Determination of individual age and ontogenetic stages of fossil tetrapods using paleohistological methods

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Abstract

The determination of individual age and ontogenetic stage (juvenile, subadult, adult) of fossil vertebrates is important for the initial determination of taxonomic affiliation, as well as for further evolutionary and paleobiological interpretations. Determination of individual age and ontogenetic stage (= relative age) is carried out by various methods, including paleohistological analysis. The study of thin sections of tetrapod bones allows us to assume how many years the animal lived (skeletochronological method) and to determine the ontogenetic stage according to a set of age-related histological markers: change in the type of bone matrix and vascularization, change in the distance between growth marks, formation of the external fundamental system (EFS), formation of the inner (endosteal) and outer (periosteal) circumferential layers (OCL, ICL), occurrences of secondary remodeling – Haversian substitution and formation of trabeculae. Depending on the phylogenetic position and biological peculiarities of the study group of tetrapods, the set of age “histologic markers” may be different.

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About the authors

P. P. Skutschas

Saint Petersburg State University

Author for correspondence.
Email: skutchas@mail.ru
Russian Federation, Saint Petersburg, 199034

V. V. Kolchanov

Saint Petersburg State University

Email: veniamin.kolchanov@mail.ru
Russian Federation, Saint Petersburg, 199034

References

  1. Клевезаль Г. А., Каллер Салас А. В., Кирпичев С. П., 1972. Об определении возраста птиц по слоям в периостальной кости // Зоологический. журнал. Т. 51. Вып. 11. С. 1726–1730.
  2. Клевезаль Г. А., Клейненберг С. Е., 1967. Определение возраста млекопитающих по слоистым структурам зубов и кости. Москва: Наука. 142 с.
  3. Клевезаль Г. А., Смирина Э. М., 2016. Регистрирующие структуры наземных позвоночных. Краткая история и современное состояние исследований // Зоологический. журнал Т. 95. Вып. 8. С. 872–896.
  4. Клейненберг С. Е., Смирина Э. М., 1969. К методике определения возраста амфибий // Зоологический. журнал Т. 48. № 7. С. 1090–1094.
  5. Мина М. В., Клевезаль Г. А., 1970. Принципы исследования регистрирующих структур // Успехи современной биологии. Т. 70. Вып. 3. С. 341–352.
  6. Alekseyev S. S., Gordeeva N. V., Samusenok V. P., Matveev A. N., Andreev R. S., Yur’ev A.L., Smirina E.M., 2013. Extant and extinct forms of Arctic charr Salvelinus alpinus (L.) complex from the Leprindo lake system (Transbaikalia): differentiation in life history, morphology, and genetics // Journal of Ichthyology. V. 53. P. 792–803.
  7. Alekseyev S. S., Samusenok V. P., Gordeeva, N.V., Yur’ev A.L., Korostelev N. B., Matveev A. N., 2024. The role of temporal reproductive isolation, trophic polymorphism and growth rate fluctuations in the diversification of Arctic charr Salvelinus alpinus (L.) in Lake Kalarskii Davatchan, Transbaikalia, Russia // Hydrobiologia. P. 1–25.
  8. Amprino R., 1947. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l’accroissement // Arch. Biol. V. 58. P. 315–330.
  9. Andrade R. C., Bantim R. A., Lima F. J., Campos L. D., Eleutéri L. H., Sayão J. M., 2015. New data about the presence and absence of the external fundamental system in archosaurs // Cad. Cult. Ciência. V. 14. P. 200–211.
  10. Averianov A. O., Skutschas P. P., Lopatin A. V., 2023. Ontogeny and miniaturization of Alvarezsauridae (Dinosauria, Theropoda) // Bio. Comm. V. 68. № 2. P. 65–73. https://doi.org/10.21638/spbu03.2023.201
