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Female-induced increase of host-plant volatiles enhance specific attraction of aphid male Dysaphis plantaginea (Homoptera: Aphididae) to the sex pheromone
All aphid species studied so far share the same sex pheromone components, nepetalactol and nepetalactone. Variation by different enantiomers and blends of the two components released by different aphid species are limited and can only partially explain species-specific attraction of males to females...
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Published in: | Bulletin of entomological research 2009-12, Vol.99 (6), p.593-602 |
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creator | van Tol, R.W.H.M. Helsen, H.H.M. Griepink, F.C. de Kogel, W.J. |
description | All aphid species studied so far share the same sex pheromone components, nepetalactol and nepetalactone. Variation by different enantiomers and blends of the two components released by different aphid species are limited and can only partially explain species-specific attraction of males to females. While some host-plant odours are known to enhance specific attraction of aphid species, herbivore-induced plant volatiles that synergise attractiveness to the sex pheromone are unknown. Here, we demonstrate that for the host-alternating rosy apple aphid (Dysaphis plantaginea (Passerini)) specificity of attraction of males to females is triggered by female-induced tree odours in combination with a 1:8 ratio of (4aS,7S,7aR)-nepetalactone and (1R,4aS,7S,7aR)-nepetalactol. Female aphid infestation induces increased release of four esters (hexyl butyrate, (E)-2-hexenyl butyrate, (Z)-3-hexenyl 3-methylbutyrate and hexyl 2-methylbutyrate) from apple leaves. Two different combinations of three esters applied in a 1:1:1 ratio increase the number of male D. plantaginea and decrease the number of other aphid species caught in water traps in the presence of the pheromone components. The ester blend alone was not attractive. Combination of the pheromone blend with each single ester was not increasing attraction of male D. plantaginea. The demonstration that sexual aphid species use herbivore-induced plant volatiles as a species-specific attractant for mate finding adds a new dimension to our understanding of insect species using or manipulating chemical cues of host plants for orientation. |
doi_str_mv | 10.1017/S0007485309006634 |
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Variation by different enantiomers and blends of the two components released by different aphid species are limited and can only partially explain species-specific attraction of males to females. While some host-plant odours are known to enhance specific attraction of aphid species, herbivore-induced plant volatiles that synergise attractiveness to the sex pheromone are unknown. Here, we demonstrate that for the host-alternating rosy apple aphid (Dysaphis plantaginea (Passerini)) specificity of attraction of males to females is triggered by female-induced tree odours in combination with a 1:8 ratio of (4aS,7S,7aR)-nepetalactone and (1R,4aS,7S,7aR)-nepetalactol. Female aphid infestation induces increased release of four esters (hexyl butyrate, (E)-2-hexenyl butyrate, (Z)-3-hexenyl 3-methylbutyrate and hexyl 2-methylbutyrate) from apple leaves. Two different combinations of three esters applied in a 1:1:1 ratio increase the number of male D. plantaginea and decrease the number of other aphid species caught in water traps in the presence of the pheromone components. The ester blend alone was not attractive. Combination of the pheromone blend with each single ester was not increasing attraction of male D. plantaginea. The demonstration that sexual aphid species use herbivore-induced plant volatiles as a species-specific attractant for mate finding adds a new dimension to our understanding of insect species using or manipulating chemical cues of host plants for orientation.