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The function(s) of bone ornamentation in the crocodylomorph osteoderms: a biomechanical model based on a finite element analysis

Published online by Cambridge University Press:  27 February 2019

François Clarac ,
Florent Goussard ,
Vivian de Buffrénil  and
Vittorio Sansalone
François Clarac
Affiliation:
Sorbonne Université, Centre National de la Recherche Scientifique, Institut des Sciences de la Terre de Paris, UMR 7193, 4 place Jussieu, BC 19-75005 Paris, France; and Département Histoire de la Terre, UMR 7207, Centre de Recherche en Paléontologie–Paris, Muséum National d'Histoire Naturelle/Centre National de la Recherche Scientifique /Sorbonne Université, Bâtiment de Géologie Paris Cedex 05, F-75231, France. E-mail: francois.clarac@mnhn.fr.
Florent Goussard
Affiliation:
Département Histoire de la Terre, UMR 7207, Centre de Recherche en Paléontologie–Paris, Muséum National d'Histoire Naturelle/Centre National de la Recherche Scientifique/ Sorbonne Université, Bâtiment de Paléontologie Paris Cedex 05, F-75231, France. E-mail: florent.goussard@mnhn.fr
Vivian de Buffrénil
Affiliation:
Département Histoire de la Terre, UMR 7207, Centre de Recherche en Paléontologie–Paris, Muséum National d'Histoire Naturelle/Centre National de la Recherche Scientifique/Sorbonne Université, Bâtiment de Géologie Paris Cedex 05, F-75231, France. E-mail: vivian.de-buffrenil@mnhn.fr
Vittorio Sansalone
Affiliation:
Université Paris-Est, Laboratoire Modélisation et Simulation Multi Echelle, MSME UMR 8208 CNRS, 61 avenue du Général de Gaulle, 94010 Créteil Cedex, France. E-mail: vittorio.sansalone@u-pec.fr
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Abstract

This paper aims at assessing the influence of the bone ornamentation and, specifically, the associated loss of bone mass on the mechanical response of the crocodylomorph osteoderms. To this end, we have performed three-dimensional (3D) modeling and a finite element analysis on a sample that includes both extant dry bones and well-preserved fossils tracing back to the Late Triassic. We simulated an external attack under various angles on the apical surface of each osteoderm and further repeated the simulation on an equivalent set of smoothed 3D-modeled osteoderms. The comparative results indicated that the presence of an apical sculpture has no significant influence on the von Mises stress distribution in the osteoderm volume, although it produces a slight increase in its numerical score. Moreover, performing parametric analyses, we showed that the Young's modulus of the osteoderm, which may vary depending on the bone porosity, the collagen fiber orientation, or the calcification density, has no impact on the von Mises stress distribution inside the osteoderm volume. As the crocodylomorph bone ornamentation is continuously remodeled by pit resorption and secondary bone deposition, we assume that the apical sculpture may be the outcome of a trade-off between the bone mechanical resistance and the involvement in physiological functions. These physiological functions are indeed based on the setup of a bone superficial vessel network and/or the recurrent release of mineral elements into the plasma: heat transfers during basking and respiratory acidosis buffering during prolonged apnea in neosuchians and teleosaurids; compensatory homeostasis in response to general calcium deficiencies. On a general morphological basis, the osteoderm geometric variability within our sample leads us to assess that the global osteoderm geometry (whether square or rectangular) does not influence the von Mises stress, whereas the presence of a dorsal keel would somewhat reduce the stress along the vertical axis.

Type
Articles
Information
Paleobiology , Volume 45 , Issue 1 , February 2019 , pp. 182 - 200
Copyright
Copyright © 2019 The Paleontological Society. All rights reserved 

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Footnotes

Present address: Uppsala University, Department of Organismal Biology, Subdepartment of Evolution and Development, Norbyvägen 18A, SE-752 36, Uppsala, Sweden.

