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A new thin sectioning method for observation of higher resolution images in bone histomorphology

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Article: e2298402 | Received 11 Jan 2023, Accepted 07 Dec 2023, Published online: 26 Jan 2024

LITERATURE CITED

  • Amson, E., de Muizon, C., Laurin, M., Argot, C., & de Buffrénil, V. (2014). Gradual adaptation of bone structure to aquatic lifestyle in extinct sloths from Peru. Proceedings of the Royal Society B, 281(1782), 20140192. DOI: 10.1098/rspb.2014.0192.
  • Amson, E., de Muizon, C., Domning, D. P., Argot, C. & de Buffrénil, V. (2015). Bone histology as a clue for resolving the puzzle of a dugong rib in the Pisco Formation, Peru. Journal of Vertebrate Paleontology, 35(3), e922981. DOI: 10.1080/02724634.2014.922981.
  • Assis, S., Keenleyside, A., Santos, A. L., & Cardoso, F. A. (2015). Bone diagenesis and its implication for disease diagnosis: Relevance of bone microstructure analysis for the study of past human remains. Microscopy and Microanalysis, 21(4), 805–825. DOI: 10.1017/S1431927615000768.
  • Atterholt, J. & Woodward, H. N. (2021). A histological survey of avian post-natal skeletal ontogeny. PeerJ, 9:e12160. DOI: 10.7717/peerj.12160.
  • Bailleul, A. M., O’Connor, J., & Schweitzer, M. H. (2019). Dinosaur paleohistology: review, trends and new avenues of investigation. PeerJ, 7:e7764. DOI: 10.7717/peerj.7764.
  • Bishop, P. J., Hocknull, S. A., Clemente, C. J., Hutchinson, J. R., Farke, A. A., Beck, B. R., Barrett, R. S., & Lloyd, D. G. (2018a). Cancellous bone and theropod dinosaur locomotion. Part I—an examination of cancellous bone architecture in the hindlimb bones of theropods. PeerJ, 6:e5778. DOI: 10.7717/peerj.5778.
  • Bishop, P. J., Hocknull, S. A., Clemente, C. J., Hutchinson, J. R., Barrett, R. S., & Lloyd, D. G. (2018b). Cancellous bone and theropod dinosaur locomotion. Part II—a new approach to inferring posture and locomotor biomechanics in extinct tetrapod vertebrates. PeerJ, 6:e5779. DOI: 10.7717/peerj.5779.
  • Bishop, P. J., Hocknull, S. A., Clemente, C. J., Hutchinson, J. R., Farke, A. A., Barrett, R. S., & Lloyd, D. G. (2018c). Cancellous bone and theropod dinosaur locomotion. Part III—Inferring posture and locomotor biomechanics in extinct theropods, and its evolution on the line to birds. PeerJ, 6:e5777. DOI: 10.7717/peerj.5777.
  • Bloom, W., Bloom, M. A. & Mclean, F. C. (1941). Calcification and ossification. Medullary bone changes in the reproductive cycle of female pigeons. Anatomical Record, 81(4), 443–466. DOI: 10.1002/ar.1090810404.
  • Boyde, A. (1984). Methodology of calcified tissue specimen preparation for SEM. In G. R. Dickson (Ed.), Methods of calcified tissue preparation (pp. 251–307). Elsevier.
  • Boyde, A. (2019). Scanning electron microscopy of bone. In A. Idris (Ed.), Bone research protocols. Methods in molecular biology, 1914 (pp. 571–616). Humana Press. DOI: 10.1007/978-1-4939-8997-3_31.
  • Boyde, A. & Riggs, C. M. (1990). The quantitative study of the orientation of collagen in compact bone slices. Bone, 11(1), 35–39. DOI: 10.1016/8756-3282(90)90069-b.
  • Bromage, T. G., Goldman, H. M., McFarlin, S. C., Warshaw, J., Boyde, A., & Riggs, C. M. (2003). Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anatomical Record (Part B: New Anat.), 274B(1), 157–168. DOI: 10.1002/ar.b.10031.