</description><identifier>ISSN: 0007-4853</identifier><identifier>EISSN: 1475-2670</identifier><identifier>DOI: 10.1017/S0007485309006634</identifier><identifier>PMID: 19224664</identifier><identifier>CODEN: BEREA2</identifier><language>eng</language><publisher>Cambridge, UK: Cambridge University Press</publisher><subject>Animal and plant ecology ; Animal reproduction ; Animal, plant and microbial ecology ; Animals ; Aphididae ; Aphids - physiology ; Autoecology ; Biological and medical sciences ; cherry-oat aphid ; cryptomyzus ; damson-hop aphid ; Dysaphis ; Dysaphis plantaginea ; Entomology ; Esters ; Female ; Females ; Flowers & plants ; Fundamental and applied biological sciences. Psychology ; Gas Chromatography-Mass Spectrometry ; herbivore-induced plant volatiles ; Homoptera ; Host plants ; Insects ; macrosiphum-euphorbia thomas ; Male ; Malus ; Malus - metabolism ; mate recognition ; megoura-viciae ; olfactory antennal responses ; pheromone ; Pheromones ; phorodon-humuli homoptera ; potato aphid ; Protozoa. Invertebrata ; rhopalosiphum-padi ; rosy apple aphid ; Sex Attractants - physiology ; Sexual Behavior, Animal ; sexual kairomone ; Volatile Organic Compounds - chemistry ; Volatile Organic Compounds - metabolism</subject><ispartof>Bulletin of entomological research, 2009-12, Vol.99 (6), p.593-602</ispartof><rights>Copyright © 2009 Cambridge University Press</rights><rights>2015 INIST-CNRS</rights><rights>Wageningen University & Research</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c521t-40e08725661d8038291ba541694f870db96d22c6bb0c7702ce6baf2a3c544afd3</citedby><cites>FETCH-LOGICAL-c521t-40e08725661d8038291ba541694f870db96d22c6bb0c7702ce6baf2a3c544afd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.cambridge.org/core/product/identifier/S0007485309006634/type/journal_article$$EHTML$$P50$$Gcambridge$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,72832</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=22124928$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19224664$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>van Tol, R.W.H.M.</creatorcontrib><creatorcontrib>Helsen, H.H.M.</creatorcontrib><creatorcontrib>Griepink, F.C.</creatorcontrib><creatorcontrib>de Kogel, W.J.</creatorcontrib><title>Female-induced increase of host-plant volatiles enhance specific attraction of aphid male Dysaphis plantaginea (Homoptera: Aphididae) to the sex pheromone</title><title>Bulletin of entomological research</title><addtitle>Bull. Entomol. Res</addtitle><description>All aphid species studied so far share the same sex pheromone components, nepetalactol and nepetalactone. Variation by different enantiomers and blends of the two components released by different aphid species are limited and can only partially explain species-specific attraction of males to females. While some host-plant odours are known to enhance specific attraction of aphid species, herbivore-induced plant volatiles that synergise attractiveness to the sex pheromone are unknown. Here, we demonstrate that for the host-alternating rosy apple aphid (Dysaphis plantaginea (Passerini)) specificity of attraction of males to females is triggered by female-induced tree odours in combination with a 1:8 ratio of (4aS,7S,7aR)-nepetalactone and (1R,4aS,7S,7aR)-nepetalactol. Female aphid infestation induces increased release of four esters (hexyl butyrate, (E)-2-hexenyl butyrate, (Z)-3-hexenyl 3-methylbutyrate and hexyl 2-methylbutyrate) from apple leaves. Two different combinations of three esters applied in a 1:1:1 ratio increase the number of male D. plantaginea and decrease the number of other aphid species caught in water traps in the presence of the pheromone components. The ester blend alone was not attractive. Combination of the pheromone blend with each single ester was not increasing attraction of male D. plantaginea. The demonstration that sexual aphid species use herbivore-induced plant volatiles as a species-specific attractant for mate finding adds a new dimension to our understanding of insect species using or manipulating chemical cues of host plants for orientation.