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A notodontid novelty: Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants

Unlike most notodontids, Theroa zethus larvae feed on plants that emit copious latex when damaged. To determine how the larvae overcome this defense, we filmed final instars on poinsettia, Euphorbia pulcherrima, then simulated their behaviors and tested how the behaviors individually and combined af...

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Autores principales: Dussourd, David E., Van Valkenburg, Madalyn, Rajan, Kalavathy, Wagner, David L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6619741/
https://www.ncbi.nlm.nih.gov/pubmed/31291279
http://dx.doi.org/10.1371/journal.pone.0218994
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author Dussourd, David E.
Van Valkenburg, Madalyn
Rajan, Kalavathy
Wagner, David L.
author_facet Dussourd, David E.
Van Valkenburg, Madalyn
Rajan, Kalavathy
Wagner, David L.
author_sort Dussourd, David E.
collection PubMed
description Unlike most notodontids, Theroa zethus larvae feed on plants that emit copious latex when damaged. To determine how the larvae overcome this defense, we filmed final instars on poinsettia, Euphorbia pulcherrima, then simulated their behaviors and tested how the behaviors individually and combined affect latex exudation. Larvae initially scraped the stem, petiole, or midrib with their mandibles, then secreted acid from their ventral eversible gland (VEG) onto the abraded surface. Scraping facilitated acid penetration by disrupting the waxy cuticle. As the acid softened tissues, the larvae used their mandibles to compress the plant repeatedly, thereby rupturing the latex canals. Scraping, acid application, and compression created withered furrows that greatly diminished latex exudation distal to the furrows where the larvae invariably fed. The VEG in notodontids ordinarily serves to deter predators; when attacked, larvae spray acid aimed directly at the assailant. Using HPLC, we documented that the VEG secretion of T. zethus contains 30% formic acid (6.53M) with small amounts of butyric acid (0.05M). When applied to poinsettia petioles, the acids caused a similar reduction in latex outflow as VEG secretion milked from larvae. VEG acid could disrupt latex canals in part by stimulating the normal acid-growth mechanism employed by plants to loosen walls for cell elongation. Histological examination of cross sections in poinsettia midribs confirmed that cell walls within furrows were often highly distorted as expected if VEG acids weaken walls. Theroa zethus is the only notodontid caterpillar known to use mandibular scraping and VEG acid to disable plant defenses. However, we document that mandibular constriction of petioles occurs also in other notodontids including species that feed on hardwood trees. This capability may represent a pre-adaptation that facilitated the host shift in the Theroa lineage onto latex-bearing plants by enabling larvae to deactivate laticifers with minimal latex contact.
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spelling pubmed-66197412019-07-25 A notodontid novelty: Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants Dussourd, David E. Van Valkenburg, Madalyn Rajan, Kalavathy Wagner, David L. PLoS One Research Article Unlike most notodontids, Theroa zethus larvae feed on plants that emit copious latex when damaged. To determine how the larvae overcome this defense, we filmed final instars on poinsettia, Euphorbia pulcherrima, then simulated their behaviors and tested how the behaviors individually and combined affect latex exudation. Larvae initially scraped the stem, petiole, or midrib with their mandibles, then secreted acid from their ventral eversible gland (VEG) onto the abraded surface. Scraping facilitated acid penetration by disrupting the waxy cuticle. As the acid softened tissues, the larvae used their mandibles to compress the plant repeatedly, thereby rupturing the latex canals. Scraping, acid application, and compression created withered furrows that greatly diminished latex exudation distal to the furrows where the larvae invariably fed. The VEG in notodontids ordinarily serves to deter predators; when attacked, larvae spray acid aimed directly at the assailant. Using HPLC, we documented that the VEG secretion of T. zethus contains 30% formic acid (6.53M) with small amounts of butyric acid (0.05M). When applied to poinsettia petioles, the acids caused a similar reduction in latex outflow as VEG secretion milked from larvae. VEG acid could disrupt latex canals in part by stimulating the normal acid-growth mechanism employed by plants to loosen walls for cell elongation. Histological examination of cross sections in poinsettia midribs confirmed that cell walls within furrows were often highly distorted as expected if VEG acids weaken walls. Theroa zethus is the only notodontid caterpillar known to use mandibular scraping and VEG acid to disable plant defenses. However, we document that mandibular constriction of petioles occurs also in other notodontids including species that feed on hardwood trees. This capability may represent a pre-adaptation that facilitated the host shift in the Theroa lineage onto latex-bearing plants by enabling larvae to deactivate laticifers with minimal latex contact. Public Library of Science 2019-07-10 /pmc/articles/PMC6619741/ /pubmed/31291279 http://dx.doi.org/10.1371/journal.pone.0218994 Text en © 2019 Dussourd et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Dussourd, David E.
Van Valkenburg, Madalyn
Rajan, Kalavathy
Wagner, David L.
A notodontid novelty: Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants
title A notodontid novelty: Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants
title_full A notodontid novelty: Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants
title_fullStr A notodontid novelty: Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants
title_full_unstemmed A notodontid novelty: Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants
title_short A notodontid novelty: Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants
title_sort notodontid novelty: theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6619741/
https://www.ncbi.nlm.nih.gov/pubmed/31291279
http://dx.doi.org/10.1371/journal.pone.0218994
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