>Culicidae</subject><subject>Culicidae - physiology</subject><subject>Disease</subject><subject>Earth Sciences</subject><subject>Ecology and Environmental Sciences</subject><subject>Entomology</subject><subject>Exhalation</subject><subject>Experiments</subject><subject>Host-Seeking Behavior - 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Differential behavioral and sensory acuity of mosquitoes to acetone and carbon dioxide</title><author>Ghaninia, Majid ; Majeed, Shahid ; Dekker, Teun ; Hill, Sharon R ; Ignell, Rickard</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-9fa35865339e0c6fe076bcf354b91536b609625c8373abdcf791d3837f015cc63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Acetone</topic><topic>Acetone - pharmacology</topic><topic>Acuity</topic><topic>Aedes - physiology</topic><topic>Aedes aegypti</topic><topic>Animals</topic><topic>Anopheles - physiology</topic><topic>Aquatic insects</topic><topic>Aroma compounds</topic><topic>Attraction</topic><topic>Behavior</topic><topic>Behavior, Animal - drug effects</topic><topic>Bioassays</topic><topic>Biological assays</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Carbon dioxide</topic><topic>Carbon Dioxide - pharmacology</topic><topic>Chemical ecology</topic><topic>Culicidae</topic><topic>Culicidae - physiology</topic><topic>Disease</topic><topic>Earth Sciences</topic><topic>Ecology and Environmental Sciences</topic><topic>Entomology</topic><topic>Exhalation</topic><topic>Experiments</topic><topic>Host-Seeking Behavior - drug effects</topic><topic>Human behavior</topic><topic>Humans</topic><topic>Malaria</topic><topic>Malaria - transmission</topic><topic>Medicine and Health Sciences</topic><topic>Mosquitoes</topic><topic>Odorants</topic><topic>Physical Sciences</topic><topic>Polymer blends</topic><topic>Smell</topic><topic>Social Sciences</topic><topic>Species</topic><topic>Tropical diseases</topic><topic>Vector-borne diseases</topic><topic>Yellow fever</topic><topic>Yellow Fever - transmission</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ghaninia, Majid</creatorcontrib><creatorcontrib>Majeed, Shahid</creatorcontrib><creatorcontrib>Dekker, Teun</creatorcontrib><creatorcontrib>Hill, Sharon R</creatorcontrib><creatorcontrib>Ignell, Rickard</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ghaninia, Majid</au><au>Majeed, Shahid</au><au>Dekker, Teun</au><au>Hill, Sharon R</au><au>Ignell, Rickard</au><au>Dickens, Joseph Clifton</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Hold your breath - Differential behavioral and sensory acuity of mosquitoes to acetone and carbon dioxide</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2019-12-30</date><risdate>2019</risdate><volume>14</volume><issue>12</issue><spage>e0226815</spage><epage>e0226815</epage><pages>e0226815-e0226815</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Host seeking in the yellow fever mosquito, Aedes aegypti, and the African malaria mosquito, Anopheles coluzzii, relies on specific and generic host-derived odorants. Previous analyses indicate that the behavioral response of these species depends differentially on the presence of carbon dioxide (CO2) and other constituents in human breath for activation and attraction. In this study, we use a flight tube assay and electrophysiological analysis to assess the role of acetone, a major component of exhaled human breath, in modulating the behavioral and sensory neuronal response of these mosquito species, in the presence and absence of CO2. When presented alone at ecologically relevant concentrations, acetone increases attraction in Ae. aegypti, but not in An. coluzzii. Moreover, in combination with CO2, human breath-equivalents of acetone ranging between 0.1 and 10 ppm reproduces a behavioral response similar to that observed to human breath in host-seeking Ae. aegypti, but not in An. coluzzii. Acetone does, however, reduce attraction to CO2 in An. coluzzii, when presented at a higher concentration of 10 ppm. We identify the capitate peg A neuron of the maxillary palp of both species as a dual detector of CO2 and acetone. The sensory response to acetone, or binary blends of acetone and CO2, reflects the observed behavioral output in both Ae. aegypti and An. coluzzii. We conclude that host recognition is contextual and dependent on a combination of ecologically relevant odorants at naturally occurring concentrations that are encoded, in this case, by differences in the temporal structure of the neuronal response. This information should be considered when designing synthetic blends for that optimally attract mosquitoes for monitoring and control.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31887129</pmid><doi>10.1371/journal.pone.0226815</doi><orcidid>https://orcid.org/0000-0002-4607-5986</orcidid><orcidid>https://orcid.org/0000-0002-6474-0214</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acetone Acetone - pharmacology Acuity Aedes - physiology Aedes aegypti Animals Anopheles - physiology Aquatic insects Aroma compounds Attraction Behavior Behavior, Animal - drug effects Bioassays Biological assays Biology Biology and Life Sciences Carbon dioxide Carbon Dioxide - pharmacology Chemical ecology Culicidae Culicidae - physiology Disease Earth Sciences Ecology and Environmental Sciences Entomology Exhalation Experiments Host-Seeking Behavior - drug effects Human behavior Humans Malaria Malaria - transmission Medicine and Health Sciences Mosquitoes Odorants Physical Sciences Polymer blends Smell Social Sciences Species Tropical diseases Vector-borne diseases Yellow fever Yellow Fever - transmission |
title | Hold your breath - Differential behavioral and sensory acuity of mosquitoes to acetone and carbon dioxide |
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