FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / PLoS One / Limb bone histology records birth in mammals.
PloS one2018; 13(6); e0198511; doi: 10.1371/journal.pone.0198511

Limb bone histology records birth in mammals.

Abstract: The annual cyclicality of cortical bone growth marks (BGMs) allows reconstruction of some important life history traits, such as longevity, growth rate or age at maturity. Little attention has been paid, however, to non-cyclical BGMs, though some record key life history events such as hatching (egg-laying vertebrates), metamorphosis (amphibians), or weaning (suggested for Microcebus and the hedgehog). Here, we investigate the relationship between non-cyclical BGMs and a stressful biological event in mammals: the moment of birth. In the present study, we histologically examine ontogenetic series of femora, tibiae and metapodia in several extant representatives of the genus Equus (E. hemionus, E. quagga and E. grevyi). Our analysis reveals the presence of a non-cyclical growth mark that is deposited around the moment of birth, analogous to the neonatal line described for teeth. We therefore refer to it as neonatal line. The presence of this feature within the bone cross-section agrees with a period of growth arrest in newborn foals regulated by the endocrine system. The neonatal line is accompanied by modifications in bone tissue type and vascularization, and has been identified in all bones studied and at different ontogenetic ages. Our discovery of a non-cyclical BGM related to the moment of birth in mammals is an important step towards the histological reconstruction of life histories in extant and fossil equids.
Get Full Text
Publication Date: 2018-06-20 PubMed ID: 29924818PubMed Central: PMC6010216DOI: 10.1371/journal.pone.0198511Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research investigates the existence of specific bone growth marks (BGMs) in mammals that indicate the time of birth. The study examines bones from different members of the Equus genus, revealing the presence of a non-cyclical neonatal line similar to that found in teeth.

Introduction

  • The research focuses on cortical bone growth marks (BGMs), marks left on bones as creatures grow. While these are usually studied for cyclical nature which allow for tracking traits like ages at maturity, growth rate and longevity.
  • However, this research honed in on non-cyclical BGMs that signal specific life events. In the case of this study, the life event was birth in mammals.

Methodology

  • The researchers examined a series of bones – specifically femora, tibiae, and metapodia – from several species grouped in the genus Equus, which includes horses and zebras.
  • The aim was to discover if there was a growth mark or a change in the bone around the time of birth similar to the neonatal line found in teeth.

Findings

  • Examination revealed non-cyclical growth marks (termed as the neonatal line, analogous to similar features in teeth) related to the time of birth.
  • This neonatal line concurred with a period of growth cessation in newborn foals, thought to be regulated by their endocrine system.
  • Accompanying the neonatal line were alterations in the bone tissue type and level of vascularization (the formation of blood vessels).
  • This neonatal line was present in all the bones studied and at varying stages of growth.

Conclusion

  • The researchers concluded that the presence of a non-cyclical BGM related to birth was significant as it provides an opportunity for the histological reconstruction of life histories in both extinct and existing equids.
  • This could open new possibilities for understanding the life histories, growth patterns and even evolutionary paths of not just equids, but possibly also of other mammals.

Cite This Article

APA
Nacarino-Meneses C, Köhler M. (2018). Limb bone histology records birth in mammals. PLoS One, 13(6), e0198511. https://doi.org/10.1371/journal.pone.0198511

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 13
Issue: 6
Pages: e0198511
PII: e0198511

Researcher Affiliations

Nacarino-Meneses, Carmen
  • Department of Evolutionary Paleobiology, Institut Català de Paleontologia Miquel Crusafont (ICP), Campus de la Universitat Autònoma de Barcelona, Bellaterra, Barcelona, Spain.
Köhler, Meike
  • Department of Evolutionary Paleobiology, Institut Català de Paleontologia Miquel Crusafont (ICP), Campus de la Universitat Autònoma de Barcelona, Bellaterra, Barcelona, Spain.
  • ICREA, Barcelona, Spain.

