Lacking fur, living in eusocial colonies and having the longest lifespan of any rodent, makes naked mole-rats (NMRs) rather peculiar mammals. Although they exhibit a high degree of polymorphism, skeletal plasticity and are considered a novel model to assess the effects of delayed puberty on the skeletal system, scarce information on their morphogenesis exists. Here, we examined a large ontogenetic sample (n = 76) of subordinate individuals to assess the pattern of bone growth and bone microstructure of fore- and hindlimb bones by using histomorphological techniques. Over 290 undecalcified thin cross-sections from the midshaft of the humerus, ulna, femur, and tibia from pups, juveniles and adults were analyzed with polarized light microscopy. Similar to other fossorial mammals, NMRs exhibited a systematic cortical thickening of their long bones, which clearly indicates a conserved functional adaptation to withstand the mechanical strains imposed during digging, regardless of their chisel-tooth predominance. We describe a high histodiversity of bone matrices and the formation of secondary osteons in NMRs. The bones of pups are extremely thin-walled and grow by periosteal bone formation coupled with considerable expansion of the medullary cavity, a process probably tightly regulated and adapted to optimize the amount of minerals destined for skeletal development, to thus allow the female breeder to produce a higher number of pups, as well as several litters. Subsequent cortical thickening in juveniles involves high amounts of endosteal bone apposition, which contrasts with the bone modeling of other mammals where a periosteal predominance exists. Adults have bone matrices predominantly consisting of parallel-fibered bone and lamellar bone, which indicate intermediate to slow rates of osteogenesis, as well as the development of poorly vascularized lamellar-zonal tissues separated by lines of arrested growth (LAGs) and annuli. These features reflect the low metabolism, low body temperature and slow growth rates reported for this species, as well as indicate a cyclical pattern of osteogenesis. The presence of LAGs in captive individuals was striking and indicates that postnatal osteogenesis and its consequent cortical stratification most likely represents a plesiomorphic thermometabolic strategy among endotherms which has been suggested to be regulated by endogenous rhythms. However, the generalized presence of LAGs in this and other subterranean taxa in the wild, as well as recent investigations on variability of environmental conditions in burrow systems, supports the hypothesis that underground environments experience seasonal fluctuations that may influence the postnatal osteogenesis of animals by limiting the extension of burrow systems during the unfavorable dry seasons and therefore the finding of food resources. Additionally, the intraspecific variation found in the formation of bone tissue matrices and vascularization suggested a high degree of developmental plasticity in NMRs, which may help explaining the polymorphism reported for this species. The results obtained here represent a valuable contribution to understanding the relationship of several aspects involved in the morphogenesis of the skeletal system of a mammal with extraordinary adaptations.

Department of Biological Sciences University of Cape Town Cape Town South Africa

Department of Pharmaceutical Sciences Northeast Ohio Medical University Rootstown OH USA

Department of Zoology Faculty of Science University of South Bohemia České Budějovice Czech Republic

Mammal Research Institute Department of Zoology and Entomology University of Pretoria Pretoria South Africa

Zobrazit více v PubMed

Allen, M. & Burr, D. (2014) Bone modeling and remodeling (Ch. 4). In: Burr, D.B. & Allen, M. (Eds.) Basic and applied bone biology. London: Academic Press, Elsevier, pp. 373.

Amprino, R. (1947) La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l’accroissement. Archives of Biology, 58, 315–330.

Artwohl, J. , Hill, T. , Comer, C. & Park, T. (2002) Naked mole‐rats: unique opportunities and husbandry challenges. Laboratory Animals, 148, 185–189. PubMed

Bach‐Gansmo, F.L. , Irvine, S.C. , Brüel, A. , Thomsen, J.S. & Birkedal, H. (2013) Calcified cartilage islands in rat cortical bone. Calcified Tissue International, 92, 330–338. PubMed

Bala, Y. , Zebaze, R. & Seeman, E. (2015) Role of cortical bone in bone fragility. Current Opinion in Rheumatology, 27, 406–413. PubMed

Beamer, W. , Donahue, L. , Rosen, C. & Baylink, D. (1996) Genetic variability in adult bone density among inbred strains of mice. Bone, 18, 397–403. PubMed

Becker, M. , Witzel, C. , Kierdorf, U. , Frölich, K. & Kierdorf, H. (2020) Ontogenetic changes of tissue compartmentalization and bone type distribution in the humerus of Soay sheep. Journal of Anatomy, 237, 334–354. PubMed PMC

Bennett, N.C. (2009) African mole‐rats (family Bathyergidae): models for studies in animal physiology. African Zoology, 44, 263–270.

Bennett, N.C. & Faulkes, C.G. (2000) African mole rats: Ecology and eusociality. Cambridge University Press.

Bennett, N.C. , Jarvis, J. , Aguilar, G.H. & Mcdaid, E.J. (1991) Growth and development in six species of African mole‐rats (Rodentia: Bathyergidae). Journal of Zoology, 225, 13–26.

Bennett, N.C. , Jarvis, J.U.M. & Davies, K.C. (1988) Daily and seasonal temperatures in the burrows of African rodent moles. South African Journal of Zoology, 23, 189–195.