  • Carnelli, D., Vena, P., Dao, M., Ortiz, C., & Contro, R. (2013). Orientation and size-dependent mechanical modulation within individual secondary osteons in cortical bone tissue. Journal of the Royal Society Interface, 10(81), 20120953. DOI: 10.1098/rsif.2012.0953.
  • Castanet, J. (2006). Time recording in bone microstructures of endothermic animals; functional relationships. General Palaeontology, 5(3–4), 629–636. DOI: 10.1016/j.crpv.2005.10.006.
  • Chabreck, R. H. & Joanen, T. (1979). Growth rates of American alligators in Louisiana. Herpetologica, 35(1), 51–57. DOI: 10.2307/1352272.
  • Chinsamy, A. & Raath, M. A. (1992). Preparation of fossil bone for histological examination. Palaeontologica Africana, 29, 39–44.
  • Cook, S. F., Brooks, S. T., & Ezra-Cohn, H. E. (1962). Histological studies on fossil bone. Journal of Paleontology, 36(3), 483–494.
  • Curry, K. A. (1990). Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): New insights on growth rates and longevity. Journal of Vertebrate Paleontology, 19(4), 654–665. DOI: 10.1080/02724634.1999.10011179.
  • Dark, W. A., Conrad, E. C., & Crossman Jr., L. W. (1974). Liquid chromatographic analysis of epoxy resins. Journal of Chromatography, 91, 247–260. DOI: 10.1016/S0021-9673(01)97904-X.
  • Davis, G. R. & Wong, F. S. (1996). X-ray microtomography of bones and teeth. Physiological Measurement, 17(3), 121–146. DOI: 10.1088/0967-3334/17/3/001.
  • de Margerie, E., Robin, J-P., Verrier, D., Cubo, J., Groscolas, R., & Castanet, J. (2004). Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus). Journal of Experimental Biology, 207(5), 869–879. DOI: 10.1242/jeb.00841.
  • Ekhtiari, S., Chiba, K., Popovic, S., Crowther, R., Wohl, G., Wong, A. K. O., Tanke, D. H., Dufault, D. M., Geen, O. D., Parasu, N., Crowther, M. A., & Evans, D. C. (2020). First case of osteosarcoma in a dinosaur: a multimodal diagnosis. Lancet Oncology, 21(8), 1021–1022. DOI: 10.1016/S1470-2045(20)30171-6.
  • Enlow, D. H. (1954). A plastic-seal method for mounting sections of ground bone. Stain Technology, 29(1), 21–22. DOI: 10.3109/10520295409115431.
  • Enlow, D. H. & Brown, S. O. (1957). A comparative histological study of fossil and recent bone tissues. Part II. Texas Journal of Science, 9, 136–214.
  • Erickson, G. M., Makovicky, P. J., Currie, P. J., Norell, M. A., Yerby, S. A., & Brochu, C. A. (2004). Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature, 430, 772–775. DOI: 10.1038/nature02699.
  • Felder, A. A., Phillips, C., Cornish, H., Cooke, M., Hutchinson, J. R., & Doube, M. (2017). Secondary osteons scale allometrically in mammalian humerus and femur. Royal Society Open Science, 4(11), 170431. DOI: 10.1098/rsos.170431.
  • Fernández-Jalvo, Y., Andrews, P., Pesquero, D., Smith, C., Marín-Monfort, D., Sánchez, B., Geigl, E., & Alonso, A. (2010). Early bone diagenesis in temperate environments part I: Surface features and histology. Palaeogeography, Palaeoclimatology, Palaeoecology, 288(1–4), 62–81. DOI: 10.1016/j.palaeo.2009.12.016.
  • García-Martínez, R., Marín-Moratalla, N., Jordana, X., & Köhler, M. (2011). The ontogeny of bone growth in two species of dormice: Reconstructing life history traits. Comptes Rendus Palevol, 10(5–6), 489–498. DOI: 10.1016/j.crpv.2011.03.011.
