Published July 1, 2023 | Version v1
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The first record of fossilized soft parts in ossified tendons and implications for the understanding of tendon mineralization

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Surmik, Dawid, Słowiak-Morkovina, Justyna, Szczygielski, Tomasz, Wojtyniak, Marcin, Środek, Dorota, Dulski, Mateusz, Balin, Katarzyna, Krzykawski, Tomasz, Pawlicki, Roman (2023): The first record of fossilized soft parts in ossified tendons and implications for the understanding of tendon mineralization. Zoological Journal of the Linnean Society 198 (3): 747-766, DOI: 10.1093/zoolinnean/zlad001, URL: https://academic.oup.com/zoolinnean/article/198/3/747/7076280

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urn:lsid:plazi.org:pub:FFAC93153E74FFAFEE07E5747F4CFFF8
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References

  • Adams JS, Organ CL. 2005. Histologic determination of ontogenetic patterns and processes in hadrosaurian ossified tendons. Journal of Vertebrate Paleontology 25: 614-622.
  • Bailleul AM, Zhou Z. 2021. SEM Analyses of fossilized chondrocytesintheextinctbirds Yanornis and Confuciusornis: insights on taphonomy and modes of preservation in the Jehol Biota. Frontiers in Earth Science 9: 694.
  • Bailleul AM, O'Connor J, Li Z, Wu Q, Zhao T, Martinez Monleon MA, Wang M, Zheng X. 2020. Confirmation of ovarian follicles in an enantiornithine (Aves) from the Jehol biota using soft tissue analyses. Communications Biology 3: 399.
  • Barth A. 2007. Infrared spectroscopy of proteins. Biochimica et Biophysica Acta, Bioenergetics 1767: 1073-1101.
  • Bennett SC. 2001. The osteology and functional morphology of the Late Cretaceous pterosaur Pteranodon: part II. Size and functional morphology. Palaeontographica, Abteilung A: Palaozoologie - Stratigraphie 260: 113-153.
  • Bennett SC. 2003. New crested specimens of the Late Cretaceous pterosaur Nyctosaurus. Palaontologische Zeitschrift 77: 61-75.
  • Bertazzo S, Maidment SCR, Kallepitis C, Fearn S, Stevens MM, Xie HN. 2015. Fibres and cellular structures preserved in 75-million-year-old dinosaur specimens. Nature Communications 6: 1-8.
  • Brown CM, Russell AP. 2012. Homology and architecture of the caudal basket of Pachycephalosauria (Dinosauria: Ornithischia): the first occurrence of myorhabdoi in Tetrapoda. PLoS One 7: e30212.
  • Buffrenil V, Sire J-V, Rage J-C. 2010. The histological structure of glyptosaurine osteoderms (Squamata: Anguidae), and the problem of osteoderm development in squamates. Journal of Morphology 271: 729-737.
  • Byler DM, Susi H. 1986. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25: 469-487.
  • Cambier P. 1986. Infrared study of goethites of varying crystallinity and particle size: II. Crystallographic and morphological changes in series of synthetic goethites. Clay Minerals 21: 201-210.
  • Cerda IA. 2009. Consideraciones sobre la histogenesis de las costillas cervicales en los dinosaurios sauropodos. Ameghiniana 46: 193-198.
  • Cerda IA, Casal GA, Martinez RD, Ibiricu LM. 2015. Histological evidence for a supraspinous ligament in sauropod dinosaurs. Royal Society Open Science 2: 1503691-1503617.
  • Cerda IA, Gasparini Z, Coria RA, Salgado L, Reguero M, Ponce D, Gonzalez R, Jannello JM, Moly J. 2019. Paleobiological inferences for the Antarctic dinosaur Antarctopelta oliveroi (Ornithischia: Ankylosauria) based on bone histology of the holotype. Cretaceous Research 103: 104171.
  • Dingus L, Loope DB, Dashzeveg D, Swisher CC, Minjin C, Novaecek MJ, Norell MA. 2008. The geology of Ukhaa Tolgod (Djadokhta Formation, Upper Cretaceous, Nemegt Basin, Mongolia). American Museum Novitates 3616: 1-40.
  • Evans DC, Brown CM , Ryan MJ, Tsogtbaatar K . 2011 . Cranial ornamentation and ontogenetic status of Homalocephale calathocercos (Ornithischia: Pachycephalosauria) from the Nemegt Formation, Mongolia. Journal of Vertebrate Paleontology 31: 84-92.
