Mammalian Biology

, Volume 78, Issue 6, pp 422–429 | Cite as

Bone histology as an approach to providing data on certain key life history traits in mammals: Implications for conservation biology

  • Nekane Marín-MoratallaEmail author
  • Xavier Jordana
  • Meike Köhler
Original Investigation


The knowledge of the life histories of wild mammals is of crucial importance in the field of conservation management. The endangered status of many species calls for faster data collection that can be used in risk assessment and, ultimately, for designing conservation policies. This study is pioneering the potential of bone histology to provide data on life history traits crucial for conservation biology in long-lived mammals. Long bone cross-sections show pronounced annual cycles of growth arrest allowing application of skeletochronology (counts of lines of arrested growth ‘LAGs’). Consequently, the number of LAGs within the primary fast-growing bone tissue up to the outer cortical slow-growing bone tissue corresponds to the age at first reproduction; whereas the age at death can be estimated by the total number of rest lines throughout the whole of bone cross-section. Furthermore, the diameters of successive growth rings as well as the osteocyte lacuna density may shed light on growth rates. We use the endangered desert dwelling antelope Addax nasomaculatus as a case study. By analyzing different ontogenetic stages in five Addax individuals (three captive and two wild specimens) from a museum collection, we show that bone histology may be a reliable tool for determining certain key life history traits. In our sample, the wild Addax female attained reproductive maturity at three years, whereas the male specimens, both the captive and the wild ones, reached maturity at four years. This is congruent with data from other large antelopes with male-biased size dimorphism, but differs slightly from data on sexual maturity previously published for wild Addax. Moreover, quantification of osteocyte lacunae in both adult males provides a higher cell density in the captive one than in the wild one suggesting the strong effect of constant resources supply in individuals from zoos on growth rates. While age at first reproduction and longevity are essentials parameters to carry out demographic models, growth rates may allow evaluation of the health status of wild populations. This approach may provide useful data on life history traits when applied to bones collected in the wild.


Lines of arrested growth Life history Longevity Age at first reproduction Demography 


