Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels

During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European ee...

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Published in:Proceedings of the National Academy of Sciences
Main Authors: Freese, Marko, Rizzo, Larissa Yokota, Pohlmann, Jan-Dag, Marohn, Lasse, Witten, Paul Eckhard, Gremse, Felix, Rütten, Stephan, Güvener, Nihan, Michael, Sabrina, Wysujack, Klaus, Lammers, Twan, Kiessling, Fabian, Hollert, Henner, Hanel, Reinhold, Brinkmann, Markus
Format: Text
Language:English
Published: National Academy of Sciences 2019
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6561237/
http://www.ncbi.nlm.nih.gov/pubmed/31085642
https://doi.org/10.1073/pnas.1817738116
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spelling ftpubmed:oai:pubmedcentral.nih.gov:6561237 2023-05-15T13:27:54+02:00 Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels Freese, Marko Rizzo, Larissa Yokota Pohlmann, Jan-Dag Marohn, Lasse Witten, Paul Eckhard Gremse, Felix Rütten, Stephan Güvener, Nihan Michael, Sabrina Wysujack, Klaus Lammers, Twan Kiessling, Fabian Hollert, Henner Hanel, Reinhold Brinkmann, Markus 2019-06-04 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6561237/ http://www.ncbi.nlm.nih.gov/pubmed/31085642 https://doi.org/10.1073/pnas.1817738116 en eng National Academy of Sciences http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6561237/ http://www.ncbi.nlm.nih.gov/pubmed/31085642 http://dx.doi.org/10.1073/pnas.1817738116 Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . CC-BY-NC-ND Biological Sciences Text 2019 ftpubmed https://doi.org/10.1073/pnas.1817738116 2019-06-23T00:21:52Z During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European eel (Anguilla anguilla) breaks down its skeleton to redistribute phosphorus and calcium from hard to soft tissues during its sexual development. Using multiple analytical and imaging techniques, we characterize the spatial and temporal degradation of the skeletal framework from initial to final gonadal maturation and use elemental mass ratios in bone, muscle, liver, and gonadal tissue to determine the fluxes and fates of selected minerals and metals in the eels’ bodies. We find that bone loss is more pronounced in females than in males and eventually may reach a point at which the mechanical stability of the skeleton is challenged. P and Ca are released and translocated from skeletal tissues to muscle and gonads, leaving both elements in constant proportion in remaining bone structures. The depletion of internal stores from hard and soft tissues during maturation-induced body reorganization is accompanied by the recirculation, translocation, and maternal transfer of potentially toxic metals from bone and muscle to the ovaries in gravid females, which may have direct deleterious effects on health and hinder the reproductive success of individuals of this critically endangered species. Text Anguilla anguilla European eel PubMed Central (PMC) Proceedings of the National Academy of Sciences 116 23 11339 11344
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Biological Sciences
spellingShingle Biological Sciences
Freese, Marko
Rizzo, Larissa Yokota
Pohlmann, Jan-Dag
Marohn, Lasse
Witten, Paul Eckhard
Gremse, Felix
Rütten, Stephan
Güvener, Nihan
Michael, Sabrina
Wysujack, Klaus
Lammers, Twan
Kiessling, Fabian
Hollert, Henner
Hanel, Reinhold
Brinkmann, Markus
Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
topic_facet Biological Sciences
description During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European eel (Anguilla anguilla) breaks down its skeleton to redistribute phosphorus and calcium from hard to soft tissues during its sexual development. Using multiple analytical and imaging techniques, we characterize the spatial and temporal degradation of the skeletal framework from initial to final gonadal maturation and use elemental mass ratios in bone, muscle, liver, and gonadal tissue to determine the fluxes and fates of selected minerals and metals in the eels’ bodies. We find that bone loss is more pronounced in females than in males and eventually may reach a point at which the mechanical stability of the skeleton is challenged. P and Ca are released and translocated from skeletal tissues to muscle and gonads, leaving both elements in constant proportion in remaining bone structures. The depletion of internal stores from hard and soft tissues during maturation-induced body reorganization is accompanied by the recirculation, translocation, and maternal transfer of potentially toxic metals from bone and muscle to the ovaries in gravid females, which may have direct deleterious effects on health and hinder the reproductive success of individuals of this critically endangered species.
format Text
author Freese, Marko
Rizzo, Larissa Yokota
Pohlmann, Jan-Dag
Marohn, Lasse
Witten, Paul Eckhard
Gremse, Felix
Rütten, Stephan
Güvener, Nihan
Michael, Sabrina
Wysujack, Klaus
Lammers, Twan
Kiessling, Fabian
Hollert, Henner
Hanel, Reinhold
Brinkmann, Markus
author_facet Freese, Marko
Rizzo, Larissa Yokota
Pohlmann, Jan-Dag
Marohn, Lasse
Witten, Paul Eckhard
Gremse, Felix
Rütten, Stephan
Güvener, Nihan
Michael, Sabrina
Wysujack, Klaus
Lammers, Twan
Kiessling, Fabian
Hollert, Henner
Hanel, Reinhold
Brinkmann, Markus
author_sort Freese, Marko
title Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_short Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_full Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_fullStr Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_full_unstemmed Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_sort bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
publisher National Academy of Sciences
publishDate 2019
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6561237/
http://www.ncbi.nlm.nih.gov/pubmed/31085642
https://doi.org/10.1073/pnas.1817738116
genre Anguilla anguilla
European eel
genre_facet Anguilla anguilla
European eel
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6561237/
http://www.ncbi.nlm.nih.gov/pubmed/31085642
http://dx.doi.org/10.1073/pnas.1817738116
op_rights Copyright © 2019 the Author(s). Published by PNAS.
https://creativecommons.org/licenses/by-nc-nd/4.0/
https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
op_rightsnorm CC-BY-NC-ND
op_doi https://doi.org/10.1073/pnas.1817738116
container_title Proceedings of the National Academy of Sciences
container_volume 116
container_issue 23
container_start_page 11339
op_container_end_page 11344
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