Loading…

Larval defense against attack from parasitoid wasps requires nociceptive neurons

Parasitoid wasps are a fierce predator of Drosophila larvae. Female Leptopilina boulardi (LB) wasps use a sharp ovipositor to inject eggs into the bodies of Drosophila melanogaster larvae. The wasp then eats the Drosophila larva alive from the inside, and an adult wasp ecloses from the Drosophila pu...

Full description

Saved in:
Bibliographic Details
Published in:PloS one 2013-10, Vol.8 (10), p.e78704-e78704
Main Authors: Robertson, Jessica L, Tsubouchi, Asako, Tracey, W Daniel
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c526t-e100f76f12a553d340c696efd3d3214655e4daa301e5ee497415f29bfedc3bc63
cites cdi_FETCH-LOGICAL-c526t-e100f76f12a553d340c696efd3d3214655e4daa301e5ee497415f29bfedc3bc63
container_end_page e78704
container_issue 10
container_start_page e78704
container_title PloS one
container_volume 8
creator Robertson, Jessica L
Tsubouchi, Asako
Tracey, W Daniel
description Parasitoid wasps are a fierce predator of Drosophila larvae. Female Leptopilina boulardi (LB) wasps use a sharp ovipositor to inject eggs into the bodies of Drosophila melanogaster larvae. The wasp then eats the Drosophila larva alive from the inside, and an adult wasp ecloses from the Drosophila pupal case instead of a fly. However, the Drosophila larvae are not defenseless as they may resist the attack of the wasps through somatosensory-triggered behavioral responses. Here we describe the full range of behaviors performed by the larval prey in immediate response to attacks by the wasps. Our results suggest that Drosophila larvae primarily sense the wasps using their mechanosensory systems. The range of behavioral responses included both "gentle touch" like responses as well as nociceptive responses. We found that the precise larval response depended on both the somatotopic location of the attack, and whether or not the larval cuticle was successfully penetrated during the course of the attack. Interestingly, nociceptive responses are more likely to be triggered by attacks in which the cuticle had been successfully penetrated by the wasp. Finally, we found that the class IV neurons, which are necessary for mechanical nociception, were also necessary for a nociceptive response to wasp attacks. Thus, the class IV neurons allow for a nociceptive behavioral response to a naturally occurring predator of Drosophila.
doi_str_mv 10.1371/journal.pone.0078704
format article
fullrecord <record><control><sourceid>proquest_plos_</sourceid><recordid>TN_cdi_plos_journals_1445923144</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><doaj_id>oai_doaj_org_article_712d099f75ce4fcdb3ed2658726f8a01</doaj_id><sourcerecordid>1449765797</sourcerecordid><originalsourceid>FETCH-LOGICAL-c526t-e100f76f12a553d340c696efd3d3214655e4daa301e5ee497415f29bfedc3bc63</originalsourceid><addsrcrecordid>eNptUk1vEzEQXSEQLYV_gGAlLlwS_O31BQlVBSpFggOcrYk9Dg4be2vvBvHvu23SqkWcZjR-7_nN6DXNa0qWlGv6YZunkqBfDjnhkhDdaSKeNKfUcLZQjPCnD_qT5kWtW0Ik75R63pwwwYhkRp8231dQ9tC3HgOmii1sIKY6tjCO4H63oeRdO0CBGsccffsH6lDbgldTLFjblF10OIxxj23CqeRUXzbPAvQVXx3rWfPz88WP86-L1bcvl-efVgsnmRoXSAkJWgXKQEruuSBOGYXBzz2jQkmJwgNwQlEiCqMFlYGZdUDv-Nopfta8PegOfa72eIxqqRDSMD6XGXF5QPgMWzuUuIPy12aI9naQy8ZCGaPr0WrKPDEmaOlQBOfXHD1TstNMhQ4InbU-Hn-b1rvZAqaxQP9I9PFLir_sJu8t70jHOjkLvD8KlHw1YR3tLlaHfQ8J83Tr22gltdEz9N0_0P9vJw4oV3KtBcO9GUrsTUDuWPYmIPYYkJn25uEi96S7RPBrTjy6iA</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1445923144</pqid></control><display><type>article</type><title>Larval defense against attack from parasitoid wasps requires nociceptive neurons</title><source>Publicly Available Content Database</source><source>PubMed Central</source><creator>Robertson, Jessica L ; Tsubouchi, Asako ; Tracey, W Daniel</creator><contributor>Skoulakis, Efthimios M. C.</contributor><creatorcontrib>Robertson, Jessica L ; Tsubouchi, Asako ; Tracey, W Daniel ; Skoulakis, Efthimios M. C.