The Science of Nature

, 103:58 | Cite as

Scaling effect on the mid-diaphysis properties of long bones—the case of the Cervidae (deer)

  • Eli Amson
  • Christian Kolb
Original Paper


How skeletal elements scale to size is a fundamental question in biology. While the external shape of long bones was intensively studied, an important component of their organization is also found in their less accessible inner structure. Here, we studied mid-diaphyseal properties of limb long bones, characterizing notably the thickness of their cortices (bone walls), in order to test whether body size directly influences bone inner organization. Previous examinations of scaling in long bones used broad samplings to encompass a wide range of body sizes. To account for the effect of confounding factors related to different lifestyles, we focused our comprehensive sampling on a mammalian clade that comprises various body sizes but a relatively uniform lifestyle, the Cervidae. Positive allometry was found in femoral cross-sectional shape, indicating greater directional bending rigidity in large-sized taxa. None of the compactness parameters scaled allometrically in any of their bones. The cortices of sampled zeugopodial bones (tibia and radius) were found as significantly thicker than those of stylopodial bones (femur and humerus). Furthermore, while the mean relative cortical thickness values for both stylopodial and zeugopodial bones are close to mass-saving optima, the variance for the stylopodial bones is significantly lower. This suggests that mass saving is less intensively selected in zeugopodial bones. Finally, the long-legged Elk (Alces) and the short-legged dwarf Cretan deer (Candiacervus) featured rather thin and thick cortices, respectively, suggesting that the acquisition of a different limb proportion is accompanied by a modification of the relative mid-diaphyseal cortical thickness.


Allometry Bone compactness Cervidae Cortical thickness Cross-sectional shape Long bone 



We thank Hatem Alkadhi (UniversitätsSpital Zürich) for performing the CT scans. Christine Argot, Christine Lefèvre, and Joséphine Lesur (Muséum national d’Histoire naturelle, Paris), Emma Bernard (Natural History Museum, London), Christiane Funk and Frieder Mayer (Museum für Naturkunde, Berlin), Loïc Costeur (Naturhistorisches Museum Basel), John de Vos (Naturalis Biodiversity Center, Leiden), Heinz Furrer, Christian Klug, and Winand Brinkmann (Paläontologisches Institut und Museum der Universität Zürich, PIMUZ), Shoji Hayashi and Hiroyuki Taruno (Osaka Museum of Natural History), Renate Lücht and Heiner Luttmann (Zoologisches Institut der Universität Kiel), Nigel Monaghan (National Museum of Ireland, Natural History), Barbara Oberholzer (Zoologisches Museum der Universität Zürich), Gertrud E. Rössner (Bayerische Staatssammlung für Paläontologie und Geologie), Christian Stauffer (Wildnispark Zürich), and Frank Zachos and Alexander Bibl (Naturhistorisches Museum Wien) are acknowledged for granting us access to the collections under their care. Marcelo Sánchez-Villagra and Juan Carillo (both PIMUZ) are thanked for fruitful discussions. Stephan Spiekman (Leiden University) and Philipp Münst (University of Zurich) are thanked for their preliminary data acquisition and analyses. We finally thank three anonymous reviewers and Marcelo Sánchez-Villagra and Andrew Biewener (Harvard University) for the substantial improvements they brought to previous versions of the manuscript. Both authors were funded by the Swiss National Fund SNF 31003A_149605 granted to M. R. Sánchez-Villagra, and EA was subsequently funded by the Alexander von Humboldt Foundation.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


Both authors were funded by the Swiss National Fund SNF 31003A_149605 granted to M. R. Sánchez-Villagra, and EA was subsequently funded by the Alexander von Humboldt Foundation.

Supplementary material

114_2016_1379_MOESM1_ESM.docx (4.3 mb)
Online resource 1 Supplementary figure and tables (DOCX 4.34 MB)
114_2016_1379_MOESM2_ESM.nex (29 kb)
Online resource 2 This nexus file comprises the matrices of data and timetree allowing to perform the phylogenetically informed statistical tests on the relative cortical thickness (P parameter) and associated section maximum diameter (MD). (NEX 28 kb)
114_2016_1379_MOESM3_ESM.nex (30 kb)
Online resource 3 This nexus file comprises the matrices of data and timetree allowing to perform the phylogenetically informed statistical tests on the cross-sectional shape (CSS) and associated cross-sectional area (CSA). (NEX 29 kb)
114_2016_1379_MOESM4_ESM.xlsx (171 kb)
Online resource 4 This MS excel file comprises all measured compactness parameters for the whole dataset. (XLSX 170 kb)
114_2016_1379_MOESM5_ESM.xlsx (26 kb)
Online resource 5 This MS excel file comprises all measured slice geometry parameters for the whole dataset. (XLSX 26 kb)


