Paleobiological implications of the bone histology of the extinct Australian marsupial Nimbadon lavarackorum

Abstract Despite the recognition that bone histology provides much information about the life history and biology of extinct animals, osteohistology of extinct marsupials is sorely lacking. We studied the bone histology of the ca. 15-million-year-old Nimbadon lavarackorum from Australia to obtain insight into its biology. The histology of thin sections of five femora and five tibiae of juveniles, subadult, and adult Nimbadon lavarackorum was studied. Growth marks in the bones suggest that N. lavarackorum took at least 7–8 years (and likely longer) to reach skeletal maturity. The predominant bone tissue during early ontogeny is parallel-fibered bone, whereas an even slower rate of bone formation is indicated by the presence of lamellar bone tissue in the periosteal parts of the compacta in older individuals. Deposition of bone was interrupted periodically by lines of arrested growth or annuli. This cyclical growth strategy indicates that growth in N. lavarackorum was affected by the prevailing environmental conditions and available resources, as well as seasonal physiological factors such as decreasing body temperatures and metabolic rates.

[1]  N. Bennett,et al.  Bone remodeling in the longest living rodent, the naked mole‐rat: Interelement variation and the effects of reproduction , 2021, Journal of anatomy.

[2]  N. Bennett,et al.  Long bone histomorphogenesis of the naked mole‐rat: Histodiversity and intraspecific variation , 2020, Journal of anatomy.

[3]  Serdar Mayda,et al.  Bone histology, palaeobiology, and early diagenetic history of extinct equids from Turkey , 2020, Quaternary Research.

[4]  N. Warburton,et al.  Ontogenetic growth and the development of a unique fibrocartilage entheses in Macropus fuliginosus. , 2020, Zoology.

[5]  J. A. Nyakatura,et al.  Evolution of bone cortical compactness in slow arboreal mammals , 2020, bioRxiv.

[6]  A. Herries,et al.  Humerus midshaft histology in a modern and fossil wombat , 2020 .

[7]  U. Göhlich,et al.  Bone histology yields insights into the biology of the extinct elephant birds (Aepyornithidae) from Madagascar , 2020 .

[8]  T. Gaudin,et al.  Ontogenetic changes in the long bone microstructure in the nine-banded armadillo (Dasypus novemcinctus) , 2019, PloS one.

[9]  J. A. Nyakatura,et al.  Bone cortical compactness in ‘tree sloths’ reflects convergent evolution , 2018, Journal of anatomy.

[10]  L. Legendre,et al.  Digging the compromise: investigating the link between limb bone histology and fossoriality in the aardvark (Orycteropus afer) , 2018, PeerJ.

[11]  Michał M Kłosowski,et al.  Limb bone scaling in hopping macropods and quadrupedal artiodactyls , 2018, bioRxiv.

[12]  J. Hume,et al.  Bone histology sheds new light on the ecology of the dodo (Raphus cucullatus, Aves, Columbiformes) , 2017, Scientific Reports.

[13]  J. Hume,et al.  Bone histology sheds new light on the ecology of the dodo (Raphus cucullatus, Aves, Columbiformes) , 2017, Scientific Reports.

[14]  M. Archer,et al.  The identification of Oligo-Miocene mammalian palaeocommunities from the Riversleigh World Heritage Area, Australia and an appraisal of palaeoecological techniques , 2017, PeerJ.

[15]  I. Dohoo,et al.  Skeletal fluorosis in marsupials: A comparison of bone lesions in six species from an Australian industrial site. , 2017, The Science of the total environment.

[16]  M. Archer,et al.  Patterns in the history of Australia's mammals and inferences about palaeohabitats , 2017 .

[17]  A. Chinsamy,et al.  Long bone histology of the subterranean rodent Bathyergus suillus (Bathyergidae): ontogenetic pattern of cortical bone thickening , 2017, Journal of anatomy.

[18]  A. Forasiepi,et al.  Mammalian bone palaeohistology: a survey and new data with emphasis on island forms , 2015, PeerJ.

[19]  V. Slon,et al.  Hyperostotic bone disease in a wombat (Vombatus ursinus). , 2014, Research in veterinary science.

[20]  M. Archer,et al.  Reconstructing a Miocene pitfall trap: Recognition and interpretation of fossiliferous Cenozoic palaeokarst , 2014 .