MeSH Terms

  • Animals
  • Animals, Newborn
  • Bone Development
  • Female
  • Femur / metabolism
  • Femur / pathology
  • Horses
  • Male
  • Metacarpus / metabolism
  • Metacarpus / pathology
  • Tibia / metabolism
  • Tibia / pathology

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 81 references
  1. de Margerie E, Cubo J, Castanet J. Bone typology and growth rate: testing and quantifying 'Amprino's rule' in the mallard (Anas platyrhynchos).. C R Biol 2002 Mar;325(3):221-30.
    doi: 10.1016/S1631-0691(02)01429-4pubmed: 12017770google scholar: lookup
  2. Cubo J, le Roy N, Martinez-Maza C, Montes L. Paleohistological estimation of bone growth rate in extinct archosaurs. Paleobiology 2012;38: 335–349.
    doi: 10.5061/dryad.j2m25n82google scholar: lookup
  3. Lee AH, Huttenlocker AK, Padian K, Woodward HN. Analysis of Growth Rates. 2013. pp. 217–251.
  4. Padian K, de Ricqlès AJ, Horner JR. Dinosaurian growth rates and bird origins.. Nature 2001 Jul 26;412(6845):405-8.
    doi: 10.1038/35086500pubmed: 11473307google scholar: lookup
  5. Castanet J, Croci S, Aujard F, Perret M, Cubo J, de Margerie E. Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus. J Zool 2004;263: 31–39.
    doi: 10.1017/S0952836904004844google scholar: lookup
  6. Köhler M, Moyà-Solà S. Physiological and life history strategies of a fossil large mammal in a resource-limited environment.. Proc Natl Acad Sci U S A 2009 Dec 1;106(48):20354-8.
    doi: 10.1073/pnas.0813385106pmc: PMC2777955pubmed: 19918076google scholar: lookup
  7. Nacarino-Meneses C, Jordana X, Köhler M. First approach to bone histology and skeletochronology of Equus hemionus. Comptes Rendus—Palevol 2016;15: 267–277.
    doi: 10.1016/j.crpv.2015.02.005google scholar: lookup
  8. Woodward HN, Freedman Fowler EA, Farlow JO, Horner JR. Maiasaura, a model organism for extinct vertebrate population biology: a large sample statistical assessment of growth dynamics and survivorship. Paleobiology 2015;41: 503–527.
    doi: 10.1017/pab.2015.19google scholar: lookup
  9. Köhler M. Fast or slow? The evolution of life history traits associated with insular dwarfing. 2010. pp. 261–280.
  10. Marín-Moratalla N, Jordana X, Köhler M. Bone histology as an approach to providing data on certain key life history traits in mammals: Implications for conservation biology. Mamm Biol 2013;78: 422–429.
    doi: 10.1016/j.mambio.2013.07.079google scholar: lookup
  11. Nacarino-Meneses C, Jordana X, Köhler M. Histological variability in the limb bones of the Asiatic wild ass and its significance for life history inferences.. PeerJ 2016;4:e2580.
    doi: 10.7717/peerj.2580pmc: PMC5068390pubmed: 27761353google scholar: lookup
  12. Jordana X, Marín-Moratalla N, Moncunill-Solé B, Nacarino-Meneses C, Köhler M. Ontogenetic changes in the histological features of zonal bone tissue of ruminants: A quantitative approach. Comptes Rendus—Palevol 2016;15: 255–266.
    doi: 10.1016/j.crpv.2015.03.008google scholar: lookup
  13. Chinsamy A, Valenzuela N. Skeletochronology of the endangered side-neck turtles Podocnemis expansa. S Afr J Sci 2008;104: 311–314.
  14. Castanet J, Rogers KC, Cubo J, Boisard JJ. Periosteal bone growth rates in extant ratites (ostriche and emu). Implications for assessing growth in dinosaurs.. C R Acad Sci III 2000 Jun;323(6):543-50.
    doi: 10.1016/S0764-4469(00)00181-5pubmed: 10923210google scholar: lookup
  15. Chinsamy-Turan A. The microstructure of dinosaur bone. Deciphering biology with fine-scale techniques. 2005.
  16. Huttenlocker AK, Woodward HN, Hall BK. The biology of bone. 2013. pp. 13–34.
    doi: 10.1007/s13398-014-0173-7.2google scholar: lookup
  17. Amprino R. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l’accroissement. Arch Biol 1947;58: 315–330.