  11. Bapinaev R. A., Golovneva L. B., Zolina A. A., Averianov A. O., Skutschas P. P., 2023. New data on high-latitude hadrosaurid dinosaurs from the Upper Cretaceous Kakanaut formation of Chukotka, Russia // Cret. Res. V. 149. 105552.
  12. Bennett S. C., 1993. The ontogeny of Pteranodon and other pterosaurs // Paleobiology. V. 19. P. 92–106.
  13. Boitsova E. A., Skutschas P. P., Sennikov A. G., Golubev V. K., Masuytin V. V., Masuytina O. A., 2019. Bone histology of two pareiasaurs from Russia (Deltavjatia rossica and Scutosaurus karpinskii) with implications for pareiasaurian palaeobiology // Biol. J. Linn. Soc. V. 128. № 2. P. 289–310. https://doi.org/10.1093/biolinnean/blz094
  14. Botha J., Huttenlocker A., 2021. Nonmammalian Synapsids // Vertebrate skeletal histology and paleohistology. de Buffrénil V., de Ricqlès A. J., Zylberberg L., Padian K. (Eds). Boca Raton, CRC Press. P. 550–563.
  15. Castanet J., Francillon-Viellot H., Meunier E., De Ricqles A., 1993. Bone and individual aging. // Bone, Hall B. K. (Ed). London, UK, CRC Press. P. 245– 283.
  16. Castanet J., Naulleau G., 1974. Donnees experimentalessur la valeur des marques squelettiques comme indicateur de l’age chez Vipera aspis (L.) (Ophidia, Viperidae) // Zoologica Scripta. V. 3. P. 201–208.
  17. Castanet J., Smirina E. M., 1990. Introduction to the skeletochronological method in amphibians and reptiles // Annales des Sciences Naturelles, Zoologie 13e Series. V. 11. P. 191–196.
  18. Cerda I. A., Chinsamy A., Pol D., Apaldetti C., Otero A., Powell J. E., et al., 2017. Novel insight into the origin of the growth dynamics of sauropod dinosaurs // PLoS ONE. V. 12. № 6. e0179707. https://doi.org/10.1371/journal.pone.0179707
  19. Cullen T. M., Brown C. M., Chiba K., Brink K. S., Makovicky P. J., Evans D. C., 2021. Growth variability, dimensional scaling, and the interpretation of osteohistological growth data // Biol. Lett. V. 17. 20210383. https://doi.org/10.1098/rsbl.2021.0383
  20. de Buffrénil V., Castanet J., 2000. Age estimation by skeletochronology in the Nile monitor (Varanus niloticus), a highly exploited species // J. Herpetol. V. 34. P. 414–424.
  21. de Buffrénil V., Quilhac A., 2021. Bone Tissue Types: A Brief Account of Currently Used Categories // Vertebrate skeletal histology and paleohistology. de Buffrénil V., de Ricqlès A. J., Zylberberg L., Padian K. (Eds). Boca Raton, CRC Press. P. 148–182.
  22. de Buffrénil V., Quilhac A., 2021a. Bone Remodeling // Vertebrate skeletal histology and paleohistology. de Buffrénil V., de Ricqlès A. J., Zylberberg L., Padian K. (Eds). Boca Raton, CRC Press. P. 229–246.
  23. de Buffrénil V., Quilhac A., Castanet J., 2021. Cyclical growth and skeletochronology // Vertebrate skeletal histology and paleohistology. de Buffrénil V., de Ricqlès A. J., Zylberberg L., Padian K. (Eds). Boca Raton, CRC Press. P. 626–644.
  24. de Buffrénil V., Quilhac A., Cubo J., 2021a. Accretion Rate and Histological Features of Bone // Vertebrate skeletal histology and paleohistology. de Buffrénil V., de Ricqlès A. J., Zylberberg L., Padian K. (Eds). Boca Raton, CRC Press. P. 221–228.
  25. de Ricqlès A., Padian K., Horner J. R., Francillon-Viellot H., 2000. Paleohistology of the bones of pterosaurs (Reptilia: Archosauria): anatomy, ontogeny and biochemical implications // Zool. J. Linn. Soc. V. 129. P. 349–385.
  26. Eden C. S., Whiteman H. H., Duobinis-Gray L., Wissinger S. A., 2007. Accuracy assessment of skeletochronology in the Arizona tiger salamander (Ambystoma tigrinum nebulosum) // Copeia. № 2. P. 471–477.
  27. Erickson G. M., 2005. Assessing dinosaur growth patterns: a microscopic revolution // Trends Ecol. Evol. V. 20. 677e684. https://doi.org/10.1016/j.tree.2005.08.012
  28. Erickson G. M. Rogers K. C., Yerby S. A., 2001. Dinosaur growth patterns and rapid avian growth rates // Nature. V. 412. P. 429–433.