Berkovitz, B. & Faulkes, C. (2001) Eruption rates of the mandibular incisors of naked mole‐rats (Heterocephalus glaber). Journal of Zoology, 255, 461–466. 10.1017/S0952836901001546 DOI

Biewener, A.A. & Bertram, J.E.A. (1993) Mechanical loading and bone growth in vivo. In: Hall, B.K. (Ed.) Bone Volumen 7 Bone Growth ‐ B. Boca Raton: CRC Press, pp. 353.

Biknevicius, A. (1993) Biomechanical scaling of limb bones and differential limb use in caviomorph rodents. Journal of Mammalogy, 74, 95–107.

Botha, J. & Chinsamy, A. (2004) Growth and life habits of the Triassic cynodont Trirachodon, inferred from bone histology. Acta Palaeontologica Polonica, 49, 619–627.

Boyles, J.G. , Verburgt, L. , McKechnie, A.E. & Bennett, N.C. (2012) Heterothermy in two mole‐rat species subjected to interacting thermoregulatory challenges. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 317, 73–82. PubMed

Brett, R.A. (1991) The ecology of naked‐mole‐rat colonies: burrowing, food, and limiting factors. In: Sherman, P.W. , Jarvis, J.U.M. and Alexander, R.D. (Eds.) The biology of the naked mole‐rat. Princeton, NJ: Princeton University Press, pp. 137–148.

Bromage, T.G. , Goldman, H.M. , McFarlin, S.C.J. , Warshaw, A.B. & Riggs, C.M. (2003) Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anatomical Record. Part B, New Anatomist, 274, 157–168. PubMed

Bromage, T.G. , Lacruz, R.S. , Hogg, R. , Goldman, H.M. , McFarlin, S.C. , Warshaw, J. et al. (2009) Lamellar bone is an incremental tissue reconciling enamel rhythms, body size, and organismal life history. Calcified Tissue International, 84, 388–404. PubMed

Buffenstein, R. (1996) Ecophysiological responses to a subterranean habitat; a Bathyergid perspective. Mammalia, 60, 591–605.

Buffenstein, R. (2000) Ecophysiological responses of subterranean rodents to underground habitats. In: Lacey, E.A. , Patton, J. and Cameron, G.N. (Eds.) Life underground: The biology of subterranean rodents. Chicago, IL: The University of Chicago Press, p. 449.

Buffenstein, R. (2008) Negligible senescence in the longest living rodent, the naked mole‐rat: Insights from a successfully aging species. Journal of Comparative Physiology B, 178, 439–445. PubMed

Buffenstein, R. , Jarvis, J. , Opperman, L.A. , Cavaleros, M. , Ross, F.P. & Pettifor, J.M. (1994) Subterranean mole‐rats naturally have an impoverished calciol status, yet synthesize calciol metabolites and calbindins. European Journal of Endocrinology, 130, 402–409. PubMed

Buffenstein, R. , Laundy, M. , Pitcher, T. & Pettifor, J.M. (1995) Vitamin D3 intoxication in naked mole‐rats (Heterocephalus glaber) leads to hypercalcemia and increased calcium deposition in teeth with evidence of abnormal skin calcification. General and Comparative Endocrinology, 99, 35–40. PubMed

Buffenstein, R. , Lewis, K.N. , Gibney, P.A. , Narayan, V. , Grimes, K.M. , Smith, M. et al. (2020) Probing pedomorphy and prolonged lifespan in naked mole‐rats and dwarf mice. Physiology, 35(2), 96–111. PubMed

Buffenstein, R. & Pitcher, T. (1996) Calcium homeostasis in mole‐rats by manipulation of teeth and bone calcium reservoirs. In: Dacke, C.G. , Danks, J. , Caple, I. and Flik, G. (Eds.) The comparative endocrinology of calcium regulation. Bristol: Society for Endocrinology, p. 220.

Buffenstein, R. , Sergeev, I.N. & Pettifor, J.M. (1993) Vitamin D hydroxylases and their regulation in a naturally vitamin D‐deficient subterranean mammal, the naked mole rat (Heterocephalus glaber). Journal of Endocrinology, 138(1993), 59–64. PubMed

Buffenstein, R. & Yahav, S. (1991) Is the naked mole‐rat, Heterocephalus glaber, a poikilothermic or poorly thermoregulating endothermic mammal? Journal of Thermal Biology, 16, 227–232.

Cadet, E.R. , Gafni, R.I. , McCarthy, E.F. , McCray, D.R. , Bacher, J.D. , Barnes, K.M. , et al. (2003) Mechanisms responsible for longitudinal growth of the cortex: coalescence of trabecular bone into cortical bone. Journal of Bone and Joint Surgery. American Volume, 85, 1737–1748. PubMed

Calderón, T. , DeMiguel, D. , Arnold, W. , Stalder, G. & Köhler, M. (2019) Calibration of life history traits with epiphyseal closure, dental eruption and bone histology in captive and wild red deer. Journal of Anatomy, 235, 205–216. PubMed PMC

Cambra‐Moo, O. , Nacarino Meneses, C. , Rodríguez Barbero, M.A. , García Gil, O. , Rascón Pérez, J. , Rello Varona, S. et al. (2014) An approach to the histomorphological and histochemical variations of the humerus cortical bone through human ontogeny. Journal of Anatomy, 224(6), 636–646. PubMed PMC