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.5qb8387

References

Literature Cited

Acrai, B., and Wagner, H. D.. 2013. Micro-structure and mechanical properties of the turtle carapace as a biological composite shield. Acta Biomaterialia 9:5890–5902.Google Scholar
Akhtar, R., Sherratt, M. J., Kennedy Cruickshank, J., and Derby, B.. 2011. Characterizing the elastic properties of tissues. Materials Today 14:96–105.Google Scholar
Anjan, B., and Bhullar, S.. 2008. Osteoderms of the California legless lizard Anniella (Squamata: Anguidae) and their relevance for considerations of miniaturization. Copeia 4:785–793.Google Scholar
Azevedo, F. C. C., and Verdade, L. M.. 2011. Predator–prey interactions: jaguar predation on caiman in a floodplain forest. Journal of Zoology 286:200–207.Google Scholar
Benton, M. J, and Walker, A. D.. 2002. Erpetosuchus, a crocodile-like basal archosaur from the Late Triassic of Elgin, Scotland. Zoological Journal of the Linnean Society 136:25–47.Google Scholar
Blanton, P. L., and Biggs, N. L.. 1968. Density of fresh and embalmed human compact and cancellous bone. American Journal of Physiological Anthropology 29:39–44.Google Scholar
Bochaton, C., de Buffrénil, V., Lemoine, M., Bailon, S., and Ineich, Y.. 2013. Body location and tail regeneration effects on osteoderms morphology—are they useful tools for systematic, paleontology, and skeletochronology in diploglossine lizards (Squamata, Anguidae)? Journal of Morphology 276:1333–1344.Google Scholar
Broeckhoven, C., Diedericks, G., and Mouton, P. L. F. N.. 2015. What doesn't kill you might make you stronger: functional basis for variation in body armour. Journal of Animal Ecology 84:1213–1221.Google Scholar
Broin, F., and Taquet, P.. 1966. Découverte d'un crocodilien nouveau dans le Crétacé inférieur du Sahara (Discovery of a new crocodilian in the lower Cretaceous of the Sahara). Comptes Rendus de l'Académie des Sciences, Paris, série D 262: 2326–2329.Google Scholar
Buffrénil, V. de. 1982. Morphogenesis of bone ornamentation in extant and extinct crocodilians. Zoomorphology 99:155–166.Google Scholar
Buffrénil, V. de, Clarac, F., Fau, M., Martin, S., Martin, B., Pellé, E., and Laurin, M.. 2015. Differentiation and growth of bone ornamentation in vertebrates: a comparative histological study among the Crocodylomorpha. Journal of Morphology 21:1–21.Google Scholar
Buffrénil, V. de, Clarac, F., Canoville, A., and Laurin, M.. 2016. Comparative data on the differentiation and growth of bone ornamentation in gnathostomes (Chordata: Vertebrata). Journal of Morphology 277:634–670.Google Scholar
Burdak, V. D. 1986. Fonction de protection et fonction de dissimulation du squelette externe. In Meunier, F. J. and Sire, J. Y., eds. Morphologie fonctionnelle du tégument écailleux des poissons. Société Française d'Ichtyologie 10(3):31–88. Paris, France.Google Scholar
Burns, M. E., Vickaryous, M. K., and Currie, P. J. 2013. Histological variability in fossil and recent alligatoroid osteoderms: systematic and functional implications. Journal of Morphology 274:676–686.Google Scholar
Bystrow, A. P. 1935. Morphologische Untersuchungen der Deckknochen des Schädels der Wirbeltiere. I. Mitteilung—Schädel der Stegocephalen. Acta Zoologica Stockholm 16:65–141.Google Scholar
Cerda, I. A., and Desojo, J. B.. 2011. Dermal armour histology of aetosaurs (Archosauria: Pseudosuchia), from the Upper Triassic of Argentina and Brazil. Lethaia 44:417–428.Google Scholar
Cerda, I. A., Desojo, J. B., Scheyer, T. M., and Schultz, C. L.. 2013. Osteoderm microstructure of “rauisuchian” archosaurs from South America. Geobios 46:273–283.Google Scholar
Chen, I. H., Kiang, J. H., Correa, V., Lopeza, M. I., Chen, P. Y., McKittrick, J., and Meyers, M. A.. 2011. Armadillo armor: mechanical testing and micro-structural evaluation. Journal of the Mechanical Behavior of Biomedical Materials 4:713–722.Google Scholar