  • Gray, N-M., Kainec, K., Madar, S., Tomko, L., & Wolfe, S. (2007). Sink or swim? Bone density as a mechanism for buoyancy control in early cetaceans. Anatomical Record, 290(6), 638–653. DOI: 10.1002/ar.20533.
  • Hayashi, S., Houssaye, A., Nakajima, Y., Chiba, K., Ando, T., Sawamura, H., Inuzuka, N., Kaneko, N., & Osaki, T. (2013). Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria). PLoS ONE, 8(4), e59146. DOI: 10.1371/journal.pone.0059146.
  • Heck, C. T., Volkmann, G., & Woodward, H. N. (2020). Polyester or epoxy: assessing embedding product efficacy in paleohistological methods. PeerJ, 8:e10495. DOI: 10.7717/peerj.10495.
  • Huan, H., Wang, W., & Wang, J. (2011). Huan yang shuzhi rongjie ji ji qi zhibei fangfa [Epoxy resin dissolving agent and preparation method thereof] (China Patent No. CN101649068B). China National Intellectual Property Administration.
  • Jiang, G., Pickering, S. J., Lester, E. H., & Warrior, N. A. (2010). Decomposition of epoxy resin in supercritical isopropanol. Industrial and Engineering Chemistry Research, 49(10), 4535–4541. DOI: 10.1021/ie901542z.
  • Jing, D., Zhang, S., Luo, W., Gao, X., Men, Y., Ma, C., Liu, X., Yi, Y., Bugde, A., Zhou, B. O., Zhao, Z., Yuan, Q., Feng, J. Q., Gao, L., Ge, W-P., & Zhao, H. (2018). Tissue clearing of both hard and soft tissue organs with the PEGASOS method. Cell Research, 28, 803–818. DOI: 10.1038/s41422-018-0049-z.
  • Köhler, M. & Moyà-Solà, S. (2009). Physiological and life history strategies of a fossil large mammal in a resource-limited environment. PNAS, 106(48), 20354–20358. DOI: 10.1073/pnas.0813385106.
  • Kolb, C., Scheyer, T. M., Veitschegger, K., Forasiepi, A. M., Amson, E., Van der Geer, A. A. E., Van den Hoek Ostende, L. W., Hayashi, S., & Sánchez-Villagra, M. R. (2015a). Mammalian bone palaeohistology: a survey and new data with emphasis on island forms. PeerJ, 3:e1358. DOI: 10.7717/peerj.1358.
  • Kolb, C., Scheyer, T. M., Lister, A. M., Azorit, C., de Vos, J., Schlingemann, M. A. J., Rössner, G. E., Monaghan, N. T., & Sánchez-Villagra, M. R. (2015b). Growth in fossil and extant deer and implications for body size and life history evolution. BMC Evolutionary Biology, 15, 19. DOI: 10.1186/s12862-015-0295-3.
  • Kuo, L., Zhang, L., & Xu, Z. (2019). Decomposition behavior and mechanism of epoxy resin from waste integrated circuits under supercritical water condition. Journal of Hazardous Materials, 374, 356–364. DOI: 10.1016/j.jhazmat.2019.04.028.
  • Lamm, E. (2013). Preparation and sectioning of specimens. In K. Padian & E. Lamm (Eds.), Bone histology of fossil tetrapods (pp. 55–160). University of California Press. DOI: 10.1525/california/9780520273528.003.0004.
  • Legendre, L. J. & Botha-Brink, J. (2018). Digging the compromise: investigating the link between limb bone histology and fossoriality in the aardvark (Orycteropus afer). PeerJ, 6:e5216. DOI: 10.7717/peerj.5216.
  • Li, K., Zhang, L., & Xu, Z. (2019). Decomposition behavior and mechanism of epoxy resin from waste integrated circuits under supercritical water condition. Journal of Hazardous Materials, 374, 356–364. DOI: 10.1016/j.jhazmat.2019.04.028.
  • Liu, Y., Gong, X., Wu, S., & Li, L. (2012). Decomposition of epoxy resin E-44/METHPA by tetrahydronaphthalene. In, 2012 International Conference on Biomedical Engineering and Biotechnology (pp. 1304–1306). IEEE. DOI: 10.1109/iCBEB.2012.124.