Cambra‐Moo, O. , Nacarino‐Meneses, C. , Díaz‐Güemes, I. , Enciso, S. , García Gil, O. , Llorente Rodríguez, L. et al. (2015) Multidisciplinary characterization of the long‐bone cortex growth patterns through sheep’s ontogeny. Journal of Structural Biology, 191, 1–9. PubMed

Carmeli‐Ligati, S. , Shipova, A. , Dumont, M. , Holtz, S. , Hildebrandt, T. & Shahar, R. (2019) The structure, composition and mechanical properties of the skeleton of the naked mole‐rat (Heterocephalus glaber). Bone, 128, 115035. PubMed

Carrier, R. (1983) Postnatal ontogeny of the musculo‐skeletal system in the Black‐ tailed jack rabbit (Lepus californicus). Journal of Zoology, London, 201, 27–55.

Casinos, A. , Quintana, C. & Viladiu, C. (1993) Allometry and adaptation in the long bones of a digging group of rodents (Ctenomyinae). Zoological Journal of the Linnean Society, 107, 107–115.

Castanet, J. (2006) Time recording in bone microstructures of endothermic animals; functional relationships. Comptes Rendus Palevol, 5, 629–636.

Castanet, J. , Croci, S. , Aujard, F. , Perret, M. , Cubo, J. & de Margerie, E. (2004) Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus . Journal of Zoology of London, 263, 31–39.

Castanet, J. , Francillon‐Vieillot, H. , Meunier, F. & de Ricqlès, A. (1993) Bone and individual aging. In: Hall, B.B. (Ed.) Bone vol. 7 bone growth. Boca Raton, FL: CRC Press, 353 pp.

Cerroni, A.M. , Tomlinson, G.A. , Turnquist, J.E. & Grynpas, M.D. (2000) Bone mineral density, osteopenia, and osteoporosis in the rhesus Macaques of Cayo Santiago. American Journal of Physical Anthropology, 113, 389–410. PubMed

Chinsamy, A. & Hurum, J. (2006) Bone microstructure and growth patterns of early mammals. Acta Palaeontologica Polonica, 51, 325–338.

Chinsamy, A. & Raath, M. (1992) Preparation of fossil bone for histological examination. Palaeontologia Africana, 29, 39–44.

Chinsamy, A. & Warburton, N.M. Ontogenetic growth and the development of a unique fibrocartilage entheses in Macropus fuliginosus . Zoology, 144, (in press). 10.1016/j.zool.2020.125860 PubMed DOI

Chinsamy‐Turan, A. (2005) The microstructure of dinosaur bone. Deciphering biology with fine‐scale techniques. Baltimore, Maryland: The Johns Hopkins University Press.

Chinsamy‐Turan, A. (2012) The microstructure of bones and teeth of nonmammalian therapsids. In: Chinsamy‐Turan, A. (Ed.) Forerunners of mammals: Radiation, histology, biology. Bloomington and Indianapolis: Indiana University Press, pp. 65–88.

Currey, J. & Alexander, R. (1985) The thickness of the walls of tubular bones. Journal of Zoology (A), 206, 453–468.

Currey, M.N. & Dean, R.S. (2017) Revisiting the links between bone remodeling and osteocytes: insights from across phyla. Biological Reviews of the Cambridge Philosophical Society, 92, 1702–1719. PubMed

Dammann, P. & Burda, H. (2007) Senescence patterns in African mole‐rats (Bathyergidae, Rodentia). In: Begall, S. , Burda, H. & Schleich, C. (Eds.) Subterranean rodents: News from underground. Heiderberg, Germany: Springer‐Verlag, pp. 251–263.

de Margerie, E. , Cubo, J. & Castanet, J. (2002) Bone typology and growth rate: testing and quantifying “Amprino’s rule” in the mallard (Anas platyrhynchos). Comptes Rendus Biologies, 325, 221–230. PubMed

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, 869–879. PubMed

de Ricqlès, A. , Meunier, F.J. , Castanet, J. & Francillon‐Vieillot, H. (1991) Comparative microstructure of bone. In: Hall, B.K. (Ed.) Bone matrix and bone specific products. Boca Raton, FL: CRC Press, pp. 1–78.

de Ricqlès, A.J. , Padian, K. , & (2003) On the bone histology of some Triassic pseudosuchian archosaurs and related taxa. Annales de Paléontologie, 89, 67–101.

Dengler‐Crish, C.M. & Catania, K.C. (2007) Phenotypic plasticity in female naked mole‐rats after removal from reproductive suppression. Journal of Experimental Biology, 210, 4351–4358. PubMed

Dengler‐Crish, C. & Catania, K.C. (2009) Cessation of reproduction‐related spine elongation after multiple breeding cycles in female naked mole‐rats. Anatomical Record, 292, 131–137. PubMed PMC

Duque, G. & Watanabe, K. (2011) Osteoporosis research. In: Duque, G. & Watanabe, K. (Eds.) Animal models. London: Springer.

