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Morphological responses to feeding in ticks (Ixodes ricinus)

BACKGROUND: Ticks can survive long periods without feeding but, when feeding, ingest large quantities of blood, resulting in a more than 100-fold increase of body volume. We study morphological adaptations to changes in opisthosoma volume during feeding in the castor bean tick, Ixodes ricinus. We ai...

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Autores principales: Starck, J. Matthias, Mehnert, Lisa, Biging, Anja, Bjarsch, Juliana, Franz-Guess, Sandra, Kleeberger, Daniel, Hörnig, Marie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6091150/
https://www.ncbi.nlm.nih.gov/pubmed/30123529
http://dx.doi.org/10.1186/s40851-018-0104-0
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author Starck, J. Matthias
Mehnert, Lisa
Biging, Anja
Bjarsch, Juliana
Franz-Guess, Sandra
Kleeberger, Daniel
Hörnig, Marie
author_facet Starck, J. Matthias
Mehnert, Lisa
Biging, Anja
Bjarsch, Juliana
Franz-Guess, Sandra
Kleeberger, Daniel
Hörnig, Marie
author_sort Starck, J. Matthias
collection PubMed
description BACKGROUND: Ticks can survive long periods without feeding but, when feeding, ingest large quantities of blood, resulting in a more than 100-fold increase of body volume. We study morphological adaptations to changes in opisthosoma volume during feeding in the castor bean tick, Ixodes ricinus. We aim to understand the functional morphological features that accommodate enormous changes in volume changes. METHODS: Using light and electron microscopy, we compare the cuticle and epidermis of the alloscutum, the epithelium of the midgut diverticula, and the tracheae of adult female ticks when fasting, semi-engorged, and fully engorged. RESULTS: Our results add to an existing body of knowledge that the area of the epidermis increases by cellular differentiation, cellular hypertrophy, and changes in the shape of epithelial cells from pseudostratified to single layered prismatic in semi-engorged ticks, and to thin squamous epithelium in fully engorged ticks. We did not find evidence for cell proliferation. The midgut diverticula accommodate the volume increase by cellular hypertrophy and changes in cell shape. In fully engorged ticks, the epithelial cells of the midgut diverticula are stretched to an extremely thin, squamous epithelium. Changes in size and shape (and cell divisions) contribute to the accommodation of volume changes. Tracheae do not increase in size, but extend in length, thus following the volume changes of the opisthosoma in feeding ticks to secure oxygen supply to the internal organs. CONCLUSIONS: Changes of epithelial tissue configuration in the epidermis and the midgut diverticula are described as important components of the morphological response to feeding in ticks. We provide evidence for a previously unknown mechanism hosted in the endocuticle of the tracheae that allows the tracheae of castor bean ticks to expand when the body volume increases and the distance between the respiratory spiracle and the oxygen demanding tissue enlarges. This is the first report of expandable tracheae in arthropods. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40851-018-0104-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-60911502018-08-17 Morphological responses to feeding in ticks (Ixodes ricinus) Starck, J. Matthias Mehnert, Lisa Biging, Anja Bjarsch, Juliana Franz-Guess, Sandra Kleeberger, Daniel Hörnig, Marie Zoological Lett Research Article BACKGROUND: Ticks can survive long periods without feeding but, when feeding, ingest large quantities of blood, resulting in a more than 100-fold increase of body volume. We study morphological adaptations to changes in opisthosoma volume during feeding in the castor bean tick, Ixodes ricinus. We aim to understand the functional morphological features that accommodate enormous changes in volume changes. METHODS: Using light and electron microscopy, we compare the cuticle and epidermis of the alloscutum, the epithelium of the midgut diverticula, and the tracheae of adult female ticks when fasting, semi-engorged, and fully engorged. RESULTS: Our results add to an existing body of knowledge that the area of the epidermis increases by cellular differentiation, cellular hypertrophy, and changes in the shape of epithelial cells from pseudostratified to single layered prismatic in semi-engorged ticks, and to thin squamous epithelium in fully engorged ticks. We did not find evidence for cell proliferation. The midgut diverticula accommodate the volume increase by cellular hypertrophy and changes in cell shape. In fully engorged ticks, the epithelial cells of the midgut diverticula are stretched to an extremely thin, squamous epithelium. Changes in size and shape (and cell divisions) contribute to the accommodation of volume changes. Tracheae do not increase in size, but extend in length, thus following the volume changes of the opisthosoma in feeding ticks to secure oxygen supply to the internal organs. CONCLUSIONS: Changes of epithelial tissue configuration in the epidermis and the midgut diverticula are described as important components of the morphological response to feeding in ticks. We provide evidence for a previously unknown mechanism hosted in the endocuticle of the tracheae that allows the tracheae of castor bean ticks to expand when the body volume increases and the distance between the respiratory spiracle and the oxygen demanding tissue enlarges. This is the first report of expandable tracheae in arthropods. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40851-018-0104-0) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-04 /pmc/articles/PMC6091150/ /pubmed/30123529 http://dx.doi.org/10.1186/s40851-018-0104-0 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Starck, J. Matthias
Mehnert, Lisa
Biging, Anja
Bjarsch, Juliana
Franz-Guess, Sandra
Kleeberger, Daniel
Hörnig, Marie
Morphological responses to feeding in ticks (Ixodes ricinus)
title Morphological responses to feeding in ticks (Ixodes ricinus)
title_full Morphological responses to feeding in ticks (Ixodes ricinus)
title_fullStr Morphological responses to feeding in ticks (Ixodes ricinus)
title_full_unstemmed Morphological responses to feeding in ticks (Ixodes ricinus)
title_short Morphological responses to feeding in ticks (Ixodes ricinus)
title_sort morphological responses to feeding in ticks (ixodes ricinus)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6091150/
https://www.ncbi.nlm.nih.gov/pubmed/30123529
http://dx.doi.org/10.1186/s40851-018-0104-0
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