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  1. Alden, P.C, Estes, R.D., Schlitter, D., McBride, B., 1995. National Audubon Society Field Guide to African Wildlife. Chanticleer Press, New York.Google Scholar
  2. Asa, C.S., 2010. Reproductive physiology. In: Kleiman, D.G., Thompson, K.V., Kirk-Baer, C. (Eds.), Wild Mammals in Captivity. The University of Chicago Press, London, pp. 219–252.Google Scholar
  3. Azorit, C, Analla, M., Hervas, J., Carrasco, R., Muñoz-Cobo, J., 2002a. Growth marks observation: preferential techniques and teeth for aging of Spanish Red Deer (Cervus elaphus hispanicus). Anat. Histol. Embryol. 31, 303–307.CrossRefGoogle Scholar
  4. Azorit, C, Muñoz-Cobo, J., Analla, M., 2002b. Seasonal deposition of cementum in first lower molars from Cervus elaphus hispanicus. Mamm. Biol. 67, 243–245.Google Scholar
  5. Azorit, C, Muñoz-Cobo, J., Hervas, J., Analla, M., 2004. Aging through growth marks in teeth of Spanish red deer. Wildl. Soc. Bull. 32, 702–710.CrossRefGoogle Scholar
  6. Ballou, D., Lees, C, Faust, L.J., Long, S., Lynch, C, Lackey, L.B., Foose, T.J., 2010. Demographic and genetic management of captive populations. In: Kleiman, D.G., Thompson, K.V., Kirk-Baer, C. (Eds.), Wild Mammals in Captivity. The University of Chicago Press, London, pp. 219–252.Google Scholar
  7. Bon, R., Campan, R., 1996. Unexplained sexual segregation in polygamous ungulates: a defense o fan ontogenetic approach. Behav. Process. 38, 131–154.CrossRefGoogle Scholar
  8. Bromage, T.G., Lacruz, R.S., Hogg, R., Goldman, H.M., McFarlin, S.C., Warshaw, J., Dirks, W., Perez-Ochoa, A., Smolyar, I., Enlow, D.H., Boyde, A., 2009. Lamellar bone is an incremental tissue reconciling enamel rhythms, body size, and organismal life history. Calcif. Tissue Int. 84, 404–688.CrossRefGoogle Scholar
  9. Capurro, A.F., Gatto, M., Tosi, G., 1997. Delayed and inverse density dependence in a chamois population of the Italian Alps. Ecography 20, 37–47.CrossRefGoogle Scholar
  10. Castanet, J., 2006. Time recording in bone microstructures of endothermic animals; functional relationships. C. R. Palevol. 5, 629–636.CrossRefGoogle Scholar
  11. Castanet, J., Francillon-Vieillot, H., Meunier, F.J., de Ricqlès, A., 1993. Bone and individual aging. In: Hall, B.K. (Ed.), Bone, vol. 7. CRC Press, London, pp. 245–283.Google Scholar
  12. 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. J. Zool. 263, 31–39.CrossRefGoogle Scholar
  13. Caughley, G., Sinclair, A.R.E., 1994. Wildlife Ecology and Management. Blackwell Science, Cambridge, MA, USA.Google Scholar
  14. Chinsamy, A., Hillenius, W.J., 2004. Physiology of non-aviandinosaurs. In: Weisham-pel, D.B., Dodson, P., Osmolska, I. (Eds.), The Dinosaurs. University of California Press, Berkeley, pp. 643–659.CrossRefGoogle Scholar
  15. Chinsamy, A., Valenzuela, N., 2008. Skeletochronology of the endangered side-neck turtle, Podocnemis expansa. S. Afr.J. Sci. 104, 311–314.Google Scholar
  16. Chinsamy-Turan, A., 2005. The Microstructure of Dinosaur Bone. The Johns Hopkins University Press, Baltimore and London.Google Scholar
  17. Clutton-Brock, T.H., Guiness, F.E., Albon, S.D., 1982. Reed Deer. Behaviour and Ecology of Two Sexes. The University of Chicago Press, Chicago.Google Scholar
  18. CMS ‘Convention on Migratory Species’, 2006. Technical Series Publication Num. 11: Sahelo-Saharan Antelopes, Status and Perspectives. Royal Belgian Institute of Natural Sciences, Bonn, Germany.Google Scholar
  19. Cowlishaw, G., Dunbar, R., 2000. Primate Conservation Biology. The University Chicago Press, Chicago.Google Scholar
  20. Cubo, J., Le Roy, N., Martinez-Maza, C, Montes, L., 2012. Paleohistological estimation of bone growth rate in extinct archosaurs. Paleobiology 38, 335–349.CrossRefGoogle Scholar
  21. Currey, J.D., 1984. The Mechanical Adaptations of Bones. Princeton University Press, Princeton, NJ.CrossRefGoogle Scholar