  • Marín-Moratalla, N., Jordana, X., & Köhler, M. (2013). Bone histology as an approach to providing data on certain key life history traits in mammals: Implications for conservation biology. Mammalian Biology, 78(6), 422–429. DOI: 10.1016/j.mambio.2013.07.079.
  • Mantel, G. (1850a). On a dorsal dermal spine of the Hylaeosaurus, recently discovered in the strata of Tilgate Forest. Philosophical Transactions of the Royal Society of London, 140, 391–392. DOI: 10.1098/rstl.1850.0018.
  • Mantel, G. (1850b). On the Palorosaurus; an undescribed gigantic terrestrial reptile whose remains are associated with those of the Iguanodon and other saurian in the strata of Tilgate Forest, Sussex. Philosophical Transactions of the Royal Society of London, 140, 379–390. DOI: 10.1098/rstl.1850.0017.
  • Meier, P. S., Bickelmann, C., Scheyer, T. M., Koyabu, D., & Sánchez-Villagra, M. R. (2013). Evolution of bone compactness in extant and extinct moles (Talpidae): exploring humeral microstructure in small fossorial mammals. BMC Evolutionary Biology, 13, 55. DOI: 10.1186/1471-2148-13-55.
  • Mitchell, J., Sander, P. M., & Stein, K. (2017). Can secondary osteons be used as ontogenetic indicators in sauropods? Extending the histological ontogenetic stages into senescence. Paleobiology, 43(2), 321–342. DOI: 10.1017/pab.2016.47.
  • Moncunill-Solè, B., Orlandi-Oliveras, G., Jordana, X., Rook, L., & Köhler, M. (2016). First approach of the life history of Prolagus apricenicus (Ochotonidae, Lagomorpha) from Terre Rosse sites (Gargano, Italy) using body mass estimation and paleohistological analysis. Comptes Rendus Palevol, 15(1–2), 227–237. DOI: 10.1016/j.crpv.2015.04.004.
  • Montoya-Sanhueza, G. & Chinsamy, A. (2017). Long bone histology of the subterranean rodent Bathyergus suillus (Bathyergidae): ontogenetic pattern of cortical bone thickening. Journal of Anatomy, 230(2), 203–233. DOI: 10.1111/joa.12547.
  • Montoya-Sanhueza, G., Bennet, N. C., Oosthuizen, M. K., Dengler-Crish, C. M., & Chinsamy, A. (2020). Long bone histomorphogenesis of the naked mole-rat: Histodiversity and intraspecific variation. Journal of Anatomy, 238(6), 1259–1283. DOI: 10.1111/joa.13381.
  • Musumci, G. (2014). Past, present and future: overview on histology and histopathology. Journal of Histology & Histopathology, 1, 5. DOI: 10.7243/2055-091X-1-5.
  • Nacarino-Meneses, C., Jordana, X., & Köhler, M. (2016). First approach to bone histology and skeletochronology of Equus hemionus. Comptes Rendus Palevol, 15(1–2), 267–277. DOI: 10.1016/j.crpv.2015.02.005.
  • Nopcsa, B. F. (1933). On the histology of the ribs in immature and half-grown trachodont dinosaurs. Proceedings of the Zoolgical Society of London, 103(1), 221–226. DOI: 10.1111/j.1096-3642.1933.tb01588.x.
  • Nopcsa, B. F. & Heidsiek, E. (1934). Über eine Pachyostotische Rippe aus der Kreide Rügens [A pachyostotic rib from the Rügen chalk]. Acta Zoologica, 15(2–3), 431–455. DOI: 10.1111/j.1463-6395.1934.tb00661.x.
  • Oliveux, G., Dandy, L. O., & Leeke, G. A. (2015). Degradation of a model epoxy resin by solvolysis routes. Polymer Degradation and Stability, 118, 96–103. DOI: 10.1016/j.polymdegradstab.2015.04.016.
