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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

The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system
The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system
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.
1742-9994
13
Chen, Chong
3faad3e1-b898-4f4b-b418-9c1736e53f95
Copley, Jonathan T.
5f30e2a6-76c1-4150-9a42-dcfb8f5788ef
Linse, Katrin
74d7ddc0-74a1-4777-ac1d-3f39ae1935ad
Rogers, Alex D.
fb474198-f059-48f7-b637-74617b5023f6
Sigwart, Julia D.
c7fae49b-7ba7-448a-bef1-b740640a4306
Chen, Chong
3faad3e1-b898-4f4b-b418-9c1736e53f95
Copley, Jonathan T.
5f30e2a6-76c1-4150-9a42-dcfb8f5788ef
Linse, Katrin
74d7ddc0-74a1-4777-ac1d-3f39ae1935ad
Rogers, Alex D.
fb474198-f059-48f7-b637-74617b5023f6
Sigwart, Julia D.
c7fae49b-7ba7-448a-bef1-b740640a4306

Chen, Chong, Copley, Jonathan T., Linse, Katrin, Rogers, Alex D. and Sigwart, Julia D. (2015) The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system Frontiers in Zoology, 12, (1), p. 13. (doi:10.1186/s12983-015-0105-1).

Record type: Article

Abstract

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.

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Published date: 2015
Organisations: Ocean and Earth Science

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Local EPrints ID: 378306
URI: http://eprints.soton.ac.uk/id/eprint/378306
ISSN: 1742-9994
PURE UUID: aa0af95c-95b2-4464-b772-fa67f3951da1

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Date deposited: 29 Jun 2015 10:48
Last modified: 17 Jul 2017 20:53

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Author: Chong Chen
Author: Katrin Linse
Author: Alex D. Rogers
Author: Julia D. Sigwart

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