  22. Currey, J.D., 2003. The many adaptations of bone. J. Biomech. 36, 1487–1495.PubMedCrossRefPubMedCentralGoogle Scholar
  23. de Blainville, H., 1816. Sur plusieurs espèces d’animaux mammifères, de l’ordre des ruminans. Bulletin des Sciences de la Société Philomatique, Paris, pp. 73–82.Google Scholar
  24. de Margerie, E., Cubo, J., Castanet, J., 2002. Bone typology and growth rate: testing and quantifying ‘Amprino’s rule’ in the mallard (Anas platyrhynchus). C. R. Biol. 325, 221–230.Google Scholar
  25. de Ricqlès, A., Meunier, F.J., Castanet, J., Francillon-Vieillot, H., 1991. Bone matrix and bone specific products. In: Hall, B.K. (Ed.), Bone, vol. 3. CRC Press, Boca Raton, London, pp. 255–334.Google Scholar
  26. Dennis, B., Munholland, P.L., Scott, J.M., 1991. Estimation of growth and extinction parameters for endangered species. Ecol. Monogr. 61, 115–144.CrossRefGoogle Scholar
  27. Dittrich, L., 1972. Gestation periods and age of sexual maturity of some African antelopes. IZY 12, 184–187.Google Scholar
  28. Durant, S.M., Harwood, J., 1992. Assessment of monitoring and Management strategies for local populations of the Mediterranean monk seal Monachus monachus. Biol. Conserv. 61, 81–92.CrossRefGoogle Scholar
  29. Erickson, G.M., 2005. Assessing dinosaur growth patterns: a microscopic revolution. TREE 20, 677–684.PubMedPubMedCentralGoogle Scholar
  30. Estes, R.D., 1991. The Behaviour Guide to African mammals. The University of California Press, Berkeley and Los Angeles.Google Scholar
  31. Festa-Bianchet, M., Urquhart, M., Smith, K.G., 1994. Mountain goat recruitment: kid production and survival to breeding age. Can. J. Zool. 72, 22–27.CrossRefGoogle Scholar
  32. Francillot-Vieillot, H., Buffrénil, V.D., Castanet, J., Géraudie, J., Meunier, F.J., Sire, J.Y., Zylberberg, G., de Ricqlès, A., 1990. Microstructure and mineralization of vertebrate skeletal tissues. In: Carter, J.G. (Ed.), Skeletal Biomineralization: Patters, Processes and Evolutionary Trends. Van Nostrand Reinhold, New York, pp. 471–530.Google Scholar
  33. Gaillard, J.M., Festa-Bianchet, M., Yoccoz, N.G., 1998. Population dynamics of large herbivores: variable recruitment with constant adult survival. TREE 13, 58–63.PubMedPubMedCentralGoogle Scholar
  34. Gaillard, J.M., Loison, A., Toïgo, C, 2003. Variation in Life History Traits and realistic population models for Wildlife management: the case of ungulates. In: Festa-Bianched, M., Apollonio, M. (Eds.), Animal Behavior and Wildlife Conservation. Island Press, Washington, pp. 115–132.Google Scholar
  35. 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. C. R. Palevol. 10, 489–498.CrossRefGoogle Scholar
  36. Hillson, S., 2005. Teeth, Cambridge Manuals in Archaeology, 2nd ed. Cambridge University Press, Cambridge.Google Scholar
  37. Horner, J.R., Padian, K., 2004. Age and growth dynamics of Tyrannosaurus rex. Proc. R. Soc. B 271, 1875–1880.CrossRefGoogle Scholar
  38. Horner, J.R., de Ricqlès, A., Padian, K., 1999. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25, 295–304.CrossRefGoogle Scholar
  39. Huda, T.F.J., Bowman, J.E., 1995. Age determination from dental microstructure in juveniles. Am. J. Phys. Anthropol. 95, 135–150.CrossRefGoogle Scholar
  40. Huttenlocker, A., Woodward, H., Hall, B.K., 2013. The biology of bone. In: Padian, K., Lamm, E.-T. (Eds.), Bone histology of fossil tetrapods. University of California Press, Berkeley, Los Angeles, London, pp. 13–34.Google Scholar
  41. Isaac, J.L., 2009. Effects of climate change on life history: implications for extinction risk in mammals. Endang. Species. Res. 7, 115–123.CrossRefGoogle Scholar
  42. Jakob, C, Seitz, A., Crivelli, A.J., Miaud, C, 2002. Growth cycle of the marbled newt (Triturus marmoratus) in the Mediterranean region assessed by skeletochronology. Amphibia-Reptilia 23, 407–418.CrossRefGoogle Scholar