  1. Alexander RM, Jayes AS, Maloiy GMO, Wathuta EM (1979) Allometry of the limb bones of mammals from shrews (Sorex) to elephant (Loxodonta). J Zool 189:305–314. doi: 10.1111/j.1469-7998.1979.tb03964.x CrossRefGoogle Scholar
  2. Amson E, Kolb C, Scheyer TM, Sánchez-Villagra MR (2015) Growth and life history of middle Miocene deer (Mammalia, Cervidae) based on bone histology. C R Palevol 14:637–645. doi: 10.1016/j.crpv.2015.07.001 CrossRefGoogle Scholar
  3. Amson E, de Muizon C, Laurin M, Argot C, de Buffrénil V (2014) Gradual adaptation of bone structure to aquatic lifestyle in extinct sloths from Peru. Proc R Soc B 281:20140192. doi: 10.1098/rspb.2014.0192 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bernáth B, Suhai B, Gerics B, Csorba G, Gasparik M, Horváth G (2004) Testing the biomechanical optimality of the wall thickness of limb bones in the red fox (Vulpes vulpes). J Biomech 37:1561–1572. doi: 10.1016/j.jbiomech.2004.01.008 CrossRefPubMedGoogle Scholar
  5. Bertram JEA, Biewener AA (1992) Allometry and curvature in the long bones of quadrupedal mammals. J Zool 226:455–467. doi: 10.1111/j.1469-7998.1992.tb07492.x CrossRefGoogle Scholar
  6. Biewener AA (1989) Scaling body support in mammals: limb posture and muscle mechanics. Science 245:45–48CrossRefPubMedGoogle Scholar
  7. Biewener AA (1991) Musculoskeletal design in relation to body size. J Biomech 24:19–29. doi: 10.1016/0021-9290(91)90374-V CrossRefPubMedGoogle Scholar
  8. Biknevicius AR (1993) Biomechanical scaling of limb bones and differential limb use in caviomorph rodents. J Mammal 74:95–107CrossRefGoogle Scholar
  9. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745CrossRefPubMedGoogle Scholar
  10. Breda M (2008) Palaeoecology and palaeoethology of the Plio-Pleistocene genus Cervalces (Cervidae, Mammalia) in Eurasia. J Vertebr Paleontol 28:886–899. doi: 10.1671/0272-4634(2008)28 CrossRefGoogle Scholar
  11. Canoville A, Laurin M (2010) Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Biol J Linn Soc 100:384–406. doi: 10.1111/j.1095-8312.2010.01431.x CrossRefGoogle Scholar
  12. Cosman MN, Sparrow LM, Rolian C (2016) Changes in shape and cross-sectional geometry in the tibia of mice selectively bred for increases in relative bone length. J Anat 288:940–951. doi: 10.1111/joa.12459 CrossRefGoogle Scholar
  13. Costeur L, Guérin C, Maridet O (2012) Paléoécologie et paléoenvironnement du site miocène de Sansan. In: Peigné S, Sen S (eds) Mammifères Sansan. Mémoires du Muséum Natl d’Histoire Nat, Paris, pp. 661–693Google Scholar
  14. Curran SC (2012) Expanding ecomorphological methods: geometric morphometric analysis of Cervidae post-crania. J Archaeol Sci 39:1172–1182. doi: 10.1016/j.jas.2011.12.028 CrossRefGoogle Scholar
  15. Currey JD (2003) The many adaptations of bone. J Biomech 36:1487–1495. doi: 10.1016/S0021-9290(03)00124-6 CrossRefPubMedGoogle Scholar
  16. Currey JD, Alexander RM (1985) The thickness of the walls of tubular bones. J Zool 206:453–468. doi: 10.1111/j.1469-7998.1985.tb03551.x CrossRefGoogle Scholar
  17. Demes B, Jungers WL, Selpien K (1991) Body size, locomotion, and long bone cross-sectional geometry in indriid primates. Am J Phys Anthropol 86:537–547. doi: 10.1002/ajpa.1330860409 CrossRefPubMedGoogle Scholar
  18. Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, Schmid B, Hutchinson JR, Shefelbine SJ (2010) BoneJ: free and extensible bone image analysis in ImageJ. Bone 47:1076–1079. doi: 10.1016/j.bone.2010.08.023 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Doube M, Klosowski MM, Wiktorowicz-Conroy AM, Hutchinson JR, Shefelbine SJ (2011) Trabecular bone scales allometrically in mammals and birds. Proc R Soc B 278:3067–3073. doi: 10.1098/rspb.2011.0069 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Feldhamer GA, Farris-Renner KC, Barker CM (1988) Dama dama. Mamm Species 317:1–8CrossRefGoogle Scholar