  • Orlandi-Oliveras, G., Nacarino-Meneses, C., & Köhler, M. (2018). Bone histology provides insights into the life history mechanisms underlying dwarfing in hipparionins. Scientific Reports, 8, 17203. DOI: 10.1038/s41598-018-35347-x.
  • Pawlicki, R., Korbel, A., & Kubiak, H. (1966). Cells, collagen fibrils and vessels in dinosaur bone. Nature, 5049, 655–657. DOI: 10.1038/211655a0.
  • Quekett, J. (1849). On the intimate structure of bone, as composing the skeleton in the four great classes of animals, viz., mammals, birds, reptiles, and fishes, with some remarks on the great value of the knowledge of such structure in determining the affinities of minute fragments of organic remains. Transactions of the Microscopical Society of London, 2(1), 46–58. DOI: 10.1111/j.1365-2818.1849.tb05102.x.
  • Sander, P. M. (2000). Longbone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology, 26(3), 466–488. DOI: 10.1666/0094-8373(2000)026<0466:LHOTTS>2.0.CO;2.
  • Sawada, J., Nara, T., Fukui, J., Dodo, Y., & Hirata, K. (2014). Histomorphological species identification of tiny bone fragments from a Paleolithic site in the Northern Japanese Archipalago. Journal of Archaeological Science, 46, 270–280. DOI: 10.1016/j.jas.2014.03.025.
  • Schrof, S., Varga, P., Galvis, L., Raum, K., & Masic, A. (2014). 3D Raman mapping of the collagen fibril orientation in human osteonal lamellae. Journal of Structural Biology, 187(3), 266–275. DOI: 10.1016/j.jsb.2014.07.001.
  • Schweitzer, M. H., Marshall, M., Carron, K., Bohle, D. S., Busse, S. C., Arnold, E. V., Barnard, D., Horner, J. R., & Starkey, J. R. (1997). Heme compounds in dinosaur trabecular bone. Proceedings of the National Academy of Sciences of the United States of America, 94(12), 6291–6296. DOI: 10.1073/pnas.94.12.6291.
  • Schweitzer, M. H., Wittmeyer, J. L., Horner, J. R., & Toporski, J. K. (2005). Soft-tissue vessels and cellular preservation in Tyrannosaurus rex. Science, 307(5717), 1952–1955. DOI: 10.1126/science.1108397.
  • Schweitzer, M. H., Elsey, R. M., Dacke, C. G., Horner, J. R., & Lamm, E. (2007). Do egg-laying crocodilian (Alligator mississippiensis) archosaurs form medullary bone? Bone, 40(4), 1152–1158. DOI: 10.1016/j.bone.2006.10.029.
  • Skedros, J. G., Bloebaum, R. D., Mason, M. W., & Bramble, D. M. (1994). Analysis of a tension/compression skeletal system: Possible strain-specific differences in the hierarchical organization of bone. Anatomical Record, 239(4), 396–404. DOI: 10.1002/ar.1092390406.
  • Stein, K. & Sander, M. (2009). Histological core drilling: A less destructive method for studying bone histology. In M. A. Brown, J. F. Kane, & W. G. Parker (Eds.), Methods in fossil preparation: proceedings of the first annual fossil preparation and collections symposium (pp. 69–80). Petrified Forest National Park.
  • Stein, M., Hayashi, S., & Sander, P. M. (2013). Long bone histology and growth patterns in ankylosaurs: Implications for life history and evolution. PLoS ONE, 8(7), e68590. DOI: 10.1371/journal.pone.0068590.
  • Straehl, F. R., Scheyer, T. M., Forasiepi, A. M., & MacPhee, R. D. (2013). Evolutionary patterns of bone histology and bone compactness in xenarthran mammal long bones. PLoS ONE, 8(7), e69275. DOI: 10.1371/journal.pone.0069275.
  • Suniaga, S., Rolvien, T., vom Scheidt, A., Fiedler, I. A. K., Hrishikesh, A. B., Huysseune, A., Witten, P. E., Amling, M., & Busse, B. (2018). Increased mechanical loading through controlled swimming exercise induces bone formation and mineralization in adult zebrafish. Scientific Reports, 8(1), 3646. DOI: 10.1038/s41598-018-21776-1.