  43. Jarman, P., 1983. Mating system and sexual dimorphism in large, terrestrial, mammalian herbivores. Biol. Rev. 58, 485–520.CrossRefGoogle Scholar
  44. Kingdon, J., 1997. The Kingdon Field Guide to African Mammals. Academic Press, CA, USA.Google Scholar
  45. Klevezal, G.A., 1996. Recording Structures of Mammals: Determination of Age and Reconstruction of Life History. AA Balkema, Rotterdam.Google Scholar
  46. Köhler, M., 2010. Fast or slow? The evolution of life history traits associated with insular dwarfing. In: Pérez-Mellado, V., Ramón, M.M. (Eds.), Islands and Evolution. Institut Menorquíd’Estudis: Recerca 19, Menorca, pp. 261–279.Google Scholar
  47. Köhler, M., Moyà-Solà, S., 2009. Physiological and life history strategies of a fossil large mammal in a resource-limited environment. PNAS 106, 20354–20358.PubMedCrossRefGoogle Scholar
  48. Köhler, M., Moyà-Solà, S., Esteban-Trivigno, S., 2008. Morphological variables and associated individual body weight for bovids. New equations for body mass predictions. Mitt. Hamb. Zool. Mus. Inst 105, 103–136.Google Scholar
  49. 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.PubMedCrossRefGoogle Scholar
  50. Krausman, P., Casey, A., 2007. Addax nasomaculatus. Mamm. Species 807, 1–4.CrossRefGoogle Scholar
  51. Lieberman, D.E., 1993. Life history variables preserved in dental cementum microstructure. Science 261, 1162–1164.PubMedCrossRefPubMedCentralGoogle Scholar
  52. Lubinski, P.M., 2001. Observations on seasonality and mortality from recent catastrophic death assemblage. J. Arch. Sci. 28, 833–842.CrossRefGoogle Scholar
  53. Mallon, D.P., Kingswood, S.C., 2001. Antelopes. Global Survey and Regional Action Plans, Part 4: North Africa, the Middle East, and Asia. IUCN, Gland, Switzerland.Google Scholar
  54. Marín-Moratalla, N., Jordana, X., García-Martínez, R., Köhler, M., 2011. Tracing the evolution of fitness components in fossil bovids under different selective regimes. C. R. Palevol. 10, 469–478.CrossRefGoogle Scholar
  55. Martin, R.B., Burr, D.B., Sharkey, N.A., 1998. Skeletal Tissue Mechanics. Springer-Verlag, New York.CrossRefGoogle Scholar
  56. McKinney, M.L., 1997. Extinction vulnerability and selectivity: combining ecological and paleontological views. Annu. Rev. Ecol. Syst. 28, 495–516.CrossRefGoogle Scholar
  57. Mduma, S.A.R., Sinclair, A.R.E., Hilborn, R., 1999. Food regulates the Serengeti wildebeest: a 40-year record. J. Anim. Ecol. 68, 1101–1122.CrossRefGoogle Scholar
  58. Mésochina, P., Chardonnet, P., Mallon, D., 2009. One Fourth of Antelope Species are Threatened with Extinction in the World. IUCN, Gland, Switzerland.Google Scholar
  59. Nowak, R.M., 1999. Walker’s Mammals of the World, 6th ed. The Johns Hopkins University Press, Baltimore and London.Google Scholar
  60. Ostrowski, S., Williams, J.B., Mésochina, P., Sauerwein, H., 2006. Physiological acclimation of a desert antelope, Arabian oryx (Oryx leucoryx), to long-term food and water restriction. J. Comp. Physiol. B 176, 191–201.CrossRefGoogle Scholar
  61. Owens, P.F., Bennett, P.M., 2000. Ecological basis on extinction risk in birds: habitat loss versus human persecution and introduced predators. PNAS 97, 12144–12148.PubMedCrossRefPubMedCentralGoogle Scholar
  62. Owen-Smith, N., 1993. Mortality rates of male and female Kudus: the costs of sexual size dimorphism. J. Anim. Ecol. 63, 428–440.CrossRefGoogle Scholar
  63. Padian, K., 2013. Why study the bone microstructure of fossil tetrapods? In: Padian, K., Lamm, E.-T. (Eds.), Bone Histology of Fossil Tetrapods. University of California Press, Berkeley, Los Angeles, London, pp. 1–12.CrossRefGoogle Scholar
  64. Padian, K., Lamm, E.T., 2013. Bone Histology of Fossil Tetrapods. University of California Press, Berkeley, Los Angeles, London.CrossRefGoogle Scholar
