{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T23:47:47Z","timestamp":1787010467894,"version":"build-2736575974"},"reference-count":66,"publisher":"The Royal Society","issue":"1841","license":[{"start":{"date-parts":[[2016,10,26]],"date-time":"2016-10-26T00:00:00Z","timestamp":1477440000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/journals\/ethics-policies\/data-sharing-mining\/"}],"funder":[{"name":"PIER","award":["PIF-2014-28"],"award-info":[{"award-number":["PIF-2014-28"]}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["BU 2562\/2-1"],"award-info":[{"award-number":["BU 2562\/2-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["BU 2562\/3-1"],"award-info":[{"award-number":["BU 2562\/3-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["royalsocietypublishing.org"],"crossmark-restriction":true},"short-container-title":["Proc. R. Soc. B."],"published-print":{"date-parts":[[2016,10,26]]},"abstract":"<jats:p>\n                    European eels (\n                    <jats:italic>Anguilla anguilla<\/jats:italic>\n                    ) undertake an impressive 5 000 km long migration from European fresh waters through the North Atlantic Ocean to the Sargasso Sea. Along with sexual maturation, the eel skeleton undergoes a remarkable morphological transformation during migration, where a hitherto completely obscure bone loss phenomenon occurs. To unravel mechanisms of the maturation-related decay of the skeleton, we performed a multiscale assessment of eels' bones at different life-cycle stages. Accordingly, the skeleton reflects extensive bone loss that is mediated via multinucleated bone-resorbing osteoclasts, while other resorption mechanisms such as osteocytic osteolysis or matrix demineralization were not observed. Preserving mechanical stability and releasing minerals for energy metabolism are two mutually exclusive functions of the skeleton that are orchestrated in eels through the presence of two spatially segregated hard tissues: cellular bone and acellular notochord. The cellular bone serves as a source of mineral release following osteoclastic resorption, whereas the mineralized notochord sheath, which is inaccessible for resorption processes due to an unmineralized cover layer, ensures sufficient mechanical stability as a part of the notochord sheath. Clearly, an eel's skeleton is structurally optimized to meet the metabolic challenge of fasting and simultaneous sexual development during an exhausting journey to spawning areas, while the function of the vertebral column is maintained to achieve this goal.\n                  <\/jats:p>","DOI":"10.1098\/rspb.2016.1550","type":"journal-article","created":{"date-parts":[[2016,10,19]],"date-time":"2016-10-19T05:09:14Z","timestamp":1476853754000},"page":"20161550","update-policy":"https:\/\/doi.org\/10.1098\/crossmark-policy","source":"Crossref","is-referenced-by-count":15,"title":["How the European eel (\n                    <i>Anguilla anguilla<\/i>\n                    ) loses its skeletal framework across lifetime"],"prefix":"10.1098","volume":"283","author":[{"given":"Tim","family":"Rolvien","sequence":"first","affiliation":[{"name":"Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, 22529 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Florian","family":"Nagel","sequence":"additional","affiliation":[{"name":"Gesellschaft f\u00fcr Marine Aquakultur mbh, Hafent\u00f6rn 3, 25761 B\u00fcsum, Germany"},{"name":"Aller Aqua Research GmbH, Hafent\u00f6rn 3, 25761 B\u00fcsum, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Petar","family":"Milovanovic","sequence":"additional","affiliation":[{"name":"Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, 22529 Hamburg, Germany"},{"name":"Laboratory for Anthropology, Institute of Anatomy, Faculty of Medicine, University of Belgrade, Dr Subotica 4\/2, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sven","family":"Wuertz","sequence":"additional","affiliation":[{"name":"Leibnitz Institute of Freshwater Ecology and Inland Fisheries, M\u00fcggelseedamm 310, 12587 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert Percy","family":"Marshall","sequence":"additional","affiliation":[{"name":"Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, 22529 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anke","family":"Jeschke","sequence":"additional","affiliation":[{"name":"Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, 