  • Fang M, Goldstein EL, Turner AS, Les CM, Orr BG, Fisher GJ, Welch KB, Rothman ED, Banaszak Holl MM. 2012. Type i collagen D-spacing in fibril bundles of dermis, tendon, and bone: bridging between nano- and micro-level tissue hierarchy. ACS Nano 6: 9503-9514.
  • Flaig PP, McCarthy PJ, Fiorillo AR. 2013. Anatomy, evolution, and paleoenvironmental interpretation of an ancient arctic coastal plain: integrated paleopedology and palynology from the Upper Cretaceous (Maastrichtian) Prince Creek Formation, North Slope, Alaska, USA. SEPM Special Publications 104: 179-230.
  • Frey E, Buchy M, Stinnesbeck W, Gonzalez A, Stefano A. 2006. Muzquizopteryx coahuilensis n. g., n. sp., a nyctosaurid pterosaur with soft tissue preservation from the Coniacian (Late Cretaceous) of northeast Mexico (Coahuila). Oryctos 6: 19-30.
  • Fysh SA, Fredericks PM. 1983. Fourier transform infrared studies of aluminous goethites and hematites. Clays & Clay Minerals 31: 377-382.
  • Gallina PA. 2011. Estudio anatomico, sistematico y paleobiologico de Bonitasaura salgadoi (Dinosauria: sauropoda): su importancia en el contexto de la evolucion de los titanosaurios del cretacico superior de la Argentina. Ph.D. thesis, Universidad Nacional de La Plata.
  • Gangloff RA, Fiorillo AR. 2010. Taphonomy and paleoecology of a bonebed from the Prince Creek Formation, North Slope, Alaska. Palaios 25: 299-317.
  • Goryl M, Marynowski L, Brocks JJ, Bobrovskiy I, Derkowski A. 2018. Exceptional preservation of hopanoid and steroid biomarkers in Ediacaran sedimentary rocks of the East European Craton. Precambrian Research 316: 38-47.
  • Hall BK. 2015. Tendon skeletogenesis and sesamoids. In: Hall BK, ed. Bones and cartilage. developmental and evolutionary skeletal biology, 2nd edn. Elsevier, 137-149.
  • Handsfield GG, Greiner J, Madl J, Rog-Zielinska EA, Hollville E, Vanwanseele B, Shim V. 2020. Achilles subtendon structure and behavior as evidenced from tendon imaging and computational modeling. Frontiers in Sports and Active Living 2: 70.
  • Hill RV, Witmer LM, Norell MA. 2003. A new specimen of Pinacosaurus grangeri (Dinosauria: Ornithischia) from the Late Cretaceous of Mongolia: Ontogeny and phylogeny of ankylosaurs. American Museum Novitates 3395: 1-29.
  • Horner JR, Woodward HN, Bailleul AM. 2016. Mineralized tissues in dinosaurs interpreted as having formed through metaplasia: a preliminary evaluation. Comptes Rendus Palevol 15: 176-196.
  • Jackson M, Mantsch HH. 1995. The use and misuse of FTIR spectroscopy in the determination of protein structure. Critical Reviews in Biochemistry and Molecular Biology 30: 95-120.
  • Jastrzebska M, Tarnawska D, Wrzalik R, Chrobak A, Grelowski M, Wylegala E, Zygadlo D, Ratuszna A. 2017. New insight into the shortening of the collagen fibril D-period in human cornea. Journal of Biomolecular Structure and Dynamics 35: 551-563.
  • Jerzykiewicz T. 2000. Lithostratigraphy and sedimentary settings of the Cretaceous dinosaur beds of Mongolia. In: Benton MJ, Shishkin MA, Unwin DM, Kurochkin EN, eds. The age of dinosaurs in Russia and Mongolia. Cambridge: Cambridge University Press, 279-296.
  • Kannus P. 2000. Structure of the tendon connective tissue. Scandinavian Journal of Medicine and Science in Sports 10: 312-320.
  • Klein N, Christian A, Sander PM. 2012. Histology shows that elongated neck ribs in sauropod dinosaurs are ossified tendons. Biology Letters 8: 1032-1035.
  • Lee YC, Chiang CC, Huang PY, Chung CY, Huang TD, Wang CC, Chen CI, Chang RS, Liao CH, Reisz RR. 2017. Evidence of preserved collagen in an Early Jurassic sauropodomorph dinosaur revealed by synchrotron FTIR microspectroscopy. Nature Communications 8: 14220.