</creatorcontrib><description>Parasitoid wasps are a fierce predator of Drosophila larvae. Female Leptopilina boulardi (LB) wasps use a sharp ovipositor to inject eggs into the bodies of Drosophila melanogaster larvae. The wasp then eats the Drosophila larva alive from the inside, and an adult wasp ecloses from the Drosophila pupal case instead of a fly. However, the Drosophila larvae are not defenseless as they may resist the attack of the wasps through somatosensory-triggered behavioral responses. Here we describe the full range of behaviors performed by the larval prey in immediate response to attacks by the wasps. Our results suggest that Drosophila larvae primarily sense the wasps using their mechanosensory systems. The range of behavioral responses included both "gentle touch" like responses as well as nociceptive responses. We found that the precise larval response depended on both the somatotopic location of the attack, and whether or not the larval cuticle was successfully penetrated during the course of the attack. Interestingly, nociceptive responses are more likely to be triggered by attacks in which the cuticle had been successfully penetrated by the wasp. Finally, we found that the class IV neurons, which are necessary for mechanical nociception, were also necessary for a nociceptive response to wasp attacks. Thus, the class IV neurons allow for a nociceptive behavioral response to a naturally occurring predator of Drosophila.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0078704</identifier><identifier>PMID: 24205297</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Anesthesiology ; Animal behavior ; Animals ; Drosophila ; Drosophila melanogaster ; Drosophila melanogaster - cytology ; Drosophila melanogaster - parasitology ; Drosophila melanogaster - physiology ; Eggs ; Escape Reaction - physiology ; Female ; Host-Parasite Interactions ; Hymenoptera ; Insects ; Larva - cytology ; Larva - parasitology ; Larva - physiology ; Larvae ; Leptopilina boulardi ; Locomotion - physiology ; Male ; Neurons ; Neurosciences ; Nociceptors - cytology ; Ovipositor ; Pain perception ; Parasitoids ; Prey ; Wasps - physiology</subject><ispartof>PloS one, 2013-10, Vol.8 (10), p.e78704-e78704</ispartof><rights>2013 Robertson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Robertson et al 2013 Robertson et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-e100f76f12a553d340c696efd3d3214655e4daa301e5ee497415f29bfedc3bc63</citedby><cites>FETCH-LOGICAL-c526t-e100f76f12a553d340c696efd3d3214655e4daa301e5ee497415f29bfedc3bc63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1445923144/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1445923144?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,315,733,786,790,891,25783,27957,27958,37047,37048,44625,53827,53829,75483</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24205297$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Skoulakis, Efthimios M. C.</contributor><creatorcontrib>Robertson, Jessica L</creatorcontrib><creatorcontrib>Tsubouchi, Asako</creatorcontrib><creatorcontrib>Tracey, W Daniel</creatorcontrib><title>Larval defense against attack from parasitoid wasps requires nociceptive neurons</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Parasitoid wasps are a fierce predator of Drosophila larvae. Female Leptopilina boulardi (LB) wasps use a sharp ovipositor to inject eggs into the bodies of Drosophila melanogaster larvae. The wasp then eats the Drosophila larva alive from the inside, and an adult wasp ecloses from the Drosophila pupal case instead of a fly. However, the Drosophila larvae are not defenseless as they may resist the attack of the wasps through somatosensory-triggered behavioral responses. Here we describe the full range of behaviors performed by the larval prey in immediate response to attacks by the wasps. Our results suggest that Drosophila larvae primarily sense the wasps using their mechanosensory systems. The range of behavioral responses included both "gentle touch" like responses as well as nociceptive responses. We found that the precise larval response depended on both the somatotopic location of the attack, and whether or not the larval cuticle was successfully penetrated during the course of the attack. Interestingly, nociceptive responses are more likely to be triggered by attacks in which the cuticle had been successfully penetrated by the wasp. Finally, we found that the class IV neurons, which are necessary for mechanical nociception, were also necessary for a nociceptive response to wasp attacks. Thus, the class IV neurons allow for a nociceptive behavioral response to a naturally occurring predator of Drosophila.