22529 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Felix N.","family":"Schmidt","sequence":"additional","affiliation":[{"name":"Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, 22529 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Hahn","sequence":"additional","affiliation":[{"name":"Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, 22529 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"P. Eckhard","family":"Witten","sequence":"additional","affiliation":[{"name":"Department of Biology, Research Group Evolutionary Developmental Biology, Ghent University, Ledeganckstraat 35, 9000 Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Amling","sequence":"additional","affiliation":[{"name":"Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, 22529 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3099-8073","authenticated-orcid":false,"given":"Bj\u00f6rn","family":"Busse","sequence":"additional","affiliation":[{"name":"Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, 22529 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"175","published-online":{"date-parts":[[2016,10,26]]},"reference":[{"key":"e_1_3_7_2_2","first-page":"408","author":"Tesch FW","year":"2003","journal-title":"The Eel"},{"key":"e_1_3_7_3_2","doi-asserted-by":"publisher","DOI":"10.1007\/s11160-006-0005-8"},{"key":"e_1_3_7_4_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.01524"},{"key":"e_1_3_7_5_2","doi-asserted-by":"publisher","DOI":"10.1023\/A:1015059524947"},{"key":"e_1_3_7_6_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1178120"},{"key":"e_1_3_7_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cbpa.2007.03.021"},{"key":"e_1_3_7_8_2","doi-asserted-by":"publisher","DOI":"10.1038\/251220a0"},{"key":"e_1_3_7_9_2","doi-asserted-by":"publisher","DOI":"10.1023\/A:1007720600588"},{"key":"e_1_3_7_10_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-185X.2009.00077.x"},{"key":"e_1_3_7_11_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02408525"},{"key":"e_1_3_7_12_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02546406"},{"key":"e_1_3_7_13_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ygcen.2006.12.009"},{"key":"e_1_3_7_14_2","doi-asserted-by":"publisher","DOI":"10.1677\/JOE-08-0492"},{"key":"e_1_3_7_15_2","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1002\/9781118453926.ch22","volume-title":"Primer on the metabolic bone diseases and disorders of mineral metabolism","author":"Favus MJ","year":"2013"},{"key":"e_1_3_7_16_2","first-page":"17","article-title":"Evolutionary physiology of bone: bone metabolism in changing environments","volume":"30","author":"Doherty AH","year":"2015","journal-title":"Physiology (Bethesda)"},{"key":"e_1_3_7_17_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.064790"},{"key":"e_1_3_7_18_2","doi-asserted-by":"publisher","DOI":"10.1002\/9781118453926.ch4"},{"key":"e_1_3_7_19_2","doi-asserted-by":"publisher","DOI":"10.3109\/03008207.2015.1013193"},{"key":"e_1_3_7_20_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1051930304"},{"key":"e_1_3_7_21_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1065"},{"key":"e_1_3_7_22_2","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-381320-6.00010-2"},{"key":"e_1_3_7_23_2","doi-asserted-by":"publisher","DOI":"10.1242\/dmm.019091"},{"key":"e_1_3_7_24_2","doi-asserted-by":"publisher","DOI":"10.1242\/dev.071035"},{"key":"e_1_3_7_25_2","doi-asserted-by":"publisher","DOI":"10.1038\/bonekey.2013.77"},{"key":"e_1_3_7_26_2","first-page":"432","volume-title":"Major transitions in vertebrate evolution","author":"Hall BK","year":"2007"},{"key":"e_1_3_7_27_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02152363"},{"key":"e_1_3_7_28_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.aquaculture.2005.04.031"},{"key":"e_1_3_7_29_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4020-9095-0_13"},{"key":"e_1_3_7_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ygcen.2011.08.009"},{"key":"e_1_3_7_31_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1095-8649.1982.tb03994.x"},{"key":"e_1_3_7_32_2","doi-asserted-by":"publisher","DOI":"10.1002\/jbmr.1805"},{"key":"e_1_3_7_33_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bone.2014.05.010"},{"key":"e_1_3_7_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bone.2007.10.021"},{"key":"e_1_3_7_35_2","doi-asserted-by":"publisher","DOI":"10.1002\/jbmr.2340"},{"key":"e_1_3_7_36_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.biomaterials.2006.11.043"},{"key":"e_1_3_7_37_2","doi-asserted-by":"publisher","DOI":"10.1021\/nn401360u"},{"key":"e_1_3_7_38_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bone.2011.11.013"},{"key":"e_1_3_7_39_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-3495(02)75673-7"},{"key":"e_1_3_7_40_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1095-8649.2003.00229.x"},{"key":"e_1_3_7_41_2","doi-asserted-by":"publisher","DOI":"10.1093\/clinchem\/45.8.1347"},{"key":"e_1_3_7_42_2","doi-asserted-by":"publisher","DOI":"10.1111\/jfb.12870"},{"key":"e_1_3_7_43_2","first-page":"1","article-title":"Lipid and protein content in Anguilla anguilla during growth and starvation","volume":"4","author":"Boetius I","year":"1985","journal-title":"Dana"},{"key":"e_1_3_7_44_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10695-010-9397-4"},{"key":"e_1_3_7_45_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bone.2011.08.017"},{"key":"e_1_3_7_46_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1051670105"},{"key":"e_1_3_7_47_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.aquatox.2006.12.014"},{"key":"e_1_3_7_48_2","doi-asserted-by":"publisher","DOI":"10.1016\/0305-0491(84)90027-0"},{"key":"e_1_3_7_49_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1469-7580.2003.00239.x"},{"key":"e_1_3_7_50_2","unstructured":"Meunier F. 1989 The acellularisation process in osteichthyan bone. Trends in vertebrate morphology. In Proc. of the 2nd Int. Symp. on Vertebrate Morphology Vienna Austria 1986 (ed. HHH Splechtna) pp. 443\u2013446. Stuttgart Germany: Fischer."},{"key":"e_1_3_7_51_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1474-9726.2010.00633.x"},{"key":"e_1_3_7_52_2","doi-asserted-by":"publisher","DOI":"10.1002\/jbmr.1567"},{"key":"e_1_3_7_53_2","doi-asserted-by":"publisher","DOI":"10.1159\/000141794"},{"key":"e_1_3_7_54_2","doi-asserted-by":"publisher","DOI":"10.1007\/s004410050782"},{"key":"e_1_3_7_55_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1412372111"},{"key":"e_1_3_7_56_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.020636"},{"key":"e_1_3_7_57_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02441217"},{"key":"e_1_3_7_58_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.124073"},{"key":"e_1_3_7_59_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.biomaterials.2014.12.024"},{"key":"e_1_3_7_60_2","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.3006286"},{"key":"e_1_3_7_61_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cbpc.2015.08.007"},{"key":"e_1_3_7_62_2","doi-asserted-by":"publisher","DOI":"10.1111\/jfd.12189"},{"key":"e_1_3_7_63_2","doi-asserted-by":"publisher","DOI":"10.1186\/1471-213X-12-28"},{"key":"e_1_3_7_64_2","doi-asserted-by":"publisher","DOI":"10.5962\/bhl.title.82144"},{"key":"e_1_3_7_65_2","first-page":"115","article-title":"Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis","volume":"21","author":"Manolagas SC","year":"2000","journal-title":"Endocr. Rev"},{"key":"e_1_3_7_66_2","doi-asserted-by":"publisher","DOI":"10.1359\/jbmr.2001.16.2.221"},{"key":"e_1_3_7_67_2","doi-asserted-by":"publisher","DOI":"10.1242\/dev.01812"}],"container-title":["Proceedings of the Royal Society B: Biological Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2016.1550","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/full-xml\/10.1098\/rspb.2016.1550","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2016.1550","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,20]],"date-time":"2021-02-20T15:55:31Z","timestamp":1613836531000},"score":1,"resource":{"primary":{"URL":"https:\/\/royalsocietypublishing.org\/doi\/10.1098\/rspb.2016.1550"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,10,26]]},"references-count":66,"journal-issue":{"issue":"1841","published-print":{"date-parts":[[2016,10,26]]}},"alternative-id":["10.1098\/rspb.2016.1550"],"URL":"https:\/\/doi.org\/10.1098\/rspb.2016.1550","relation":{},"ISSN":["0962-8452","1471-2954"],"issn-type":[{"value":"0962-8452","type":"print"},{"value":"1471-2954","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,10,26]]},"assertion":[{"value":"2016-07-15","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2016-09-22","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2016-10-26","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}