  • Susaki, E. A., Tainaka, K., Perrin, D., Kishino, F., Tawara, T., Watanabe, T. M., Yokoyama, C., Onoe, H., Eguchi, M., Yamaguchi, S., Abe, T., Kiyonari, H., Shimizu, Y., Miyawaki, A., Yokota, H., & Ueda, H. R. (2014). Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis. Cell, 157(3), 726–739. DOI: 10.1016/j.cell.2014.03.042.
  • Tainaka, K., Kubota, S. I., Suyama, T. Q., Susaki, E. A., Perrin, D., Ukai-Tadenuma, M., Ukai, H., & Ueda, H. R. (2014). Whole-body imaging with single-cell resolution by tissue decolorization. Cell, 159(4), 911–924. DOI: 10.1016/j.cell.2014.10.034.
  • Tajiri, R. & Fujita, T. (2013). Jushihomai to kenma ni yoru dobutsu soshiki kansatsu shiryo sakusei-ho: ko-soshiki to nan-soshiki no doji kansatsu [Observation methods of hard and soft animal tissues by grinding specimens impregnated with resin]. TAXA, Proceeding of the Japanese Society of Systematic Zoology, 35, 24–34.
  • Taylor, M. A. (2000). Functional significance of bone ballastin in the evolution of buoyancy control strategies by aquatic tetrapods. Historical Biology, 14(1–2), 15–31. DOI: 10.1080/10292380009380550.
  • Urano, Y., Sugimoto, Y., Tanoue, K., Matsumoto, R., Kawabe, S., Ohashi, T., & Fujiwara, S. (2019). The sandwich structure of keratinours layers controls the form and growth orientation of chicken rhinotheca. Journal of Anatomy, 235(2), 299–312. DOI: 10.1111/joa.12998.
  • Wang, M., O’Connor, J. K., Bailleul, A. M., & Li, Z. (2020). Evolution and distribution of medullary bone: evidence from a new Early Cretaceous enantiornithine bird. National Science Review, 7(6), 1068–1078. DOI: 10.1093/nsr/nwz214.
  • Wegst, U. G. K., Bai, H., Saiz, E., Tomsia, A. P., & Ritchie, R. O. (2014). Bioinspired structural materials. Nature Materials, 14(1), 23–26. DOI: 10.1038/nmat4089.
  • Weissleder, R. (2001). A clearer vision for in vivo imaging. Nature Biotechnology, 19, 316–317. DOI: 10.1038/86684.
  • Wolf, D., Kalthoff, D. C., & Sander, P. M. (2012). Osteoderm histology of the Pampatheriidae (Cingulata, Xenarthra, Mammalia): Implications for systematics, osteoderm growth, and biomechanical adaptation. Journal of Morphology, 273(4), 388–404. DOI: 10.1002/jmor.11029.
  • Woodward, H. N., Horner, J. R. & Farlow, J. O. (2014). Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology. PeerJ, 2:e422. DOI: 10.7717/peerj.422.
  • Woodward, H. N. (2019). Maiasaura (Dinosauria: Hadrosauridae) tibia osteohistology reveals non-annual cortical vascular rings in young of the year. Frontiers in Earth Sciences, 7, 50. DOI: 10.3389/feart.2019.00050.
  • Zedda, M. & Babosová, R. (2021). Does the osteon morphology depend on the body mass? A scaling study on macroscopic and histomorphometric differences between cow (Bos taurus) and sheep (Ovis aries). Zoomorphology, 140, 169–181. DOI: 10.1007/s00435-021-00516-6.
  • Zedda, M., Lepore, G., Manca, P., Chisu, V., & Farina, V. (2008). Comparative bone histology of adult horses (Equus caballus) and Cows (Bos taurus). Anatomia Histologia Embryologia, 37(6), 442–445. DOI: 10.1111/j.1439-0264.2008.00878.x.

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