</description><subject>Animal and plant ecology</subject><subject>Animal reproduction</subject><subject>Animal, plant and microbial ecology</subject><subject>Animals</subject><subject>Aphididae</subject><subject>Aphids - physiology</subject><subject>Autoecology</subject><subject>Biological and medical sciences</subject><subject>cherry-oat aphid</subject><subject>cryptomyzus</subject><subject>damson-hop aphid</subject><subject>Dysaphis</subject><subject>Dysaphis plantaginea</subject><subject>Entomology</subject><subject>Esters</subject><subject>Female</subject><subject>Females</subject><subject>Flowers & plants</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gas Chromatography-Mass Spectrometry</subject><subject>herbivore-induced plant volatiles</subject><subject>Homoptera</subject><subject>Host plants</subject><subject>Insects</subject><subject>macrosiphum-euphorbia thomas</subject><subject>Male</subject><subject>Malus</subject><subject>Malus - metabolism</subject><subject>mate recognition</subject><subject>megoura-viciae</subject><subject>olfactory antennal responses</subject><subject>pheromone</subject><subject>Pheromones</subject><subject>phorodon-humuli homoptera</subject><subject>potato aphid</subject><subject>Protozoa. Invertebrata</subject><subject>rhopalosiphum-padi</subject><subject>rosy apple aphid</subject><subject>Sex Attractants - physiology</subject><subject>Sexual Behavior, Animal</subject><subject>sexual kairomone</subject><subject>Volatile Organic Compounds - chemistry</subject><subject>Volatile Organic Compounds - metabolism</subject><issn>0007-4853</issn><issn>1475-2670</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><recordid>eNp9kstu1DAUhiMEokPhAdggC4nbImA7jp101xbagiohroturBPnZMYlYwc7oe2r8LQ4zEAlEGx8ZJ3v_3VuWXaf0eeMMvXiA6VUiaosaE2plIW4kS2YUGXOpaI3s8Wczuf8TnYnxvP0FbWob2c7rOZcSCkW2fcjXEOPuXXtZLAl1pmAEJH4jqx8HPOhBzeSb76H0fYYCboVOIMkDmhsZw2BcQxgRuvdrIFhZVsyW5KXV3H-RfLTApbWIZCnJ37thxED7JH9mbUt4DMyejKukilekmGFITEO72a3Ougj3tvG3ezT0auPhyf56dvj14f7p7kpORtzQZFWipdSsraiRcVr1kApmKxFVynaNrVsOTeyaahRinKDsoGOQ2FKIaBri91sb-N7AUt01qVHOwjGRu3B6t42AcKVvpiCdv0chqmJuqioUEUSP9mIh-C_ThhHvbbRYJ9aRj9FrQrBeMFlmcjH_yU5S1up5Gz58A_w3E_BpRFoTguWWqiqBLENZIKPMWCnh2DXc52M6vk49F_HkTQPtsZTs8b2WrG9hgQ82gIQDfRdSJtOU_jFcc64SDUmLt9wNo54-TsP4YuWqlCllsfv9MGbA3WmPr_XZ4kvtsXCugm2XeJ1S_8u9weQxeIi</recordid><startdate>20091201</startdate><enddate>20091201</enddate><creator>van Tol, R.W.H.M.</creator><creator>Helsen, H.H.M.</creator><creator>Griepink, F.C.</creator><creator>de Kogel, W.J.</creator><general>Cambridge University Press</general><scope>BSCLL</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T7</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>F1W</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H95</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>L.G</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>QVL</scope></search><sort><creationdate>20091201</creationdate><title>Female-induced increase of host-plant volatiles enhance specific attraction of aphid male Dysaphis plantaginea (Homoptera: Aphididae) to the sex pheromone</title><author>van Tol, R.W.H.M. ; Helsen, H.H.M. ; Griepink, F.C. ; de Kogel, W.J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c521t-40e08725661d8038291ba541694f870db96d22c6bb0c7702ce6baf2a3c544afd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Animal and plant ecology</topic><topic>Animal reproduction</topic><topic>Animal, plant and microbial ecology</topic><topic>Animals</topic><topic>Aphididae</topic><topic>Aphids - physiology</topic><topic>Autoecology</topic><topic>Biological and medical sciences</topic><topic>cherry-oat aphid</topic><topic>cryptomyzus</topic><topic>damson-hop aphid</topic><topic>Dysaphis</topic><topic>Dysaphis plantaginea</topic><topic>Entomology</topic><topic>Esters</topic><topic>Female</topic><topic>Females</topic><topic>Flowers & plants</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gas Chromatography-Mass Spectrometry</topic><topic>herbivore-induced plant volatiles</topic><topic>Homoptera</topic><topic>Host plants</topic><topic>Insects</topic><topic>macrosiphum-euphorbia thomas</topic><topic>Male</topic><topic>Malus</topic><topic>Malus - metabolism</topic><topic>mate recognition</topic><topic>megoura-viciae</topic><topic>olfactory antennal responses</topic><topic>pheromone</topic><topic>Pheromones</topic><topic>phorodon-humuli homoptera</topic><topic>potato aphid</topic><topic>Protozoa. Invertebrata</topic><topic>rhopalosiphum-padi</topic><topic>rosy apple aphid</topic><topic>Sex Attractants - physiology</topic><topic>Sexual Behavior, Animal</topic><topic>sexual kairomone</topic><topic>Volatile Organic Compounds - chemistry</topic><topic>Volatile Organic Compounds - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>van Tol, R.W.H.M.</creatorcontrib><creatorcontrib>Helsen, H.H.M.</creatorcontrib><creatorcontrib>Griepink, F.C.</creatorcontrib><creatorcontrib>de Kogel, W.J.