  29. Fernández-Dumont M.L., Pereyra M. E., Bona P., Apesteguía S., 2021. New data on the palaeosteohistology and growth dynamic of the notosuchian Araripesuchus Price, 1959 // Lethaia. https://doi.org/10.1111/let.12423
  30. Francillon H., 1979. Etude experimentale des marques de croissance sur les humerus et les femurs des tritons cretes (Triturus cristatus Laurenti) en relation avec la determination de l’age individual // Acta Zoologica Stockholm. V. 60. P. 223–232.
  31. Francillon H., Castanet J., 1985. Mise en evidence experimentale du caractere annuel des lignes d’arret de croissance squelettique chez Rana esculenta (Amphibia, Anura) // Comptes Rendus de l’Academie des Sciences. Ser. 3. V. 300. P. 327–332.
  32. Francillon-Vieillot H., de Buffrénil V., Castanet J., Géraudie J., Meunier F. J., Sire J. Y., Zylberberg L., de Ricqlès A., 1990. Microstructure and mineralization of vertebrate skeletal tissues // Skeletal biomineralization: patterns, processes and evolutionary trends. Carter J. G., (Ed.). New York (NY), Van Nostrand Reinhold. P. 471–548.
  33. Francillon-Vieillot H., Arntzen J. W., Geraudie J., 1990a. Age, growth and longevity of sympatric Triturus cristatus, T. narinoratus and their hybrids (Amphibia, Urodela): a skeleto- chronological comparison // J. Herpetol. V. 24. P. 13–22.
  34. Frazier J., 1985. A review of in vivo labels for studies of age determination and growth in amphibians and reptiles // Herpetologica. V. 41. P. 222–227.
  35. Frazier J., 1985a. Tetracycline as in vivo label in bones of green turtles, Chelonia mydas (L.) // Herpetologica. V. 41. P. 228–234.
  36. Griffin T. C., Stocker R. M., Colleary C., Stefanic C. M., Lessner E. J., Riegler M., Formoso K., Koeller K., Nesbitt S. J., 2021. Assessing ontogenetic maturity in extinct saurian reptiles // Biol. Rev. V. 96. P. 470–525. 470 doi: 10.1111/brv.12666
  37. Hayashi S., Kubo M. O., Sánchez-Villagra M.R., Taruno H., Izawa M., Shiroma T., Nakano T., Fujita M., 2023. Variation and process of life history evolution in insular dwarfism as revealed by a natural experiment // Front. Earth Sci. V. 11. 1095903. doi: 10.3389/feart.2023.1095903
  38. Horner J., de Ricqlès A., Padian K., 1999. Variation in dinosaur skeletochronology indicators: Implications for age assessment and physiology // Paleobiology. V. 25. P. 295–304. 10.1017/S0094837300021308
  39. Huttenlocker A. K., Woodward H., Hall B. K., 2013. The biology of bone // Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation. Padian K., Lamm E-T., (Eds). Berkeley: University of California Press. P. 13–34.
  40. Jordana X., Marín-Moratallaa N., Moncunill-Solèa B., Nacarino-Meneses C., Köhler M., 2016. Ontogenetic changes in the histologocal features of zonal bone tissue of ruminants: A quantitative approach // C. R. Palevol. V. 15. P. 255–266.
  41. Khonsue W., Matsui M., 2001. Absence of Lines of Arrested Growth in Overwintered Tadpoles of the American Bullfrog, Rana catesbeiana (Amphibia, Anura). Current Herpetology. V. 20. № 1. P. 33–37.
  42. Klein N., Sander P. M., 2008. Ontogenetic stages in the long bone histology of sauropod dinosaurs // Paleobiology. V. 34. P. 248–264.
  43. Klein N., Foth C., Schoch R. R., 2017. Preliminary observations on the bone histology of the Middle Triassic pseudosuchian archosaur Batrachotomus kupferzellensis reveal fast growth with laminar fibrolamellar bone tissue // J. Vertebr. Paleontol. doi: 10.1080/02724634.2017.1333121
  44. 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., 2015. Mammalian bone palaeohistology: A survey and new data with emphasis on island forms // Peer J. V. 3. e1358.