Edrey, Y.H. , Park, T.J. , Kang, H. , Biney, A. & Buffenstein, R. (2011) Endocrine function and neurobiology of the longest‐living rodent, the naked molerat. Experimental Gerontology, 46, 116–123. PubMed

Enlow, D.H. (1962) A study of the post‐natal growth and remodeling of bone. American Journal of Anatomy, 110, 79–101. PubMed

Enlow, D.H. (1963) Principles of bone remodeling. an account of post‐natal growth and remodeling processes in long bones and the mandible. Springfield, IL: Charles C. Thomas.

Enlow, D.H. (1969) The bone of reptiles. In: Gans, C. (Ed.) Biology of the reptilia, vol. 1 morphology A. London: Academic Press, pp. 373.

Enlow, D. & Brown, S. (1958) A comparative histological study of fossil and recent bone tissues. Part III. The Texas Journal of Science, 10, 187–230.

Faulkes, C.G. & Bennett, N.C. (2009) Reproductive skew in African mole‐rats: behavioral and physiological mechanisms to maintain high skew. Ch. 13. In: Hager, R. & Jones, C.B. (Eds.) Reproductive skew in vertebrates: Proximate and ultimate causes. Cambridge, UK: Published by Cambridge University Press, pp. 369–396.

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. PubMed PMC

Foote, J. (1916) A contribution to the comparative histology of the femur. In: Hrdlicka, A. (Ed.) Washington: The Smithsonian Institution.

Francillon‐Vieillot, H. , de Buffrénil, V. & Castanet, J. (1990) Microstructures and mineralization of vertebrate skeletal tissues. In: Carter, J. (Ed.) Skeletal biomineralizations: Patterns, processes and evolutionary trends. New York: Van Nostrand Reinhold, pp. 471–530.

Frost, H.M. & Jee, W.S. (1992) On the rat model of human osteopenias and osteoporoses. Bone and Mineral, 18, 227–236. PubMed

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, 489–498.

Geiger, M. , Wilson, L.A.B. , Costeur, L. , Sánchez, R. & Sánchez‐Villagra, M.R. (2013) Diversity and body size in giant caviomorphs (Rodentia) from the northern Neotropics—a study of femoral variation. Journal of Vertebrate Paleontology, 33, 1449–1456.

Gilbert, J.D. , Rossiter, S.J. & Faulkes, C.G. (2020) The relationship between individual phenotype and the division of labour in naked mole‐rats: It's complicated. PeerJ, 8, e9891. PubMed PMC

Golden, N.H. & Carlson, J.L. (2008) The pathophysiology of amenorrhea in the adolescent. Annals of the New York Academy of Sciences, 1135, 163–178. PubMed

Goldman, B.D. , Goldman, S.L. , Lanz, T. , Magaurin, A. & Maurice, A. (1999) Factors influencing metabolic rate in naked mole‐rats (Heterocephalus glaber). Physiology & Behavior, 66, 447–459. PubMed

Goldman, H.M. , Bromage, T.G. , Thomas, C.D.L. & Clement, J.G. (2003) Preferred collagen fiber orientation in the human mid‐shaft femur. The Anatomical Record. Part A, 272A, 434–445. PubMed

Goldman, H.M. , McFarlin, S.C. , Cooper, D.M.L. , Thomas, C.D.L. & Clement, J.G. (2009) Ontogenetic patterning of cortical bone microstructure and geometry at the human mid‐shaft femur. Anatomical Record, 292, 48–64. PubMed

Hall, B.K. (1978) Developmental and cellular skeletal biology. New York: Academic Press.

Hamar, M. & Prodanascu, A. (1971) Age determination in Spalax microphthalmus (Rodentia, Spalacidae). Annales Zoologici Fennici, 8(1), 60–63.

Hart, L. & O’Riain, M. (2006) Is the Cape dune mole‐rat, Bathyergus suillus (Rodentia: Bathyergidae), a seasonal or aseasonal breeder? Journal of Mammalogy, 87, 1078–1085.

Heck, C.T. , Varricchio, D.J. , Gaudin, T.J. , Woodward, H.N. & Horner, J.R. (2019) Ontogenetic changes in the long bone microstructure in the nine‐banded armadillo (Dasypus novemcinctus). PLoS One, 14(4), e0215655. PubMed PMC

Heinrich, R.E. , Ruff, C.B. & Adamczewski, J.Z. (1999) Ontogenetic changes in mineralization and bone geometry in the femur of muskoxen (Ovibos moschatus). Journal of Zoology, 247, 215–223.

Henry, E.C. , Dengler‐Crish, C.M. & Catania, K.C. (2007) Growing out of a caste–reproduction and the making of the queen mole‐rat. Journal of Experimental Biology, 210, 261–268. PubMed

Hislop, M.S. & Buffenstein, R. (1994) Noradrenaline induces nonshivering thermogenesis in both the naked mole‐rat (Heterocephalus glaber) and the Damara mole‐rat (Cryptomys damarensis) despite very different modes of thermoregulation. Journal of Thermal Biology, 19, 25–32.

Holtze, S. , Braude, S. , Lemma, A. , Koch, R. , Morhart, M. , Szafranski, K. et al. (2018) The microenvironment of naked mole‐rat burrows in East Africa. African Journal of Ecology, 56, 279–289.

Hood, W.R. , Kessler, D.S. & Oftedal, O.T. (2014) Milk composition and lactation strategy of a eusocial mammal, the naked mole‐rat. Journal of Zoology, 293(2), 108–118.