  21. Francillon-Vieillot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ, Sire J-Y, Zylberberg L, de Ricqlès A (1990) Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JG (ed) Skeletal biomineralization: patterns, processes and evolutionary trends, vol 1. Van Nostrand Reinhold, New York, pp. 471–530Google Scholar
  22. Franzmann AW (1981) Alces alces. Mamm Species 154:1–7CrossRefGoogle Scholar
  23. Van Der Geer A, Dermitzakis M, De Vos J (2006) Relative growth of the metapodals in a juvenile island deer: Candiacervus (Mammalia, Cervidae) from Pleistocene of Crete. Hell J Geosci 41:119–125Google Scholar
  24. Van Der Geer AAE, Lyras G, de Vos J, Dermitzakis M (2010) Evolution of island mammals. Adaptation and extinction of placental mammals on islands. Blackwell publishing, ChichesterCrossRefGoogle Scholar
  25. Geist V (1998) Deer of the world: their evolution, behaviour, and ecology. Stackpole Books, MechanicsburgGoogle Scholar
  26. Gentry AW, Rössner GE, Heizmann EPJ (1999) Suborder Ruminantia. In: Rössner GE, Heissig K (eds) Miocene land mammals of Europe. Verlag Dr. Friedrich Pfeil, München, pp. 225–258Google Scholar
  27. Germain D, Laurin M (2005) Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zool Scr 34:335–350. doi: 10.1111/j.1463-6409.2005.00198.x CrossRefGoogle Scholar
  28. Girondot M, Laurin M (2003) Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. J Vertebr Paleontol 23:458–461CrossRefGoogle Scholar
  29. Gould SJ (1974) The origin and function of ‘bizarre’ structures: antler size and skull size in the ‘Irish elk,’ Megaloceros giganteus. Evolution 28:191–220CrossRefGoogle Scholar
  30. Hammer Ø, Harper DAT, Ryan PD (2001) Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9. doi: 10.1016/j.bcp.2008.05.025 Google Scholar
  31. Hassanin A, Delsuc F, Ropiquet A, Hammer C, Jansen Van Vuuren B, Matthee C, Ruiz-Garcia M, Catzeflis F, Areskoug V, Nguyen TT, Couloux A (2012) Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C R Biol 335:32–50. doi: 10.1016/j.crvi.2011.11.002 CrossRefPubMedGoogle Scholar
  32. Houssaye A, Waskow K, Hayashi S, Lee AH, Hutchinson JR (2015) Biomechanical evolution of solid bones in large animals: a microanatomical investigation. Biol J Linn Soc 117:350–371. doi: 10.1111/bij.12660 CrossRefGoogle Scholar
  33. Josse S, Moreau T, Laurin M (2006) Stratigraphic tools for Mesquite
  34. Klingenberg CP (1998) Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 73:79–123. doi: 10.1111/j.1469-185X.1997.tb00026.x CrossRefPubMedGoogle Scholar
  35. Kriloff A, Germain D, Canoville A, Vincent P, Sache M, Laurin M (2008) Evolution of bone microanatomy of the tetrapod tibia and its use in palaeobiological inference. J Evol Biol 21:807–826. doi: 10.1111/j.1420-9101.2008.01512.x CrossRefPubMedGoogle Scholar
  36. Laurin M (2004) The evolution of body size, Cope’s rule and the origin of amniotes. Syst Biol 53:594–622. doi: 10.1080/10635150490445706 CrossRefPubMedGoogle Scholar
  37. Lemaître J-F, Vanpé C, Plard F, Gaillard JM (2014) The allometry between secondary sexual traits and body size is nonlinear among cervids. Biol Lett 10:20130869. doi: 10.1098/rsbl.2013.0869 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Linkert M, Rueden CT, Allan C, Burel JM, Moore W, Patterson A, Loranger B, Moore J, Neves C, MacDonald D, Tarkowska A, Sticco C, Hill E, Rossner M, Eliceiri KW, Swedlow JR (2010) Metadata matters: access to image data in the real world. J Cell Biol 189:777–782. doi: 10.1083/jcb.201004104 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 3.04.