</description><subject>Anesthesiology</subject><subject>Animal behavior</subject><subject>Animals</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - cytology</subject><subject>Drosophila melanogaster - parasitology</subject><subject>Drosophila melanogaster - physiology</subject><subject>Eggs</subject><subject>Escape Reaction - physiology</subject><subject>Female</subject><subject>Host-Parasite Interactions</subject><subject>Hymenoptera</subject><subject>Insects</subject><subject>Larva - cytology</subject><subject>Larva - parasitology</subject><subject>Larva - physiology</subject><subject>Larvae</subject><subject>Leptopilina boulardi</subject><subject>Locomotion - physiology</subject><subject>Male</subject><subject>Neurons</subject><subject>Neurosciences</subject><subject>Nociceptors - cytology</subject><subject>Ovipositor</subject><subject>Pain perception</subject><subject>Parasitoids</subject><subject>Prey</subject><subject>Wasps - physiology</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptUk1vEzEQXSEQLYV_gGAlLlwS_O31BQlVBSpFggOcrYk9Dg4be2vvBvHvu23SqkWcZjR-7_nN6DXNa0qWlGv6YZunkqBfDjnhkhDdaSKeNKfUcLZQjPCnD_qT5kWtW0Ik75R63pwwwYhkRp8231dQ9tC3HgOmii1sIKY6tjCO4H63oeRdO0CBGsccffsH6lDbgldTLFjblF10OIxxj23CqeRUXzbPAvQVXx3rWfPz88WP86-L1bcvl-efVgsnmRoXSAkJWgXKQEruuSBOGYXBzz2jQkmJwgNwQlEiCqMFlYGZdUDv-Nopfta8PegOfa72eIxqqRDSMD6XGXF5QPgMWzuUuIPy12aI9naQy8ZCGaPr0WrKPDEmaOlQBOfXHD1TstNMhQ4InbU-Hn-b1rvZAqaxQP9I9PFLir_sJu8t70jHOjkLvD8KlHw1YR3tLlaHfQ8J83Tr22gltdEz9N0_0P9vJw4oV3KtBcO9GUrsTUDuWPYmIPYYkJn25uEi96S7RPBrTjy6iA</recordid><startdate>20131025</startdate><enddate>20131025</enddate><creator>Robertson, Jessica L</creator><creator>Tsubouchi, Asako</creator><creator>Tracey, W Daniel</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20131025</creationdate><title>Larval defense against attack from parasitoid wasps requires nociceptive neurons</title><author>Robertson, Jessica L ; Tsubouchi, Asako ; Tracey, W Daniel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-e100f76f12a553d340c696efd3d3214655e4daa301e5ee497415f29bfedc3bc63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Anesthesiology</topic><topic>Animal behavior</topic><topic>Animals</topic><topic>Drosophila</topic><topic>Drosophila melanogaster</topic><topic>Drosophila melanogaster - cytology</topic><topic>Drosophila melanogaster - parasitology</topic><topic>Drosophila melanogaster - physiology</topic><topic>Eggs</topic><topic>Escape Reaction - physiology</topic><topic>Female</topic><topic>Host-Parasite Interactions</topic><topic>Hymenoptera</topic><topic>Insects</topic><topic>Larva - cytology</topic><topic>Larva - parasitology</topic><topic>Larva - physiology</topic><topic>Larvae</topic><topic>Leptopilina boulardi</topic><topic>Locomotion - physiology</topic><topic>Male</topic><topic>Neurons</topic><topic>Neurosciences</topic><topic>Nociceptors - cytology</topic><topic>Ovipositor</topic><topic>Pain perception</topic><topic>Parasitoids</topic><topic>Prey</topic><topic>Wasps - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Robertson, Jessica L</creatorcontrib><creatorcontrib>Tsubouchi, Asako</creatorcontrib><creatorcontrib>Tracey, W Daniel</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>ProQuest Nursing &amp; Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological &amp; Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>ProQuest Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest 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 &amp; Engineering Database (Proquest)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Advanced Technologies &amp; Aerospace Database‎ (1962 - current)</collection><collection>ProQuest Agriculture &amp; Environmental Science Database</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Technology Collection</collection><collection>ProQuest 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 &amp; Medical Complete (Alumni)</collection><collection>ProQuest Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>Biological Sciences</collection><collection>Agriculture Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>ProQuest Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content 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 China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Robertson, Jessica L</au><au>Tsubouchi, Asako</au><au>Tracey, W Daniel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Larval defense against attack from parasitoid wasps requires nociceptive neurons</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-10-25</date><risdate>2013</risdate><volume>8</volume><issue>10</issue><spage>e78704</spage><epage>e78704</epage><pages>e78704-e78704</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Conceived and designed the experiments: JLR WDT. Performed the experiments: JLR AT. Analyzed the data: JLR. Contributed reagents/materials/analysis tools: WDT. Wrote the manuscript: JLR AT WDT.</notes><notes>Competing Interests: The authors have declared that no competing interests exist.</notes><abstract>Parasitoid wasps are a fierce predator of Drosophila larvae. Female Leptopilina boulardi (LB) wasps use a sharp ovipositor to inject eggs into the bodies of Drosophila melanogaster larvae. The wasp then eats the Drosophila larva alive from the inside, and an adult wasp ecloses from the Drosophila pupal case instead of a fly. However, the Drosophila larvae are not defenseless as they may resist the attack of the wasps through somatosensory-triggered behavioral responses. Here we describe the full range of behaviors performed by the larval prey in immediate response to attacks by the wasps. Our results suggest that Drosophila larvae primarily sense the wasps using their mechanosensory systems. The range of behavioral responses included both "gentle touch" like responses as well as nociceptive responses. We found that the precise larval response depended on both the somatotopic location of the attack, and whether or not the larval cuticle was successfully penetrated during the course of the attack. Interestingly, nociceptive responses are more likely to be triggered by attacks in which the cuticle had been successfully penetrated by the wasp. Finally, we found that the class IV neurons, which are necessary for mechanical nociception, were also necessary for a nociceptive response to wasp attacks. Thus, the class IV neurons allow for a nociceptive behavioral response to a naturally occurring predator of Drosophila.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24205297</pmid><doi>10.1371/journal.pone.0078704</doi><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1932-6203
ispartof PloS one, 2013-10, Vol.8 (10), p.e78704-e78704
issn 1932-6203
1932-6203
language eng
recordid cdi_plos_journals_1445923144
source Publicly Available Content Database; PubMed Central
subjects Anesthesiology
Animal behavior
Animals
Drosophila
Drosophila melanogaster
Drosophila melanogaster - cytology
Drosophila melanogaster - parasitology
Drosophila melanogaster - physiology
Eggs
Escape Reaction - physiology
Female
Host-Parasite Interactions
Hymenoptera
Insects
Larva - cytology
Larva - parasitology
Larva - physiology
Larvae
Leptopilina boulardi
Locomotion - physiology
Male
Neurons
Neurosciences
Nociceptors - cytology
Ovipositor
Pain perception
Parasitoids
Prey
Wasps - physiology
title Larval defense against attack from parasitoid wasps requires nociceptive neurons
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-09-23T04%3A32%3A34IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Larval%20defense%20against%20attack%20from%20parasitoid%20wasps%20requires%20nociceptive%20neurons&rft.jtitle=PloS%20one&rft.au=Robertson,%20Jessica%20L&rft.date=2013-10-25&rft.volume=8&rft.issue=10&rft.spage=e78704&rft.epage=e78704&rft.pages=e78704-e78704&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0078704&rft_dat=%3Cproquest_plos_%3E1449765797%3C/proquest_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c526t-e100f76f12a553d340c696efd3d3214655e4daa301e5ee497415f29bfedc3bc63%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1445923144&rft_id=info:pmid/24205297&rfr_iscdi=true