Hulbert, A.J. (1980) The evolution of energy metabolism in mammals. In: Schmidt‐Nielsen, K. , Bolis, L. & Taylor, C. R. (Eds.) Comparative physiology: Primitive mammals. Cambridge, UK: Cambridge University Press, pp. 129–139.

Hurum, J.H. & Chinsamy‐Turan, A. (2012) The radiation, bone histology, and biology of early mammals. In: Chinsamy‐Turan, A. (Ed.) Forerunners of mammals: radiation, histology, biology. Bloomington: Indiana University Press, pp. 249–270.

Jarvis, J.U.M. (1981) Eusociality in a mammal: Cooperative breeding in naked mole‐rat colonies. Science, 212, 571–573. PubMed

Jarvis, J.U.M. (1991) Reproduction of naked mole‐rats. In: Sherman, P.W. , Jarvis, J.U.M. and Alexander, R.D. (Eds.) The biology of the naked mole‐rat. Princeton, NJ: Princeton University Press, pp. 384–425.

Jarvis, J.U.M. , O’Riain, M.J. & McDaid, E. (1991) Growth and factors affecting body size in naked mole‐rats. In: Sherman, P.W. , Jarvis, J.U.M. and Alexander, R.D. (Eds.) The biology of the naked mole‐rat. Princeton, NJ: Princeton Univ. Press, pp. 258–383.

Jarvis, J. & Sale, J. (1971) Burrowing and burrow patterns of East African mole‐rats Tachyoryctes, Heliophobius and Heterocephalus . Journal of Zoology, 163, 451–479.

Jarvis, J.U.M. & Sherman, P.W. (2002) Heterocephalus glaber. Mammalian Species, No., 706, 1–9.

Jordana, X. , Marín‐Moratalla, N. , Moncunill‐Solèa, B. , Nacarino‐Menesesa, C. & Köhler, M. (2016) Ontogenetic changes in the histological features of zonal bone tissue of ruminants: a quantitative approach C. Rendus Palevol, 15(2016), 255–266.

Klevezal, G.A. (1996) Recording structures of mammals. Determination of age and reconstruction of life history. Rotterdam: A.A Balkema.

Klevezal, G.A. & Kleinberg, S.E. (1967) Age determination of mammals from annual layers in teeth and bones. Jerusalem, Israel: Translated from Russian by the Israel Program for Scientific Translations.

Klevezal, G.A. & Mina, M.V. (1973) Factors determining the patterns of annual layers in the dental tissue and bones of mammals. Zhurnal Obshchei Biologii, 34(4), 594–605. PubMed

Köhler, M. , Marín‐Moratalla, N. , Jordana, X. & Aanes, R. (2012) Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature, 487, 358–361. PubMed

Köhler, M. & Moyà‐Solà, S. (2009) Physiological and life history strategies of a fossil large mammal in a resource‐limited environment. Proceedings of the National Academy of Sciences of the United States of America, 106, 20354–20358. PubMed PMC

Kolb, C. , Scheyer, T.M. , Veitschegger, K. , Forasiepi, A.M. , Amson, E. , Van der Geer, A.A.E. et al. (2015) Mammalian bone palaeohistology: A survey and new data with emphasis on island forms. PeerJ, 3, e1358. PubMed PMC

Kronenberg, H. (2003) Developmental regulation of the growth plate. Nature, 423, 332–336. PubMed

Lacey, E.A. & Sherman, P.W. (1991) Social organization of naked mole‐rat colonies: evidence for divisions of labor. In: Sherman, P.W. , Jarvis, J.U.M. & Alexander, R.D. (Eds.) The biology of the naked mole‐rat. Princeton, NJ: Princeton University Press, pp. 275–336.

Lammers, A.R. & German, R.Z. (2002) Ontogenetic allometry in the locomotor skeleton of specialized half‐bounding mammals. Journal of Zoology, London, 258, 485–495.

Leahy, G.D. (1991) Lamellar‐zonal bone in fossil mammals: implications for dinosaur and therapsid paleophysiology. The Journal of Vertebrate Paleontology, 11(3), 42A.

Lee, A. & Simons, E. (2015) Wing bone laminarity is not an adaptation for torsional resistance in bats. PeerJ, 3, e823. PubMed PMC

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. PubMed PMC

Locke, M. (2004) Structure of long bones in mammals. Journal of Morphology, 262, 546–565. PubMed

Lovegrove, B.G. , Heldmaier, G. & Ruf, T. (1993) Circadian activity rhythms in colonies of ‘blind’ Molerats, Cryptomysdamarensis (Bathyergidae). South African Journal of Zoology, 28(1), 46–55.

Lövy, M. , Šklíba, J. & Šumbera, R. (2013) Spatial and temporal activity patterns of the free‐living giant mole‐rat (Fukomys mechowii), the largest social bathyergid. PLoS One, 8(1), e55357. PubMed PMC

Maloney, S.K. , Fulley, A. , Meyer, L.C.R. , Kamerman, P.R. , Mitchell, G. & Mitchell, D. (2011) Minimum core body temperatures in western grey kangaroos decreases as summer advances: a seasonal pattern or a direct response to water, heat or energy supply? Journal of Experimental Biology, 214, 1813–1820. PubMed

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, 422–429.