  18. Marín-Moratalla N, Cubo J, Jordana X, Moncunill-Solé B, Köhler M. Correlation of quantitative bone histology data with life history and climate: A phylogenetic approach. Biol J Linn Soc 2014;112: 678–687.
    doi: 10.1111/bij.12302google scholar: lookup
  19. Orlandi-Oliveras G, Jordana X, Moncunill-Solé B, Köhler M. Bone histology of the giant fossil dormouse Hypnomys onicensis (Gliridae, Rodentia) from Balearic Islands. Comptes Rendus—Palevol 2016;15: 238–244.
    doi: 10.1016/j.crpv.2015.05.001google scholar: lookup
  20. Woodward HN, Padian K, Lee AH. Skeletochronology. 2013. pp. 195–215.
  21. Moncunill-Solé B, Orlandi-Oliveras G, Jordana X, Rook L, Köhler M. 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 2016;15: 227–237.
    doi: 10.1016/j.crpv.2015.04.004google scholar: lookup
  22. Köhler M, Marín-Moratalla N, Jordana X, Aanes R. Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology.. Nature 2012 Jul 19;487(7407):358-61.
    doi: 10.1038/nature11264pubmed: 22763443google scholar: lookup
  23. Castanet J, Francillon-Vieillot H, Meunier F, Ricqlès A. Bone and individual aging. 1993. pp. 245–283.
  24. Castanet J. Time recording in bone microstructures of endothermic animals; functional relationships. Comptes Rendus—Palevol 2006;5: 629–636.
    doi: 10.1016/j.crpv.2005.10.006google scholar: lookup
  25. Martin RB, Burr DB, Sharkey NA. Skeletal tissue mechanics. 1998.
  26. Currey JD. Bones. Structure and mechanics. 2002.
    doi: 10.1016/B978-0-12-801238-3.03760–0google scholar: lookup
  27. Bruce RC, Castanet J. Application of skeletochronology in aging larvae of the salamanders Gyrinophilus porphyriticus and Pseudotriton ruber. J Herpetol 2006;40: 85–90.
    doi: 10.1670/42-05N.1google scholar: lookup
  28. Castanet J, Baéz M. Adaptation and evolution in Gallotia lizards from the Canary Islands: age, growth, maturity and longevity. Amphibia-Reptilia 1991;12: 81–102.
    doi: 10.1163/156853891X00356google scholar: lookup
  29. Chinsamy A, Hurum JH. Bone microstructure and growth patterns of early mammals. Acta Palaeontol Pol 2006;51: 325–338.
  30. Hugi J, Sánchez-Villagra MR. Life history and skeletal adaptations in the galapagos marine iguana (Amblyrhynchus cristatus) as reconstructed with bone histological data—A comparative study of iguanines. J Herpetol 2012;46: 312–324.
    doi: 10.1670/11-071google scholar: lookup
  31. Sinsch U. Review: Skeletochronological assessment of demographic life-history traits in amphibians. Herpetol J 2015;25: 5–13.
  32. Olgun K, Uzum N, Avci A, Miaud C. Age, size and growth of the southern Triturus karelinii in a population from Turkey. Amphibia-Reptilia 2005;26: 223–230.
    doi: 10.1163/1568538054253465google scholar: lookup
  33. Hemelaar A. An improved method to estimate the number of year rings resorbed in phalanges of Bufo bufo (L.) and its application to populations from different latitudes and altitudes. Amphib Publ Soc Eur Herpetol 1985;6: 323–341.
    doi: 10.1016/j.ijhydene.2008.11.098google scholar: lookup
  34. Jakob C, Seitz A, Crivelli A, Miaud C. Growth cycle of the marbled newt (Triturus marmoratus) in the Mediterranean region assessed by skeletochronology. Amphibia-Reptilia 2002;23: 407–418.
    doi: 10.1163/15685380260462329google scholar: lookup
  35. Ento K, Matsui M. Estimation of age structure by skeletochronology of a population of Hynobius nebulosus in a breeding season (Amphibia, Urodela).. Zoolog Sci 2002 Feb;19(2):241-7.
    doi: 10.2108/zsj.19.241pubmed: 12012788google scholar: lookup
  36. Esteban M, García-París M, Buckley D, Castanet J. Bone growth and age in Rana saharica, a water frog living in a desert environment. Finnish Zool Bot Publ Board 1999;36: 53–62.
  37. Esteban M, Sánchez-Herráiz MJ, Barbadillo LJ, Castanet J, Márquez R. Effects of age, size and temperature on the advertisement calls of two Spanish populations of Pelodytes punctatus. Amphibia-Reptilia 2002;23: 249–258.
