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The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system
INTRODUCTION: The ‘scaly-foot gastropod’ (Chrysomallon squamiferum Chen et al., 2015) from deep-sea hydrothermal vent ecosystems of the Indian Ocean is an active mobile gastropod occurring in locally high densities, and it is distinctive for the dermal scales covering the exterior surface of its foo...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470333/ https://www.ncbi.nlm.nih.gov/pubmed/26085836 http://dx.doi.org/10.1186/s12983-015-0105-1 |
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author | Chen, Chong Copley, Jonathan T. Linse, Katrin Rogers, Alex D. Sigwart, Julia D. |
author_facet | Chen, Chong Copley, Jonathan T. Linse, Katrin Rogers, Alex D. Sigwart, Julia D. |
author_sort | Chen, Chong |
collection | PubMed |
description | INTRODUCTION: The ‘scaly-foot gastropod’ (Chrysomallon squamiferum Chen et al., 2015) from deep-sea hydrothermal vent ecosystems of the Indian Ocean is an active mobile gastropod occurring in locally high densities, and it is distinctive for the dermal scales covering the exterior surface of its foot. These iron-sulfide coated sclerites, and its nutritional dependence on endosymbiotic bacteria, are both noted as adaptations to the extreme environment in the flow of hydrogen sulfide. We present evidence for other adaptations of the ‘scaly-foot gastropod’ to life in an extreme environment, investigated through dissection and 3D tomographic reconstruction of the internal anatomy. RESULTS: Our anatomical investigations of juvenile and adult specimens reveal a large unganglionated nervous system, a simple and reduced digestive system, and that the animal is a simultaneous hermaphrodite. We show that Chrysomallon squamiferum relies on endosymbiotic bacteria throughout post-larval life. Of particular interest is the circulatory system: Chrysomallon has a very large ctenidium supported by extensive blood sinuses filled with haemocoel. The ctenidium provides oxygen for the host but the circulatory system is enlarged beyond the scope of other similar vent gastropods. At the posterior of the ctenidium is a remarkably large and well-developed heart. Based on the volume of the auricle and ventricle, the heart complex represents approximately 4 % of the body volume. This proportionally giant heart primarily sucks blood through the ctenidium and supplies the highly vascularised oesophageal gland. Thus we infer the elaborate cardiovascular system most likely evolved to oxygenate the endosymbionts in an oxygen poor environment and/or to supply hydrogen sulfide to the endosymbionts. CONCLUSIONS: This study exemplifies how understanding the autecology of an organism can be enhanced by detailed investigation of internal anatomy. This gastropod is a large and active species that is abundant in its hydrothermal vent field ecosystem. Yet all of its remarkable features—protective dermal sclerites, circulatory system, high fecundity—can be viewed as adaptations beneficial to its endosymbiont microbes. We interpret these results to show that, as a result of specialisation to resolve energetic needs in an extreme chemosynthetic environment, this dramatic dragon-like species has become a carrying vessel for its bacteria. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-015-0105-1) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4470333 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-44703332015-06-18 The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system Chen, Chong Copley, Jonathan T. Linse, Katrin Rogers, Alex D. Sigwart, Julia D. Front Zool Research INTRODUCTION: The ‘scaly-foot gastropod’ (Chrysomallon squamiferum Chen et al., 2015) from deep-sea hydrothermal vent ecosystems of the Indian Ocean is an active mobile gastropod occurring in locally high densities, and it is distinctive for the dermal scales covering the exterior surface of its foot. These iron-sulfide coated sclerites, and its nutritional dependence on endosymbiotic bacteria, are both noted as adaptations to the extreme environment in the flow of hydrogen sulfide. We present evidence for other adaptations of the ‘scaly-foot gastropod’ to life in an extreme environment, investigated through dissection and 3D tomographic reconstruction of the internal anatomy. RESULTS: Our anatomical investigations of juvenile and adult specimens reveal a large unganglionated nervous system, a simple and reduced digestive system, and that the animal is a simultaneous hermaphrodite. We show that Chrysomallon squamiferum relies on endosymbiotic bacteria throughout post-larval life. Of particular interest is the circulatory system: Chrysomallon has a very large ctenidium supported by extensive blood sinuses filled with haemocoel. The ctenidium provides oxygen for the host but the circulatory system is enlarged beyond the scope of other similar vent gastropods. At the posterior of the ctenidium is a remarkably large and well-developed heart. Based on the volume of the auricle and ventricle, the heart complex represents approximately 4 % of the body volume. This proportionally giant heart primarily sucks blood through the ctenidium and supplies the highly vascularised oesophageal gland. Thus we infer the elaborate cardiovascular system most likely evolved to oxygenate the endosymbionts in an oxygen poor environment and/or to supply hydrogen sulfide to the endosymbionts. CONCLUSIONS: This study exemplifies how understanding the autecology of an organism can be enhanced by detailed investigation of internal anatomy. This gastropod is a large and active species that is abundant in its hydrothermal vent field ecosystem. Yet all of its remarkable features—protective dermal sclerites, circulatory system, high fecundity—can be viewed as adaptations beneficial to its endosymbiont microbes. We interpret these results to show that, as a result of specialisation to resolve energetic needs in an extreme chemosynthetic environment, this dramatic dragon-like species has become a carrying vessel for its bacteria. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-015-0105-1) contains supplementary material, which is available to authorized users. BioMed Central 2015-06-18 /pmc/articles/PMC4470333/ /pubmed/26085836 http://dx.doi.org/10.1186/s12983-015-0105-1 Text en © Chen et al. 2015 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 work is properly credited. 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 Chen, Chong Copley, Jonathan T. Linse, Katrin Rogers, Alex D. Sigwart, Julia D. The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system |
title | The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system |
title_full | The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system |
title_fullStr | The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system |
title_full_unstemmed | The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system |
title_short | The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system |
title_sort | heart of a dragon: 3d anatomical reconstruction of the ‘scaly-foot gastropod’ (mollusca: gastropoda: neomphalina) reveals its extraordinary circulatory system |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470333/ https://www.ncbi.nlm.nih.gov/pubmed/26085836 http://dx.doi.org/10.1186/s12983-015-0105-1 |
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