</creatorcontrib><collection>Istex</collection><collection>Pascal-Francis</collection><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>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech 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>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Databases</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</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>Research Library Prep</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Research Library</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Earth, Atmospheric & Aquatic Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>NARCIS:Publications</collection><jtitle>Bulletin of entomological research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>van Tol, R.W.H.M.</au><au>Helsen, H.H.M.</au><au>Griepink, F.C.</au><au>de Kogel, W.J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Female-induced increase of host-plant volatiles enhance specific attraction of aphid male Dysaphis plantaginea (Homoptera: Aphididae) to the sex pheromone</atitle><jtitle>Bulletin of entomological research</jtitle><addtitle>Bull. Entomol. Res</addtitle><date>2009-12-01</date><risdate>2009</risdate><volume>99</volume><issue>6</issue><spage>593</spage><epage>602</epage><pages>593-602</pages><issn>0007-4853</issn><eissn>1475-2670</eissn><coden>BEREA2</coden><abstract>All aphid species studied so far share the same sex pheromone components, nepetalactol and nepetalactone. Variation by different enantiomers and blends of the two components released by different aphid species are limited and can only partially explain species-specific attraction of males to females. While some host-plant odours are known to enhance specific attraction of aphid species, herbivore-induced plant volatiles that synergise attractiveness to the sex pheromone are unknown. Here, we demonstrate that for the host-alternating rosy apple aphid (Dysaphis plantaginea (Passerini)) specificity of attraction of males to females is triggered by female-induced tree odours in combination with a 1:8 ratio of (4aS,7S,7aR)-nepetalactone and (1R,4aS,7S,7aR)-nepetalactol. Female aphid infestation induces increased release of four esters (hexyl butyrate, (E)-2-hexenyl butyrate, (Z)-3-hexenyl 3-methylbutyrate and hexyl 2-methylbutyrate) from apple leaves. Two different combinations of three esters applied in a 1:1:1 ratio increase the number of male D. plantaginea and decrease the number of other aphid species caught in water traps in the presence of the pheromone components. The ester blend alone was not attractive. Combination of the pheromone blend with each single ester was not increasing attraction of male D. plantaginea. The demonstration that sexual aphid species use herbivore-induced plant volatiles as a species-specific attractant for mate finding adds a new dimension to our understanding of insect species using or manipulating chemical cues of host plants for orientation.</abstract><cop>Cambridge, UK</cop><pub>Cambridge University Press</pub><pmid>19224664</pmid><doi>10.1017/S0007485309006634</doi><tpages>10</tpages></addata></record> |
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ispartof | Bulletin of entomological research, 2009-12, Vol.99 (6), p.593-602 |
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source | Cambridge Journals Online |
subjects | Animal and plant ecology Animal reproduction Animal, plant and microbial ecology Animals Aphididae Aphids - physiology Autoecology Biological and medical sciences cherry-oat aphid cryptomyzus damson-hop aphid Dysaphis Dysaphis plantaginea Entomology Esters Female Females Flowers & plants Fundamental and applied biological sciences. Psychology Gas Chromatography-Mass Spectrometry herbivore-induced plant volatiles Homoptera Host plants Insects macrosiphum-euphorbia thomas Male Malus Malus - metabolism mate recognition megoura-viciae olfactory antennal responses pheromone Pheromones phorodon-humuli homoptera potato aphid Protozoa. Invertebrata rhopalosiphum-padi rosy apple aphid Sex Attractants - physiology Sexual Behavior, Animal sexual kairomone Volatile Organic Compounds - chemistry Volatile Organic Compounds - metabolism |
title | Female-induced increase of host-plant volatiles enhance specific attraction of aphid male Dysaphis plantaginea (Homoptera: Aphididae) to the sex pheromone |
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