    doi: 10.1163/15685380260449135google scholar: lookup
  38. Khonsue W, Matsui M, Hirai T, Misawa Y. A comparison of age structures in two populations of a pond frog Rana nigromaculata (Amphibia: Anura). Zoolog Sci 2001;18: 597–603.
    doi: 10.2108/zsj.18.597google scholar: lookup
  39. Morris P. A method for determining absolute age in the hedgehog. J Zool 1970;161: 277–281.
    doi: 10.1111/j.1469-7998.1970.tb02043.xgoogle scholar: lookup
  40. Nowak RM. Walker’s mammals of the world. 1999.
  41. Ernest SKM. Life history characteristics of placental nonvolant mammals. Ecology 2003;84: 3402.
    doi: 10.1890/11-1341.1google scholar: lookup
  42. King SRB, Moehlman PD. Equus quagga. IUCN Red List Threat Species 2016; e.T41013A45172424.
  43. Kaczensky P, Lkhagvasuren B, Pereladova O, Hemami M, Bouskila A. Equus hemionus. IUCN Red List Threat Species 2015;e.T7951A45.
  44. Rubenstein D, Low Mackey B, Davidson Z, Kebede F, King SR. Equus grevyi. IUCN Red List Threat Species 2016; e.T7950A89624491.
  45. Schöpke K, Stubbe A, Stubbe M, Batsaikhan N, Schafberg R. Morphology and variation of the Asiatic wild ass (Equus hemionus hemionus). Erforsch Biol Ressourcen der Mongolei 2012;12: 77–84.
  46. Lkhagvasuren D, Ansorge H, Samiya R, Schafberg R, Stubbe A, Stubbe M. Age determination of the Mongolian wild ass (Equus hemionus Pallas, 1775) by the dentition patterns and annual lines in the tooth cementum. J Species Res 2013;2: 85–90.
    doi: 10.12651/JSR.2013.2.1.085google scholar: lookup
  47. Smuts GL. Age determination in Burchell’s zebra (Equus burchelli antiquorum) from the Kruger National Park. J South african Wildl Manag Assoc 1974;4: 103–105.
  48. Silver IA. The aging of domestic animals. 1963. pp. 250–268.
  49. Penzhorn BL. Age determination in cape mountain zebras Equus zebra zebra in the Mountain Zebra National Park. Koedoe 1982;25: 89–102.
  50. Nacarino-Meneses C, Jordana X, Orlandi-Oliveras G, Köhler M. Reconstructing molar growth from enamel histology in extant and extinct Equus.. Sci Rep 2017 Nov 21;7(1):15965.
    doi: 10.1038/s41598-017-16227-2pmc: PMC5698294pubmed: 29162890google scholar: lookup
  51. Lamm E-T. Preparation and sectioning of specimens. 2013. pp. 55–160.
  52. Turner-Walker G, Mays S. Histological studies on ancient bone. 2008. pp. 121–146.
    doi: 10.1002/9780470724187.ch7google scholar: lookup
  53. Zuckerman S. The breeding seasons of mammals in captivity. J Zool 1952;122: 827–950.
  54. Francillon-Vieillot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ, Sire JY. Microstructure and mineralization of vertebrate skeletal tissues. 1990. pp. 471–530.
  55. Prondvai E, Stein KHW, de Ricqlès A, Cubo J. Development-based revision of bone tissue classification: the importance of semantics for science. Biol J Linn Soc 2014;112: 799–816.
    doi: 10.1111/bij.12323google scholar: lookup
  56. Fellows I. Deducer: A Data Analysis GUI for R. J Stat Softw 2012;49: 1–15.
  57. Dytham C. Choosing and Using Statistics: A Biologist’s Guide. 2011.
  58. Smith TM, Reid DJ, Sirianni JE. The accuracy of histological assessments of dental development and age at death.. J Anat 2006 Jan;208(1):125-38.
    doi: 10.1111/j.1469-7580.2006.00500.xpmc: PMC2100178pubmed: 16420385google scholar: lookup
  59. Carlson SJ. Vertebrate dental structures. 1990. pp. 235–260.
  60. Tafforeau P, Bentaleb I, Jaeger J-J, Martin C. Nature of laminations and mineralization in rhinoceros enamel using histology and X-ray synchrotron microtomography: Potential implications for palaeoenvironmental isotopic studies. Palaeogeogr Palaeoclimatol Palaeoecol 2007;246: 206–227.
    doi: 10.1016/j.palaeo.2006.10.001google scholar: lookup
  61. Schour I. The neonatal line in the enamel and dentin of the human deciduous teeth and first permanent molar. J Am Dent Assoc 1936;23: 1946–1955.