McFarlin, S. (2006) Ontogenetic variation in long bone microstructure in catarrhines and its significance for life history research. Anthropology. New York: The City University of New York.

Mcfarlin, S.C. , Terranova, C.J. , Zihlman, A.L. & Bromage, T.G. (2016) Primary bone microanatomy records developmental aspects of life history in catarrhine primates. Journal of Human Evolution, 92, 60–79. PubMed

McNab, B.K. (1966) The metabolism of fossorial rodents: a study of convergence. Ecology, 47, 712–733.

Montoya‐Sanhueza, G. (2014) Bone microstructure of the subterranean rodent Bathyergus suillus (Rodentia: Bathyergidae). Master’s Thesis. Department of Zoology, University of Cape Town South Africa.

Montoya‐Sanhueza, G. (2020) Functional anatomy, osteogenesis and bone microstructure of the appendicular system of African mole‐rats (Rodentia: Ctenohystrica: Bathyergidae). PhD Thesis. Submitted to the Department of Biological Sciences, University of Cape Town, South Africa. 268 pp.

Montoya‐Sanhueza, G. & Chinsamy, A. (2016) Bone microstructure of two highly specialised subterranean rodents: Bathyergus suillus and Heterocephalus glaber (Bathyergidae). Biennial Conference Palaeontological Society of Southern Africa (PSSA). Abstract book. Stellenbosch, South Africa, 45.

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, 203–233. PubMed PMC

Montoya‐Sanhueza, G. & Chinsamy, A. (2018) Cortical bone adaptation and mineral mobilization in the subterranean mammal Bathyergus suillus (Rodentia: Bathyergidae): Effects of age and sex. PeerJ, 6, e4944. PubMed PMC

Montoya‐Sanhueza, G. , Wilson, L.A.B. & Chinsamy, A. (2019) Postnatal development of the largest subterranean mammal (Bathyergus suillus): Morphology, osteogenesis, and modularity of the appendicular skeleton. Developmental Dynamics. PubMed

Mora, S. & Gilsanz, V. (2010) Pubertal growth of the male skeleton (Ch 8). In: Orwoll, E. , Bilezikian, J. & Vanderschueren, D. (Eds.) Osteoporosis in men. London: Academic Press, pp. 95–103.

Moshkin, M.P. , Novikov, E.A. & Petrovski, D.V. (2001) Seasonal changes of thermoregulation in the mole vole Ellobius talpinus . Physiological and Biochemical Zoology, 74(6), 869–875. PubMed

Nacarino‐Meneses, C. , Jordana, X. & Kohler, M. (2016) First approach to bone histology and skeletochronology of Equus hemionus . Comptes Rendus Palevol, 15, 1–7.

O’Connor, T.P. , Lee, A. , Jarvis, J. & Buffenstein, R. (2002) Prolonged longevity in naked mole‐rats: age‐related changes in metabolism, body composition and gastrointestinal function. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 133(3), 835–842. PubMed

O’Riain, M.J. (1996) Pup ontogeny and factors influencing behavioural and morphological variation in naked mole‐rats, Heterocephalus glaber (Rodentia, Bathyergidae). University of Cape Town.

O’Riain, M.J. & Jarvis, J.U.M. (1998) The dynamics of growth in naked mole‐rats: the effects of litter order and changes in social structure. Journal of Zoology, 246(49–60), 1998.

O’Riain, M.J. , Jarvis, J. , Alexander, R. , Buffenstein, R. & Peeters, C. (2000) Morphological castes in a vertebrate. Proceedings of the National Academy of Sciences of the United States of America, 97, 13194–13197. PubMed PMC

Oftedal, O. (1980) Milk and mammalian evolution. In: Schmidt‐Nielsen, K. , Bolis, L. & Taylor, C. R. (Eds.) Comparative physiology: Primitive mammals. Cambridge, UK: Cambridge University Press, pp. 31–42.

Okrouhlík, J. , Šumbera, R. , Gartner, B. , Schoemann, K. , Lövy, M. & Bennett, N.C. (in press). Are southern African solitary mole‐rats homeothermic or heterothermic under natural field conditions? Journal of Thermal Biology. PubMed

Orlandi‐Oliveras, G. , Jordana, X. , Moncunill‐Sole, B. & Köhler, M. (2016) Bone histology of the giant fossil dormouse Hypnomys onicensis (Gliridae, Rodentia) from Balearic Islands. Comptes Rendus Palevol, 15, 238–244.