  45. Konietzko-Meier D., Sander P. M., 2013. Long bone histology of Metoposaurus diagnosticus (Temnospondyli) from the Late Triassic of Krasiejów (Poland) and its paleobiological implications // J. Vertebr. Paleontol. V. 33. № 5. P. 1003–1018.
  46. Marangoni F., Schaefer E. F., Cajade R., Tejedo M., 2009. Growth marks formation and chronology of two neotropical anuran species // J. Herpetol. V. 43. P. 446– 450.
  47. Margerie E. de, Cubo J., Castaney J., 2002. Bone typology and growth rate: testing and quantifying “Amprino’s rule” in the mallard (Anas platyrhynchos) // C. R. Acad. Sci. Paris (Sci. Vie). V. 325. P. 221–230.
  48. Martin D., Currie P., Kundrát M., 2023. Variability of bone microstructure and growth lines in the evolution of troodontids and dromaeosaurids // Acta Zoologica. V. 105. № 5. P. 135–175. 10.1111/azo.12467.
  49. Martinez-Maza C., Alberdi M. T., Nieto-Diaz M., Prado J. L., 2014. Life history traits of the Miocene Hipparion concudense (Spain) inferred from bone histological structure // PLoS ONE. V. 9. e1358. doi: 10.1371/journal.pone.0103708
  50. Mascarenhas-Junior P.B., Bochetti-Bassetti L.A., Sayao J. M., 2021. Bone histology of Broad-snouted Caiman Caiman latirostris (Crocodylia: Alligatoridae) as tool for morphophysiological inferences in Crocodylia // Acta Herpetol. V. 16. P. 109–121.
  51. 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. V. 43. P. 321–342.
  52. Nelson R. C., Bookhout T. A., 1980. Counts of Periosteal Layers Invalid for Aging Canada Geese // J. Wildl. Manag. V. 44. № 2. P. 518–521.
  53. Padian K., Horner J. R., Ricqlès A., 2004. Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies // J. Vert. Paleontol. V. 24. № 3. P. 555–571.
  54. Padian K., Woodward H. N., 2021. Archosauromorpha: Avemetatarsalia – dinosaurs and their relatives // Vertebrate skeletal histology and paleohistology. de Buffrénil V., de Ricqlès A. J., Zylberberg L., Padian K. (Eds). Boca Raton, CRC Press. P. 511–549.
  55. Picasso M. B.J., Hospitaleche C. A., 2024. Hindlimb bones texture through postnatal ages of Rhea americana (Aves: Palaeognathae) // Anat. Histol. Embryol. V. 53. e13004. https://doi.org/10.1111/ahe.13004
  56. Ponton F., Elzanowski A., Castanet J., Chinsamy A., Margerie E. de, Ricqlès A. de, Cubo J., 2004. Variation of the outer circumferential layer in the limb bones of birds // Acta Ornithol. V. 39. P. 21–24. doi: 10.3161/068.039.0210
  57. Prondvai E., Godefroit P., Adriaens D., Hu D.-Yu., 2018. Intraskeletal histovariability, allometric growth patterns, and their functional implications in bird-like dinosaurs // Sci Rep. V. 8. № 258. https://doi.org/10.1038/s41598-017-18218-9
  58. Sander P. M., 2000. Long bone histology of the Tendaguru sauropods: implications for growth and biology // Paleobiology. V. 26. № 3. P. 466–488.
  59. Sander P. M., Mateus O., Laven T., Knötschke N., 2006. Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur // Nature. V. 441. P. 739–741.
  60. Schucht P. J., Klein N., Lambertz M., 2021. What’s my age again? On the ambiguity of histology based skeletochronology // Proc. R. Soc. B. V. 288. 20211166. https://doi.org/10.1098/rspb.2021.1166
  61. Sinsch U., 2015. Review: Skeletochronological assessment of demographic life-history traits in amphibians // Herpetological Journal. V. 25. P. 5–13.
  62. Skutschas P. P., Boitsova E. A., Averianov A. O., Sues H-D., 2017. Ontogenetic changes in long-bone histology of an ornithomimid theropod dinosaur from the Upper Cretaceous Bissekty Formation of Uzbekistan // Historical Biology. V. 29. № 6. P. 715–729, doi: 10.1080/08912963.2016.1233180
  63. Skutschas P. P., Stein K., 2015. Long bone histology of the stem salamander Kokartus honorarius (Amphibia: Caudata) from the Middle Jurassic of Kyrgyzstan // J. Anat. V. 226. P. 334–347.