    doi: 10.14219/jada.archive.1936.0277google scholar: lookup
  62. Weber DF, Eisenmann DR. Microscopy of the neonatal line in developing human enamel.. Am J Anat 1971 Nov;132(3):375-91.
    doi: 10.1002/aja.1001320307pubmed: 4940143google scholar: lookup
  63. Martinez-Maza C, Alberdi MT, Nieto-Diaz M, Prado JL. Life-history traits of the Miocene Hipparion concudense (Spain) inferred from bone histological structure.. PLoS One 2014;9(8):e103708.
    doi: 10.1371/journal.pone.0103708pmc: PMC4123897pubmed: 25098950google scholar: lookup
  64. Stearns SC. The evolution of life histories. 1992.
  65. Anderson JF, Hall‐Martin A, Russell DA. Long‐bone circumference and weight in mammals, birds and dinosaurs. J Zool 1985;207: 53–61.
    doi: 10.1111/j.1469-7998.1985.tb04915.xgoogle scholar: lookup
  66. Damuth J, MacFadden BJ. Body size in mammalian Paleobiology Estimations and biological implications. 1990.
  67. Tacutu R, Craig T, Budovsky A, Wuttke D, Lehmann G, Taranukha D, Costa J, Fraifeld VE, de Magalhães JP. Human Ageing Genomic Resources: integrated databases and tools for the biology and genetics of ageing.. Nucleic Acids Res 2013 Jan;41(Database issue):D1027-33.
    doi: 10.1093/nar/gks1155pmc: PMC3531213pubmed: 23193293google scholar: lookup
  68. Churcher C. Equus grevyi. Mamm Species 1993;453: 1–9.
  69. Fowden AL, Forhead AJ, Ousey JC. Endocrine adaptations in the foal over the perinatal period.. Equine Vet J Suppl 2012 Feb;(41):130-9.
    doi: 10.1111/j.2042-3306.2011.00460.xpubmed: 22594041google scholar: lookup
  70. Stewart F, Goode JA, Allen WR. Growth hormone secretion in the horse: unusual pattern at birth and pulsatile secretion through to maturity.. J Endocrinol 1993 Jul;138(1):81-9.
    pubmed: 7852896doi: 10.1677/joe.0.1380081google scholar: lookup
  71. Messer NT, Riddle WT, Traub-Dargatz JL, Dargatz DA, Refsal KJ, Thompson DL Jr.. Thyroid hormone levels in thoroughbred mares and their foals at parturition. AAEP Proc 1998;44: 248–251.
  72. Buchanan CR, Preece MA. Hormonal control of bone growth. 1992. pp. 53–89.
  73. Kim HY, Mohan S. Role and Mechanisms of Actions of Thyroid Hormone on the Skeletal Development.. Bone Res 2013 Jun;1(2):146-61.
    doi: 10.4248/BR201302004pmc: PMC4472099pubmed: 26273499google scholar: lookup
  74. Curry Rogers K, Whitney M, D'Emic M, Bagley B. Precocity in a tiny titanosaur from the Cretaceous of Madagascar.. Science 2016 Apr 22;352(6284):450-3.
    pubmed: 27102482doi: 10.1126/science.aaf1509google scholar: lookup
  75. Case TJ. On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates.. Q Rev Biol 1978 Sep;53(3):243-82.
    pubmed: 362471doi: 10.1086/410622google scholar: lookup
  76. Calder WAI. Size, Function and Life History. 1984.
  77. Peters RH. The ecological implications of body size. 1983.
  78. Curtin AJ, Macdowell AA, Schaible EG, Curtin AJ, Macdowell AA, Schaible EG. Noninvasive histological comparison of bone growth patterns among fossil and extant neonatal elephantids using synchrotron radiation x-ray microtomography. J Vertebr Paleontol 2012;32: 939–955.
  79. Stover SM, Pool RR, Martin RB, Morgan JP. Histological features of the dorsal cortex of the third metacarpal bone mid-diaphysis during postnatal growth in thoroughbred horses.. J Anat 1992 Dec;181 ( Pt 3)(Pt 3):455-69.
    pmc: PMC1259699pubmed: 1304584
  80. de Margerie E. Laminar bone as an adaptation to torsional loads in flapping flight.. J Anat 2002 Dec;201(6):521-6.
    doi: 10.1046/j.1469-7580.2002.00118.xpmc: PMC1570990pubmed: 12489764google scholar: lookup
  81. de Margerie E, Robin JP, Verrier D, Cubo J, Groscolas R, Castanet J. Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus).. J Exp Biol 2004 Feb;207(Pt 5):869-79.
    doi: 10.1242/jeb.00841pubmed: 14747417google scholar: lookup

