Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2015 Jul 8;10(7):e0131131.
doi: 10.1371/journal.pone.0131131. eCollection 2015.

First Reported Cases of Biomechanically Adaptive Bone Modeling in Non-Avian Dinosaurs

Jorge Cubo  1 , Holly Woodward  2 , Ewan Wolff  3 , John R Horner  4
Affiliations

First Reported Cases of Biomechanically Adaptive Bone Modeling in Non-Avian Dinosaurs

Jorge Cubo et al. PLoS One. .

Abstract

Predator confrontation or predator evasion frequently produces bone fractures in potential prey in the wild. Although there are reports of healed bone injuries and pathologies in non-avian dinosaurs, no previously published instances of biomechanically adaptive bone modeling exist. Two tibiae from an ontogenetic sample of fifty specimens of the herbivorous dinosaur Maiasaura peeblesorum (Ornithopoda: Hadrosaurinae) exhibit exostoses. We show that these outgrowths are cases of biomechanically adaptive periosteal bone modeling resulting from overstrain on the tibia after a fibula fracture. Histological and biomechanical results are congruent with predictions derived from this hypothesis. Histologically, the outgrowths are constituted by radial fibrolamellar periosteal bone tissue formed at very high growth rates, as expected in a process of rapid strain equilibration response. These outgrowths show greater compactness at the periphery, where tensile and compressive biomechanical constraints are higher. Moreover, these outgrowths increase the maximum bending strength in the direction of the stresses derived from locomotion. They are located on the antero-lateral side of the tibia, as expected in a presumably bipedal one year old individual, and in the posterior position of the tibia, as expected in a presumably quadrupedal individual at least four years of age. These results reinforce myological evidence suggesting that Maiasaura underwent an ontogenetic shift from the primitive ornithischian bipedal condition when young to a derived quadrupedal posture when older.

PubMed Disclaimer

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Overall views of the bones showing outgrowths.
(A) Right tibiae of a one year old Maiasaura specimen and (B) a four year old specimen. The red lines indicate where the histological sample was taken. Proximal is to the left, distal to the right. Scale bar equals 10 cm.
Fig 2
Fig 2. Bone cross-sections showing the general histological aspect of the outgrowths.
(A) Right tibiae of a presumably bipedal Maiasaura specimen and (B) a presumably quadrupedal specimen. Scale bar for bone sections equals 1 cm. Abbreviations: Ant., anterior; Lat., lateral; Med., medial; Post., posterior.
Fig 3
Fig 3. Detailed histological aspect of the outgrowths.
Outgrowths are constituted by radial fibrolamellar periosteal bone tissue formed at very high bone growth rate [12, 13], to compensate the overstrain presumably produced by a fibula fracture. These outgrowths involve two pulses of periosteal growth in the one year old specimen (A) and a single pulse in the four years old specimen (B). Considering that the further from the neutral plane of bending, the higher the biomechanical constraints [14, 15], we expect higher compactness on the periphery of bone outgrowth to compensate for the increased constraints on the bone surface. Our observations support these predictions in both the first and second bursts of growth of the one year old specimen (A) and in the single burst of growth of the four years old specimen (B). Scale bar equals 1 mm.
Fig 4
Fig 4. Biomechanical analysis of the outgrowths of the one year individual MOR 005-T9.
Entire bone cross-section (A) and biomechanical analyses of bone areas (white surfaces) before fibula failure (B), after the first outgrowth subsequent to fibula failure (C), and after the second outgrowth (D). The black lines represent antero-posterior and latero-medial axes for reference. The blue line represents the maximum second moment of the area (Imax), which is proportional to the bending strength of the bone. The red line is the neutral plane. Before fibula failure, tibia Imax was oriented at 38° relative to the antero-posterior axis (B). After fibula failure, tibia Imax increased 13.8% towards the mediolateral axis (from 38° to 49°), as expected in a presumably bipedal, one year old specimen (C). The second burst of growth further increased tibia bending strength (34.6% relative to the situation before the trauma) towards the mediolateral axis (from 49° to 58°) (D). Scale bar equals 1 cm. Abbreviations: Ant., anterior; Lat., lateral; Med., medial; Post., posterior.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Horner JR, Ricqlès A, Padian K. Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum: growth dynamics and physiology based on an ontogenetic series of skeletal elements. J Vert Paleontol. 2000;20: 109–123.
    1. Horner JR, Padian K. Age and growth dynamics of Tyrannosaurus rex . Proc R Soc Lond B. 2004;271: 1875–1880. - PMC - PubMed
    1. Bybee PJ, Lee AH, Lamm ET. Sizing the Jurassic theropod dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs. J Morphol. 2006;267: 347–359. - PubMed
    1. Mead AJ, Patterson DB. Skeletal lesions in a population of Virginia opossums (Didelphis virginiana) from Baldwin county, Georgia. J Wildlife Dis. 2009;45: 325–332. - PubMed
    1. Schultz AH. Notes on diseases and healed fractures of wild apes and their bearing on the antiquity of pathological conditions in man. B Hist Med. 1939;12: 571–582.

Publication types

Grants and funding

Funding and support for HW was provided by Gerry Ohrstrom, the Museum of the Rockies, the Jurassic Foundation, the Geological Society of America, and NSF grant #EAR 8705986. Funding and support for JC was provided by the CNRS (France), the UPMC-Sorbonne Universités (France) and by the grants CGL-2011-23919 and CGL-2012-34459 of the Spanish Ministry of Economy and Competitiveness. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

LinkOut - more resources