  65. Pettorelli, N., Gaillard, J.M., Van Laere, G., Duncan, P., Kjellander, P., Liberg, O., Delorme, D., Maillard, D., 2002. Variations in adult body mass in roe deer: the effects of population density at birth and of habitat quality. Proc. Roy. Soc. B 269, 747–753.CrossRefGoogle Scholar
  66. Piccione, G., Giannetto, C, Casella, S., Caola, G., 2009. Annual rhythms of some physiological parameters in Ovies aries and Capra hircus. Biol. Rhythm Res. 40, 455–464.CrossRefGoogle Scholar
  67. Purvis, A., Gittleman, J.L., Cowlishaw, G., Mace, G.M., 2000. Predicting extinction risk in declining species. Proc. R. Soc. Lond. B 267, 1947–1952.CrossRefGoogle Scholar
  68. Reynolds, J.H., Thompson, W.L., Russell, B., 2011. Planning for success: identifying effective and efficient survey designs for monitoring. Biol. Conserv. 144, 1278–1284.CrossRefGoogle Scholar
  69. Ricklefs, R.E., 2007. The Economy of Nature, 5th ed. Freeman, New York.Google Scholar
  70. Roff, D.A., 2002. Life History Evolution. Sinauer Associates Inc., Sunderland.Google Scholar
  71. Rolandsen, CM., Solberg, E.J., Heim, M., Holmstrøm, F., Solem, M.I., Sæther, B., 2008. Accuracy and repeatability of moose (Alces alces) age as estimated from dental cement layers. Eur.J. Wildl. Res. 54 (1), 6–14.CrossRefGoogle Scholar
  72. Ryser, J., 1988. Determination of growth and maturation in the common frog, Rana temporaria by skeletochronology. J. Zool. 216, 673–685.CrossRefGoogle Scholar
  73. Sæther, B.E., Andersen, R., Hjeljord, O., Heim, M., 1996. Ecological correlates of regional variation in life history of the moose Alces alces. Ecology 77, 1496–1500.CrossRefGoogle Scholar
  74. Sagor, E.S., Oullet, M., Barten, E., Green, D., 1998. Skeletochronology and geographic variation in age structure in the wood frog, Rana sylvatica. J. Herpertol. 32, 469–474.CrossRefGoogle Scholar
  75. Signer, C, Ruf, T., Arnold, A., 2010. Hypometabolism and masking: the strategies of Alpine ibex to endure harsh over-wintering conditions. Funct. Ecol. 25, 537–547.CrossRefGoogle Scholar
  76. Stearns, S.C., 1992. The Evolution of Life Histories. Oxford Univer. Press, New York.Google Scholar
  77. Tuljapurkar, S., Caswell, H., 1996. Structured Population Models in Marine, Terrestrial, and Freshwater Systems. Chapman & Hall, New York.Google Scholar
  78. Tumarkin-Deratzian, A., 2007. Fibrolamellarbone in wild adult Alligator mississippi-ensis.J. Herpetol. 41, 341–345.CrossRefGoogle Scholar
  79. Turbill, C, Ruf, T., Mang, T., Arnold, W., 2011. Regulation of heart rate and rumen temperature in red deer: effects of Seaton and food intake. J. Exp. Biol. 214, 963–970.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Vanpé, C, Gaillard, J.M., Morellet, N., Kjellander, P., Liberg, O., Delorme, D., Hewi-son, A.J.M., 2009. Age-specific variation in male breeding success of a territorial ungulate species, the European roe deer. J. Mamm. 90, 661–665.CrossRefGoogle Scholar
  81. Williams, L.R., Echelle, A.A., Toepfer, C.S., Williams-Marsha, M.G., Fisher, F.L., 1999. Simulation modeling of population variability for the leopard darter (Percidae: Percina pantheria). Southwest. Nat. 44, 70–477.CrossRefGoogle Scholar
  82. Woodward, H.N., Padian, K., Lee, A.H., 2013. Skeletochronology. In: Padian, K., Lamm, E.-T. (Eds.), Bone Histology of Fossil Tetrapods. University of California Press, Berkeley, Los Angeles, London, pp. 195–216.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2013

Authors and Affiliations

  • Nekane Marín-Moratalla
    • 1
    Email author
  • Xavier Jordana
    • 1
  • Meike Köhler
    • 2
    • 3
  1. 1.Institut Català de Paleontologia Miquel CrusafontUniversitat Autònoma de BarcelonaBellaterraSpain
  2. 2.ICREA at the Institut Català de Paleontologia Miquel CrusafontUniversitat Autònoma de BarcelonaBellaterraSpain
  3. 3.Departament d’Ecologia, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain

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