  40. de Margerie E, Sanchez S, Cubo J, Castanet J (2005) Torsional resistance as a principal component of the structural design of long bones: comparative multivariate evidence in birds. Anat Rec 282A:49–66. doi: 10.1002/ar.a.20141 Google Scholar
  41. Meier PS, Bickelmann C, Scheyer TM, Koyabu D, Sánchez-Villagra MR (2013) Evolution of bone compactness in extant and extinct moles (Talpidae): exploring humeral microstructure in small fossorial mammals. BMC Evol Biol 13:55. doi: 10.1186/1471-2148-13-55 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Nordin M, Frankel VH (2001) Basic biomechanics of the musculoskeletal system. Lippincott Williams & Wilkins, BaltimoreGoogle Scholar
  43. Nowak RM, Paradiso JL (1983) Walker’s mammals of the world, vol I–II, 4th edn. John Hopkins University Press, BaltimoreGoogle Scholar
  44. Padian K, Lamm E-T (2013) Bone histology of fossil tetrapods: advancing methods, analysis, and interpretation. University of California Press, BerkleyCrossRefGoogle Scholar
  45. Quemeneur S, de Buffrénil V, Laurin M (2013) Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates. Biol J Linn Soc 109:644–655. doi: 10.1111/bij.12066 CrossRefGoogle Scholar
  46. Ruff CB, Holt B, Trinkaus E (2006) Who’s afraid of the big bad Wolff?: “Wolff’s law” and bone functional adaptation. Am J Phys Anthropol 129:484–498. doi: 10.1002/ajpa.20371 CrossRefPubMedGoogle Scholar
  47. Ryan TM, Shaw CN (2013) Trabecular bone microstructure scales allometrically in the primate humerus and femur. Proc R Soc B 280:20130172. doi: 10.1098/rspb.2013.0172 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ryan TM, Shaw CN (2015) Gracility of the modern Homo sapiens skeleton is the result of decreased biomechanical loading. Proc Natl Acad Sci 112:372–377. doi: 10.1073/pnas.1418646112 CrossRefPubMedGoogle Scholar
  49. Sanchez S, Ahlberg PE, Trinajstic KM, Mirone A, Tafforeau P (2012) Three-dimensional synchrotron virtual paleohistology: a new insight into the world of fossil bone microstructures. Microsc Microanal 18:1095–1105. doi: 10.1017/S1431927612001079 CrossRefPubMedGoogle Scholar
  50. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682. doi: 10.1038/nmeth.2019 CrossRefPubMedGoogle Scholar
  51. Scott KM (1983) Prediction of body weight of fossil Artiodactyla. Zool J Linnean Soc 77:199–215. doi: 10.1111/j.1096-3642.1983.tb00098.x CrossRefGoogle Scholar
  52. Swartz SM, Parker A, Huo C (1998) Theoretical and empirical scaling patterns and topological homology in bone trabeculae. J Exp Biol 201:573–590PubMedGoogle Scholar
  53. Tacutu R, Craig CT, Budovsky A, Wuttke D, Lehmann G, Taranukha D, Costa J, Fraifeld VE, De Magalhães J (2013) Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res 41:D1027–D1033. doi: 10.1093/nar/gks1155 CrossRefPubMedGoogle Scholar
  54. Vislobokova IA (2013) Morphology, taxonomy, and phylogeny of megacerines (Megacerini, Cervidae, Artiodactyla). Paleontol J 47:833–950. doi: 10.1134/S0031030113080017 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Paläontologisches Institut und Museum der Universität ZürichZürichSwitzerland
  2. 2.AG Morphologie und Formengeschichte, Bild Wissen Gestaltung-ein Interdisziplinäres Labor and Institut für BiologieHumboldt-UniversitätBerlinGermany

Personalised recommendations