Park, T.J. , Reznick, J. , Peterson, B.L. , Blass, G. , Omerbašić, D. , Bennett, N.C. et al. (2017) Fructose‐driven glycolysis supports anoxia resistance in the naked mole‐rat. Science, 356, 307–311. PubMed

Pazzaglia, U.E. , Sibilia, V. , Congiu, T. , Pagani, F. , Ravanelli, M. & Zarattini, G. (2015) Setup of a bone aging experimental model in the rabbit comparing changes in cortical and trabecular bone: Morphological and morphometric study in the femur. Journal of Morphology, 276, 733–747. PubMed

Pinto, M. , Jepsen, K.J. , Terranova, C.J. & Buffenstein, R. (2010) Lack of sexual dimorphism in femora of the eusocial and hypogonadic naked mole‐rat: A novel animal model for the study of delayed puberty on the skeletal system. Bone, 46, 112–120. PubMed PMC

Pitcher, T. , Buffenstein, R. , Keegan, J.D. , Moodley, G.P. & Yahav, S. (1992) Dietary calcium content, calcium balance and mode of uptake in a subterranean mammal, the damara mole‐rat. Journal of Nutrition, 122, 108–114. PubMed

Pitcher, T. , Pettifor, J.M. & Buffenstein, R. (1994) The effect of dietary calcium content and oral vitamin D3 supplementation on mineral homeostasis in a subterranean mole‐rat Cryptomys damarensis . Bone Miner, 27, 145–157. PubMed

Prendergast, B.J. , Renstrom, R.A. & Nelson, R.J. (2004) Genetic analyses of a seasonal interval timer. Journal of Biological Rhythms, 19(4), 298–311. PubMed

Puzachenko, AYu (1991) Age determination of Spalax microphthalmus (Rodentia, Spalacidae). Zoologicheskii Zhurnal, 70(12), 113–124.

Ratajczak, H.V. , Thomas, P.T. , Sothern, R.B. , Vollmuth, T. & Heck, J.D. (1993) Evidence for genetic basis of seasonal differences in antibody formation between two mouse strains. Chronobiology International, 10(5), 383–394. PubMed

Ray, S. & Chinsamy, A. (2004) Diictodon feliceps (Therapsida, Dicynodontia): bone histology, growth, and biomechanics. Journal of Vertebrate Paleontology, 24, 180–194. 10.1671/1914-14 DOI

Reid, R.E.H. (1996) Bone histology of the Cleveland‐Lloyd dinosaurs and of dinosaurs 541 in general, Part I, Introduction: Introduction to bone tissues. Brigham Young 542 University Geology Studies, 41, 25–72.

Riccio, A.P. & Goldman, B.D. (2000) Circadian rhythms of body temperature and metabolic rate in naked mole‐rats. Physiology & Behavior, 71, 15–22. PubMed

Ruby, J.G. , Smith, M. & Buffenstein, R. (2018) Naked mole‐rat mortality rates defy Gompertzian laws by not increasing with age. eLife, 7, e31157. PubMed PMC

Ruth, E.B. (1953) Bone studies. II. An experimental study of the haversian‐type vascular channels. The American Journal of Anatomy, 93, 429–455. PubMed

Samuels, J.X. & Van, V.B. (2008) Skeletal indicators of locomotor adaptations in living and extinct rodents. Journal of Morphology, 269, 1387–1411. PubMed

Sanger, T.J. , Norgard, E.A. , Pletscher, L.S. , Bevilacqua, M. , Brooks, V.R. , Sandell, L.J. et al. (2011) Developmental and genetic origins of murine long bone length variation. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 316, 146–161. PubMed PMC

Seeman, E. (2001) Clinical review 137: Sexual dimorphism in skeletal size, density, and strength. Journal of Clinical Endocrinology and Metabolism, 86(10), 4576–4584. PubMed

Seeman, E. (2002) Pathogenesis of bone fragility in women and men. Lancet, 359, 1841–1850. PubMed

Seney, M.L. , Kelly, D.A. , Goldman, B.D. , Šumbera, R. & Forger, N.G. (2009) Social structure predicts genital morphology in African mole‐rats. PLoS ONE, 4, e7477. 10.1371/journal.pone.0007477 PubMed DOI PMC

Sherman, P.W. & Jarvis, J.U.M. (2002) Extraordinary life spans of naked mole‐rats (Heterocephalus glaber). Journal of Zoology, 258, 307–311.

Silva, M.J. & Jepsen, K.J. (2013) Age related changes in whole‐bone structure and strength. In: Silva, M.J. (Ed.). Skeletal aging and osteoporosis. Biomechanics and mechanobiology. London: Springer, Berlin Heidelberg, pp. 1–30.

Singh, I.J. , Tonna, E.A. & Gandel, C.P. (1974) A comparative histological study of mammalian bone. Journal of Morphology, 144, 421–437. PubMed

Skinner, D.C. , Moodley, G. & Buffenstein, R. (1991) Is vitamin D3 essential for mineral metabolism in the Damara mole‐rat (Cryptomys damarensis)? General and Comparative Endocrinology, 81, 500–505. PubMed

Skulachev, V.P. , Holtze, S. , Vyssokikh, M.Y. , Bakeeva, L.E. , Skulachev, M.V. , Markov, A.V. et al. (2017) Neoteny, prolongation of youth: From naked mole rats to “naked apes” (humans). Physiological Reviews, 97, 699–720. PubMed

Smith, C.C.D. (2020) Giraffa camelopardalis: Limb bone histology through ontogeny. Masters dissertation, University of Cape Town.