  64. Skutschas P. P., Saburov P. G., Boitsova E. A., Kolchanov V. V., 2019. Ontogenetic changes in long-bone histology of the cryptobranchid Eoscapherpeton asiaticum (Amphibia: Caudata) from the Late Cretaceous of Uzbekistan // Comptes Rendus Palevol. V. 18. № 3. P. 306–316.
  65. Skutschas P. P., Saburov P. G., Uliakhin A. V., Kolchanov V. V., 2024. Long bone morphology and histology of the stem salamander Kulgeriherpeton ultimum (Caudata, Karauridae) from the Lower Cretaceous of Yakutia // Paleontological Journal. V. 58. P. 101–111.
  66. Słowiak J., Szczygielski T., Ginter M., Fostowicz-Frelik Ł., 2020. Uninterrupted growth in a non-polar hadrosaur explains the gigantism among duck-billed dinosaurs // Palaeontology. V. 63. № 4. P. 579–599. https://doi.org/10.1111/pala.12473
  67. Smirina E. M., Tsellarius A. Yu., 1996. Aging, longevity, and growth of the desert monitor (Varanus griseus Daud.) // Russian Journal of Herpetology. V. 3. P. 130–142.
  68. Smirina E. M., Tsellarius A. Yu., 1998. Vital bone marking of desert monitor (Varanus griseus DAUD.) in nature // Russian Journal of Herpetology. V. 5. P. 157–160.
  69. Snover M. L., Avens L., Hohn A. A., 2007. Back-calculating length from skeletal growth marks in loggerhead sea turtles Caretta caretta // Endangered Species Research. V. 3. P. 95–104.
  70. Snover M. L., Hohn A. A., Goshe L. R., Balazs G. H., 2011. Validation of annual skeletal marks in green sea turtles Chelonia mydas using tetracycline labeling // Aquat. Biol. V. 12. P. 197–204.
  71. Steel L., 2008. The palaeohistology of pterosaur bone: an overview // Flugsaurier: pterosaur papers in honour of Peter Wellnhofer. Zitteliana, Series B, V. 28. Special volume, Buffetaut E., Hone D. W.E., (Eds). P. 109– 125.
  72. Stein K., Csiki Z., Rogers K. C., Weishampel D. B., Redelstorff R., Carbadillo J. L., Sander P. M., 2010. Small body size and extreme cortical bone remodeling indicate phyletic dwarfism in Magyarosaurus dacus (Sauropoda: Titanosauria) // Proc. Nat. Acad. Sci. V. 107. № 20. P. 9258–9263.
  73. Stein K., Prondvai E., 2014. Rethinking the nature of fibrolamellar bone: an integrative biological revision of sauropod plexiform bone formation // Biol. Rev. V. 89. P. 24–47.
  74. Veitschegger K., Kolb C., Amson E., Scheyer T. M., Sa´nchez-Villagra M.R., 2018. Palaeohistology and life history evolution in cave bears, Ursus spelaeus sensu lato // PLoS ONE. V. 13. № 11. e0206791. https://doi.org/10.1371/journal.pone.0206791
  75. Wagner A., Schabensberger R., Sztatecsny M., Kaiser R., 2011. Skeletochronology of phalanges underestimates the true age of long-lived Alpine newts (Ichthyosaura alpestris) // Herpetological Journal. V. 21. P. 145–148.
  76. Watanabe J., Matsuoka H., 2013. Ontogenetic change of morphology and surface texture of long bones in the gray heron (Ardea cinerea, Ardeidae) // Paleornithological Research. V. 2013. P. 279–306.
  77. Woodward H. N., Horner J. R., Farlow J. O., 2011. Osteohistological evidence for determinate growth in the American Alligator // J. Herpetol. V. 45. P. 339–342. https://doi. org/10.1670/10–274.1.
  78. Woodward H. N., Horner J. R., Farlow J. O., 2014. Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology // Peer J. V. 2. e422. https://doi.org/10.7717/peerj.422
  79. Woodward H. N., Padian K., Lee A. H., 2013. Skeletochronology // Bone histology of fossil tetrapods – advancing methods, analysis and interpretation. Padian K., Lamm E.-T. (Eds). Berkeley. University of California Press. P. 195–215.
  80. Woodward B. H., Freedman F. L., Farlow J., Horner J., 2015. Maiasaura, a model organism for extinct vertebrate population biology: A large sample statistical assessment of growth dynamics and survivorship // Paleobiology. V. 41. P. 1–25. 10.1017/pab.2015.19.