[21]  X. Jordana,et al.  Bone histology as an approach to providing data on certain key life history traits in mammals: Implications for conservation biology , 2013 .

[22]  R. Macphee,et al.  Evolutionary Patterns of Bone Histology and Bone Compactness in Xenarthran Mammal Long Bones , 2013, PloS one.

[23]  G. Shaw.  The naturalist's miscellany or coloured figures of natural objects , 2013 .

[24]  V. Buffrénil,et al.  Microstructure and Mineralization of Vertebrate Skeletal Tissues , 2013 .

[25]  M. Archer,et al.  Herds Overhead: Nimbadon lavarackorum (Diprotodontidae), Heavyweight Marsupial Herbivores in the Miocene Forests of Australia , 2012, PloS one.

[26]  J. A. Nyakatura,et al.  The Convergent Evolution of Suspensory Posture and Locomotion in Tree Sloths , 2012, Journal of Mammalian Evolution.

[27]  X. Jordana,et al.  Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology , 2012, Nature.

[28]  M. Archer,et al.  Early to middle Miocene monsoon climate in Australia: COMMENT , 2012 .

[29]  S. Maloney,et al.  Minimum daily core body temperature in western grey kangaroos decreases as summer advances: a seasonal pattern, or a direct response to water, heat or energy supply? , 2011, Journal of Experimental Biology.

[30]  Michael Archer,et al.  Palaeoecological analyses of Riversleigh's Oligo-Miocene sites: Implications for Oligo-Miocene climate change in Australia , 2009 .

[31]  A. Zihlman,et al.  Regional variability in secondary remodeling within long bone cortices of catarrhine primates: the influence of bone growth history , 2008, Journal of anatomy.

[32]  A. Chinsamy-Turan.  The Microstructure of Dinosaur Bone: Deciphering Biology with Fine-Scale Techniques , 2005 .

[33]  M. Girondot,et al.  BONE PROFILER: A TOOL TO QUANTIFY, MODEL, AND STATISTICALLY COMPARE BONE-SECTION COMPACTNESS PROFILES , 2003 .

[34]  J. M. Starck,et al.  Bone microstructure and developmental plasticity in birds and other dinosaurs , 2002, Journal of morphology.

[35]  E. de Margerie,et al.  Bone typology and growth rate: testing and quantifying 'Amprino's rule' in the mallard (Anas platyrhynchos). , 2002, Comptes rendus biologies.

[36]  E. A. Tonna,et al.  A comparative histological study of mammalian bone , 1974, Journal of morphology.

[37]  C. P. Gandal.  AGE DETERMINATION IN MAMMALS , 1954 .

[38]  M. Archer,et al.  Developing a radiometrically-dated chronologic sequence for Neogene biotic change in Australia, from the Riversleigh World Heritage Area of Queensland , 2016 .

[39]  Huqiang Zhang,et al.  The Australian Summer Monsoon in Current and Future Climate , 2016 .

[40]  S. Werning.  Evolution of Bone Histological Characters in Amniotes, and the Implications for the Evolution of Growth and Metabolism , 2013 .

[41]  M. Archer,et al.  The Rise of Australian Marsupials: A Synopsis of Biostratigraphic, Phylogenetic, Palaeoecologic and Palaeobiogeographic Understanding , 2012 .

[42]  Maria Seton,et al.  Early to Middle Miocene monsoon climate in Australia , 2011 .

[43]  M. Archer,et al.  NIMBADON, A NEW GENUS AND THREE NEW SPECIES OFTERTIARY ZYGOMATURINES (MARSUPIALIA: DIPROTODONTIDAE) FROM NORTHERN AUSTRALIA, WITH A REASSESSMENT OF NEOHELOS , 2006 .

[44]  J. Hurum,et al.  Bone microstructure and growth patterns of early mammals , 2006 .

[45]  Griffith,et al.  General Zoology Or Systematic Natural History , 1999 .

[46]  Anusuya Chinsamy,et al.  Preparation of fossil bone for histological examination , 1992 .

[47]  S. E. Kleĭnenberg,et al.  Age determination of mammals from annual layers in teeth and bones , 1969 .

[48]  A. Hrdlička,et al.  A contribution to the comparative histology of the femur , 2022 .