Smith, J.W. (1960) Collagen fibre patterns in mammalian bone. Journal of Anatomy, 94, 329–344. PubMed PMC

Starck, J.M. & Chinsamy, A. (2002) Bone microstructure and developmental plasticity in birds and other dinosaurs. Journal of Morphology, 254, 232–246. PubMed

Straehl, F.R. , Scheyer, T.M. , Forasiepi, A.M. , MacPhee, R.D. & Sánchez‐Villagra, M.R. (2013) Evolutionary patterns of bone histology and bone compactness in xenarthran mammal long bones. PLoS One, 8, e69275. PubMed PMC

Streicher, S. , Boyles, J.G. , Oosthuizen, M.K. & Bennett, N.C. (2011) Body temperature patterns and rhythmicity in free‐ranging subterranean damaraland mole‐rats, Fukomys damarensis . PLoS One, 6(10), e26346. PubMed PMC

Šumbera, R. , Chitaukali, W.N. , Elichová, M. , Kubová, J. & Burda, H. (2004) Microclimatic stability in burrows of an Afrotropical solitary bathyergid rodent, the silvery mole‐rat (Heliophobius argenteocinereus). Journal of Zoology, 263, 409–416.

Šumbera, R. (2019) Thermal biology of a strictly subterranean mammalian family, the African mole‐rats (Bathyergidae, Rodentia) – A review. Journal of Thermal Biology, 79, 166–189. PubMed

Tian, J. , Azpurua, C. , Hine, A. , Vaidya, M. , Myakishev‐Rempel, J. , Ablaeva, Z. et al. (2013) High‐molecular‐mass hyaluronan mediates the Cancer resistance of the naked mole rat. Nature, 499, 346–349. PubMed PMC

Tucker, R. (1981) The digging behavior and skin differentiations in Heterocephalus glaber . Journal of Morphology, 168, 51–71. PubMed

Urison, N.T. & Buffenstein, R. (1994) Shifts in thermoregulatory patterns with pregnancy in the poikilothermic mammal ‐ the naked mole‐rat (Heterocephalus glaber). Journal of Thermal Biology, 19, 365–371.

Urison, N. & Buffenstein, R. (1995) Metabolic and body temperature changes during pregnancy and lactation in the naked mole‐rat (Heterocephalus glaber). Physiological Zoology, 68, 402–420.

Walker, M.M. , Louys, J. , Herries, A.I.R. , Gilbert, J.P. & Miszkiewicz, J.J. (2020) Humerus midshaft histology in a modern and fossil wombat. Australian Mammalogy, 10.1071/AM20005 DOI

Wall, W.P. (1983) The correlation between high limb‐bone density and aquatic habits in recent mammals. Journal of Paleontology, 57, 197–207.

Warshaw, J. (2008) Comparative primate bone microstructure: records of life history, function, and phylogeny. In: Sargis, E. & Dagosto, M. (Eds.) Mammalian evolutionary morphology. A tribute to Frederick S. Szalay. Vertebrate paleobiology and paleoanthropology series. Dordretch, The Netherlands: Springer, pp. 440.

Webber, T. , Patel, S.P. , Pensak, M. , Fajolu, O. , Rozental, T.D. & Wolf, J.M. (2015) Correlation between distal radial cortical thickness and bone mineral density. Journal of Hand Surgery, 40(3), 493–499. PubMed

Werning, S.A. (2013a) Evolution of bone histological characters in amniotes, and the implications for the evolution of growth and metabolism. PhD dissertation. University of California, Berkeley.

Werning, S.A. (2013b) Osteohistological differences between marsupials and placental mammals reflect both growth rates and life history strategies. Abstract. Society for Integrative and Comparative Biology.

Wongdee, K. , Krishnamra, N. & Charoenphandhu, N. (2012) Endochondral bone growth, bone calcium accretion, and bone mineral density: How are they related? The Journal of Physiological Sciences, 62, 299–307. PubMed PMC

Woodley, R. & Buffenstein, R. (2002) Thermogenic changes with chronic cold exposure in the naked mole‐rat (Heterocephalus glaber). Comparative Biochemistry and Physiology Part A, 133, 827–834. PubMed

Yingling, V.R. & Taylor, G. (2008) Delayed pubertal development by hypothalamic suppression causes an increase in periosteal modeling but a reduction in bone strength in growing female rats. Bone, 42, 1137–1143. PubMed PMC

Young, J.W. , Fernandez, D. & Fleagle, J.G. (2010) Ontogeny of long bone geometry in capuchin monkeys (Cebus albifrons and Cebus apella): implications for locomotor development and life history. Biology Letters, 6, 197–200. PubMed PMC

Zelová, J. , Šumbera, R. , Okrouhlík, J. , Šklíba, J. , Lövy, M. & Burda, H. (2011) A seasonal difference of daily energy expenditure in a free‐living subterranean rodent, the silvery mole‐rat (Heliophobius argenteocinereus; Bathyergidae). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 158, 17–21. PubMed

Zelová, J. , Šumbera, R. , Sedláček, F. & Burda, H. (2007) Energetics in a solitary subterranean rodent, the silvery mole‐rat, Heliophobius argenteocinereus and allometry of RMR in African mole‐rats (Bathyergidae). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 147, 412–419. PubMed

Paleohistology of Caraguatypotherium munozi (Mammalia, Notoungulata, Mesotheriidae) from the early late Miocene of northern Chile: A preliminary ontogenetic approach

Fossorial adaptations in African mole-rats (Bathyergidae) and the unique appendicular phenotype of naked mole-rats

Bone remodeling in the longest living rodent, the naked mole-rat: Interelement variation and the effects of reproduction