  • Litvinov RI, Faizullin DA, Zuev YF, Weisel JW. 2012. The α- helix to β- sheet transition in stretched and compressed hydrated fibrin clots. Biophysical Journal 103: 1020-1027.
  • Lonardelli I, Wenk HR, Lutterotti L, Goodwin M. 2005. Texture analysis from synchrotron diffraction images with the Rietveld method: dinosaur tendon and salmon scale. Journal of Synchrotron Radiation 12: 354-360.
  • Marino M, Pontrelli G, Vairo G, Wriggers P. 2017. Coupling microscale transport and tissue mechanics: modeling strategies for arterial multiphysics. In: Becker SM, ed. Modeling of microscale transport in biological processes. Amsterdam: Elsevier Academic Press, 77-112.
  • Maryanska T. 1977. Ankylosauridae (Dinosauria) from Mongolia. Palaeontologia Polonica 37: 85-151.
  • Maryanska T, Osmolska H, Kielan-Jaworowska Z. 1974. Pachycephalosauria, a new suborder of ornithischian dinosaurs. Palaeontologia Polonica 30: 45-102.
  • Moodie RL. 1928. The histological nature of ossified tendons found in dinosaurs. American Museum Novitates 311: 91-102.
  • Mori H, Druckenmiller PS, Erickson GM. 2016. A new Arctic hadrosaurid from the Prince Creek Formation (lower Maastrichtian) of northern Alaska. Acta Palaeontologica Polonica 61: 15-32.
  • Necas D, Klapetek P. 2012. Gwyddion: an open-source software for SPM data analysis. Central European Journal of Physics 10: 181-188.
  • Organ CL, Adams J. 2005. The histology of ossified tendon in dinosaurs. Journal of Vertebrate Paleontology 25: 602-613.
  • Orgel JPRO, Persikov AV, Antipova O. 2014. Variation in the helical structure of native collagen. PLoS One 9: e89519-e89519.
  • Owen R. 1860. Note on some remains of Polyptychodon from Dorking. Quarterly Journal of the Geological Society 16: 262-263.
  • Padian K, Lamm ET. 2013. Bone histology of fossil tetrapods. Berkeley, Los Angeles: University of California Press.
  • Preuschoft H, Klein N. 2013. Torsion and bending in the neck and tail of sauropod dinosaurs and the function of cervical ribs: insights from functional morphology and biomechanics. PLoS One 8: e78574.
  • Sagi I, Afratis NA, eds. 2019. Collagen. New York: Springer.
  • Sasaki S, Ikeda T, Okihara S, Nishimura S, Nakadate R, Saeki H, Oki E, Mori M, Hashizume M, Maehara Y. 2019. Principles and development of collagen-mediated tissue fusion induced by laser irradiation. Scientific Reports 9: 1-10.
  • Scheyer TM. 2007. Skeletal histology of the dermal armor of Placodontia: the occurrence of 'postcranial fibro-cartilaginous bone' and its developmental implications. Journal of Anatomy 211: 737-753.
  • Scheyer TM, Desojo JB. 2011. Palaeohistology and external microanatomy of rauisuchian osteoderms (Archosauria: Pseudosuchia). Palaeontology 54: 1289-1302.
  • Scheyer TM, Sander PM. 2009. Bone microstructures and mode of skeletogenesis in osteoderms of three pareiasaur taxa from the Permian of South Africa. Journal of Evolutionary Biology 22: 1153-1162.
  • Scheyer TM, Desojo JB, Cerda IA. 2014. Bone histology of phytosaur, aetosaur, and other archosauriform osteoderms (Eureptilia, Archosauromorpha). Anatomical Record 297: 240-260.
  • Schweitzer MH, Wittmeyer JL, Horner JR, Toporski JK. 2005. Soft-tissue vessels and cellular preservation in Tyrannosaurus rex. Science 307: 1952-1955.
  • Schweitzer MH, Avci R, Collier T , Goodwin MB. 2008. Microscopic, chemical and molecular methods for examining fossil preservation. Comptes Rendus Palevol 7: 159-184.
  • Schweitzer MH, Zheng W, Cleland TP, Goodwin MB, Boatman E, Theil E, Marcus MA, Fakra SC. 2014. A role for iron and oxygen chemistry in preserving soft tissues, cells and molecules from deep time. Proceedings of the Royal Society B 281: 20132741.