Citations

This article has been cited 21 times.
  1. Chinsamy A. Palaeoecological deductions from osteohistology. Biol Lett 2023 Aug;19(8):20230245.
    doi: 10.1098/rsbl.2023.0245pubmed: 37607578google scholar: lookup
  2. Bhat MS, Chinsamy A, Parkington J. Bone histology of Neogene angulate tortoises (Testudines: Testudinidae) from South Africa: palaeobiological and skeletochronological implications. R Soc Open Sci 2023 Mar;10(3):230064.
    doi: 10.1098/rsos.230064pubmed: 36908987google scholar: lookup
  3. Jannello JM, Chinsamy A. Osteohistology and palaeobiology of giraffids from the Mio-Pliocene Langebaanweg (South Africa). J Anat 2023 May;242(5):953-971.
    doi: 10.1111/joa.13825pubmed: 36748181google scholar: lookup
  4. Funston GF, dePolo PE, Sliwinski JT, Dumont M, Shelley SL, Pichevin LE, Cayzer NJ, Wible JR, Williamson TE, Rae JWB, Brusatte SL. The origin of placental mammal life histories. Nature 2022 Oct;610(7930):107-111.
    doi: 10.1038/s41586-022-05150-wpubmed: 36045293google scholar: lookup
  5. Tomassini RL, Pesquero MD, Garrone MC, Marin-Monfort MD, Cerda IA, Prado JL, Montalvo CI, Fernández-Jalvo Y, Alberdi MT. First osteohistological and histotaphonomic approach of Equus occidentalis Leidy, 1865 (Mammalia, Equidae) from the late Pleistocene of Rancho La Brea (California, USA). PLoS One 2021;16(12):e0261915.
    doi: 10.1371/journal.pone.0261915pubmed: 34962948google scholar: lookup
  6. Köhler M, Herridge V, Nacarino-Meneses C, Fortuny J, Moncunill-Solé B, Rosso A, Sanfilippo R, Palombo MR, Moyà-Solà S. Palaeohistology reveals a slow pace of life for the dwarfed Sicilian elephant. Sci Rep 2021 Nov 24;11(1):22862.
    doi: 10.1038/s41598-021-02192-4pubmed: 34819557google scholar: lookup
  7. Kulik ZT, Lungmus JK, Angielczyk KD, Sidor CA. Living fast in the Triassic: New data on life history in Lystrosaurus (Therapsida: Dicynodontia) from northeastern Pangea. PLoS One 2021;16(11):e0259369.
    doi: 10.1371/journal.pone.0259369pubmed: 34739492google scholar: lookup
  8. Calderón T, Arnold W, Stalder G, Painer J, Köhler M. Labelling experiments in red deer provide a general model for early bone growth dynamics in ruminants. Sci Rep 2021 Jul 7;11(1):14074.
    doi: 10.1038/s41598-021-93547-4pubmed: 34234258google scholar: lookup
  9. Becker M, Witzel C, Kierdorf U, Frölich K, Kierdorf H. Ontogenetic changes of tissue compartmentalization and bone type distribution in the humerus of Soay sheep. J Anat 2020 Aug;237(2):334-354.
    doi: 10.1111/joa.13194pubmed: 32255514google scholar: lookup
  10. Calderón T, DeMiguel D, Arnold W, Stalder G, Köhler M. Calibration of life history traits with epiphyseal closure, dental eruption and bone histology in captive and wild red deer. J Anat 2019 Aug;235(2):205-216.
    doi: 10.1111/joa.13016pubmed: 31148188google scholar: lookup
  11. Orlandi-Oliveras G, Nacarino-Meneses C, Koufos GD, Köhler M. Bone histology provides insights into the life history mechanisms underlying dwarfing in hipparionins. Sci Rep 2018 Nov 21;8(1):17203.