Supplementary files

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2. Fig. 1. Diagram of a cross-section of a tetrapod bone limb showing growth marks (including double LAGs), histological markers (external fundamental system, reduction of the distance between growth marks) and their corresponding events in ontogenesis.

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3. Fig. 2. A diagram of a cross-section of a tetrapod limb bone showing growth marks, histological markers (external fundamental system, changes in the type of bone matrix and vascularization, external and internal circular layers) and their corresponding events in ontogenesis.

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4. Fig. 3. Diagram of ontogenetic changes in the bones of tetrapod limbs associated with secondary remodeling.

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5. Fig. 4. Cross sections of the limb bones of fossil tetrapods in normal (A) and polarized light with a wave plate (B–E). A is a primitive Early Cretaceous stem salamander Kulgeriherpeton ultimum, a section of the humerus at the level of the middle of the diaphysis (see Skutschas et al., 2024). The absence of a reduction in the distance between cyclic growth marks indicates that this humerus belonged to an actively growing animal that had not yet reached the maximum individual age. Also pay attention to the presence of double LAGs. The yellow arrows indicate the height marks. B is a primitive Late Cretaceous cryptobranchid salamander Eoscapherpeton asiaticum, a section of the femur at the level of the middle of the diaphysis (see Skutschas et al., 2019). Pay attention to the network of vascular channels in the primary cortex, which appears in the late stages of ontogenesis. B – late Permian pareiasaurus Deltavjatia rossica, a section of the tibia of an individual that reached less than 25% of the maximum

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6. Fig. 5. Cross sections of limb bones and ribs of fossil tetrapods in polarized light with a wave plate. A is a Late Cretaceous duckbilled dinosaur, a section of the femur (see Bapinaev et al., 2023). The cortex is entirely formed by secondary osteons – there was a complete replacement of the primary periostelial bone with a secondary bone with the formation of a dense Haversoid bone, therefore, the animal is an adult. B – Late Jurassic Stegosaurus, rib section. Pay attention to the secondary trabeculae formed by the lamellar bone. B is a Late Cretaceous basal ornithomimid, a section of the femur of a large individual (see Skutschas et al., 2017). The cortex is entirely formed by secondary osteons – there was a complete replacement of the primary periostelial bone with a secondary bone with the formation of a dense Haversoid bone, therefore, the animal is an adult. G – Late Cretaceous pterosaur Azhdarcho lancicollis, a section of limb bone. The presence of both external and internal circular layers of evidence

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