  • Skedros JG, Holmes JL, Vajda EG, Bloebaum RD. 2005. Cement lines of secondary osteons in human bone are not mineral-deficient: new data in a historical perspective. Anatomical Record - Part A Discoveries in Molecular, Cellular, and Evolutionary Biology 286: 781-803.
  • Surmik D, Boczarowski A, Balin K, Dulski M, Szade J, Kremer B, Pawlicki R. 2016. Spectroscopic studies on organic matter from Triassic reptile bones, Upper Silesia, Poland. PLoS One 11: e0151143.
  • Surmik D, Rothschild BM, Pawlicki R. 2017. Unusual intraosseous fossilized soft tissues from the middle triassic nothosaurus bone. The Science of Nature 104: 25.
  • Surmik D, Dulski M, Kremer B, Szade J, Pawlicki R. 2021. Iron-mediated deep-time preservation of osteocytes in a Middle Triassic reptile bone. Historical Biology 33: 186-193.
  • Takasaki R, Fiorillo AR, Kobayashi Y, Tykoski RS, McCarthy PJ. 2019. The first definite lambeosaurine bone from the Liscomb Bonebed of the Upper Cretaceous Prince Creek Formation, Alaska, United States. Scientific Reports 9: 5384.
  • Takasaki R, Fiorillo AR, Tykoski RS, Kobayashi Y. 2020. Re-examination of the cranial osteology of the Arctic Alaskan hadrosaurine with implications for its taxonomic status. PLoS One 15: e0232410.
  • Vesentini S, Redaelli A, Gautieri A. 2013. Nanomechanics of collagen microfibrils. Muscles, Ligaments and Tendons Journal 3: 23-34.
  • Vickaryous MK, Sire J-Y. 2009. The integumentary skeleton of tetrapods: origin, evolution, and development. Journal of Anatomy 214: 441-464.
  • Vickaryous MK, Meldrum G, Russel AP. 2015. Armored geckos: a histological investigation of osteoderm development in Tarentola (Phyllodactylidae) and Gekko (Gekkonidae) with comments on their regeneration and inferred function. Journal of Morphology 276: 1345-1357.
  • Wallace JM, Orr BG, Marini JC, Holl MMB. 2011. Nanoscale morphology of Type I collagen is altered in the Brtl mouse model of Osteogenesis Imperfecta. Journal of Structural Biology 173: 146-152.
  • Wess TJ, Orgel JP. 2000. Changes in collagen structure: drying, dehydrothermal treatment and relation to long term deterioration. Thermochimica Acta 365: 119-128.
  • Williston SW. 1903. On the osteology of Nyctosaurus (Nyctodactylus), with notes on American pterosaurs. Field Columbian Museum Publication. Geological Series 2: 125-163.
  • Wosik M, Goodwin MB, Evans DC. 2019. Nestling-sized hadrosaurine cranial material from the Hell Creek Formation of northeastern Montana, USA, with an analysis of cranial ontogeny in Edmontosaurus annectens. PaleoBios 36: 1-18.
  • Xing H, Mallon JC, Currie ML. 2017. Supplementary cranial description of the types of Edmontosaurus regalis (Ornithischia: Hadrosauridae), with comments on the phylogenetics and biogeography of Hadrosaurinae. PLoS One 12: e0175253.
  • Zheng X, Bailleul AM, Li Z, Wang X, Zhou Z. 2021. Nuclear preservation in the cartilage of the Jehol dinosaur Caudipteryx. Communications Biology 4: 1125.
  • Zhou Z. 2014. The Jehol Biota, an Early Cretaceous terrestrial Lagerstatte: new discoveries and implications. National Science Review 1: 543-559.
  • Zhou CF, Gao KQ, Fox RC. 2010. Morphology and histology of lattice-like ossified epaxial tendons in Psittacosaurus (Dinosauria: Ceratopsia). Acta Geologica Sinica - English Edition 84: 463-471.
  • Zou Z, Tang T, Macias-Sanchez E, Sviben S, Landis WJ, Bertinetti L, Fratzl P. 2020. Three-dimensional structural interrelations between cells, extracellular matrix, and mineral in normally mineralizing avian leg tendon. Proceedings of the National Academy of Sciences of the USA 117: 14102-14109.