    doi: 10.1038/s41598-018-35347-xpubmed: 30464210google scholar: lookup
  12. Chinsamy A, Pereyra ME. Stochastic growth marks in Crocodylus niloticus. Sci Rep 2025 Dec 18;16(1):1811.
    doi: 10.1038/s41598-025-31384-5pubmed: 41413165google scholar: lookup
  13. Delsett LL, Faure-Brac MG, Engelschiøn VS, Houssaye A, Chinsamy A, Hurum JH, Kear BP. Vertebral microstructure marks the emergence of pelagic ichthyosaurs soon after the End Permian Mass Extinction. Sci Rep 2025 Sep 5;15(1):30221.
    doi: 10.1038/s41598-025-14335-ypubmed: 40913021google scholar: lookup
  14. Funston GF, Kynigopoulou Z, Williamson TE, Brusatte SL. Palaeohistology and life history of the early Palaeocene taeniodont Conoryctes comma (Mammalia: Eutheria). J Anat 2025 Sep-Oct;247(3-4):819-841.
    doi: 10.1111/joa.70010pubmed: 40657952google scholar: lookup
  15. Maíllo J, Hidalgo-Sanz J, Gasca JM, Canudo JI, Moreno-Azanza M. Intraskeletal histovariability and skeletochronology in an ornithopod dinosaur from the Maestrazgo Basin (Teruel, Spain). J Anat 2025 Sep-Oct;247(3-4):643-664.
    doi: 10.1111/joa.14225pubmed: 39876055google scholar: lookup
  16. Pereyra ME, Bona P, Siroski P, Chinsamy A. Analyzing the Life History of Caimans: The Growth Dynamics of Caiman latirostris From an Osteohistological Approach. J Morphol 2025 Jan;286(1):e70010.
    doi: 10.1002/jmor.70010pubmed: 39692278google scholar: lookup
  17. Goldsmith ER, Barta DE, Kligman BT, Nesbitt SJ, Marsh AD, Parker WG, Stocker MR. Osteohistological signal from the smallest known phytosaur femur reveals slow growth and new insights into the evolution of growth in Archosauria. J Anat 2025 Sep-Oct;247(3-4):556-575.
    doi: 10.1111/joa.14185pubmed: 39626238google scholar: lookup
  18. Curry Rogers K, Martínez RN, Colombi C, Rogers RR, Alcober O. Osteohistological insight into the growth dynamics of early dinosaurs and their contemporaries. PLoS One 2024;19(4):e0298242.
    doi: 10.1371/journal.pone.0298242pubmed: 38568908google scholar: lookup
  19. Atkins-Weltman KL, Simon DJ, Woodward HN, Funston GF, Snively E. A new oviraptorosaur (Dinosauria: Theropoda) from the end-Maastrichtian Hell Creek Formation of North America. PLoS One 2024;19(1):e0294901.
    doi: 10.1371/journal.pone.0294901pubmed: 38266012google scholar: lookup
  20. Köhler M, Nacarino-Meneses C, Cardona JQ, Arnold W, Stalder G, Suchentrunk F, Moyà-Solà S. Insular giant leporid matured later than predicted by scaling. iScience 2023 Sep 15;26(9):107654.
    doi: 10.1016/j.isci.2023.107654pubmed: 37694152google scholar: lookup
  21. Heck CT, Woodward HN. Intraskeletal bone growth patterns in the North Island Brown Kiwi (Apteryx mantelli): Growth mark discrepancy and implications for extinct taxa. J Anat 2021 Nov;239(5):1075-1095.
    doi: 10.1111/joa.13503pubmed: 34258760google scholar: lookup
Subscribe to our newsletter
Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.