Chen, I. H., Yang, W., and Meyers, M. A.. 2014. Alligator osteoderms: mechanical behavior and hierarchical structure. Material Science Engineering C 35:441–448.Google Scholar
Chen, I. H., Yang, W., and Meyers, M. A.. 2015. Leatherback sea turtle shell: a tough and flexible biological design. Acta Biomaterialia 28:2–12.Google Scholar
Clarac, F., Souter, T., Cornette, R., Cubo, J., and de Buffrénil, V.. 2015. A quantitative assessment of bone area increase due to ornamentation in the Crocodylia. Journal of Morphology 276:1183–1192.Google Scholar
Clarac, F., de Buffrénil, V., Brochu, C. A., and Cubo, J.. 2017a. The evolution of bone ornamentation in Pseudosuchia: morphological constraints versus ecological adaptation. Biological Journal of the Linnean Society 121:395–408.Google Scholar
Clarac, F., Goussard, F., Teresi, L., de Buffrénil, V., and Sansalone, V.. 2017b. Do the ornamented osteoderms influence the heat conduction through the skin? A finite element analysis in Crocodylomorpha. Journal of Thermal Biology 69:39–53.Google Scholar
Clarac, F., de Buffrénil, V., Cubo, J., and Quilhac, A.. 2018. Vascularization in ornamented osteoderms: physiological implications in ectothermy and amphibious lifestyle in the crocodylomorphs? Anatomical Record 301:175–183.Google Scholar
Coldiron, R. W. 1974. Possible functions of ornament in the labyrinthodont amphibians. Occasional Papers of the of Museum National History of Kansas 33:1–19.Google Scholar
Cope, E. D. 1861. Recent species of Emydosaurian reptiles represented in the Museum of the Academy. Proceedings of the Academy of Natural Sciences of Philadelphia1860:549–551.Google Scholar
Dacke, C. G., Elsey, R. M., Trosclair, P. L., Sugiyama, T., Nevarez, J. G., and Schweitzer, M. H.. 2015. Alligator osteoderms as a source of labile calcium for eggshell formation. Journal of Zoology 297:255–264.Google Scholar
Da Silveira, R., Ramalho, E. E., Thorbjarnarson, J. B., and Magnusson, W. E.. 2010. Depredation by jaguars on caimans and importance of reptiles in the diet of jaguar. Journal of Herpetology 44:418–424.Google Scholar
Desojo, J. B., and Vizcaíno, S.. 2009. Jaw biomechanics in the South American aetosaur Neoaetosauroides engaeus. Paläontologische Zeitschrift 83:499–510.Google Scholar
Desojo, J. B., Heckert, A. B., Martz, J. W., Parker, W. G., Schoch, R. R., Small, B. J., and Sulej, T.. 2013. Aetosauria: a clade of armoured pseudosuchians from the Late Triassic continental beds. In Nesbitt, S. J., Desojo, J. B., and Irmis, R. B., eds. Anatomy, phylogeny and palaeobiology of early archosaurs and their kin. Geological Society Special Publication 379:203–239.Google Scholar
Dubansky, B. H., and Dubansky, B. D.. 2018. Natural development of dermal ectopic bone in the American alligator (Alligator mississippiensis) resembles heterotopic ossification disorders in humans. Anatomical Record 301:56–76.Google Scholar
Du Plessis, A., Broeckhoven, C., Yadroitsev, I., Yadroitsava, I., and le Roux, S. G.. 2018. Analyzing nature's protective design: the glyptodont body armor. Journal of the Mechanical Behavior of Biomedical Materials 82:218–223.Google Scholar
Dzik, J., and Sulej, T.. 2007. A review of the early Late Triassic Krasiejów biota from Silesia, Poland. Palaeontologia Polonica 64:3–27.Google Scholar
Erickson, G. M., Gignac, P. M., Steppan, S. J., Lappin, A. K., Vliet, K. A., Brueggen, J. D., Inouye, B. D., Kledzik, D., and Webb, G. J. W.. 2012. Insights into the ecology and evolutionary success of crocodilians revealed through bite-force and tooth-pressure experimentation. PLoS ONE 7(3):e31781. doi: 10.1371/journal.pone.0031781.Google Scholar
Farlow, J. O., Hayashi, S., and Tattersall, G. J.. 2010. Internal vascularity of the dermal plates of Stegosaurus (Ornithischia, Thyreophora). Swiss Journal of Geosciences 103:173–185.Google Scholar
Fraas, O. 1877. Aetosaurus ferratus Fr. Die gepanzerte Vogel-Echse aus dem Stubensandstein bei Stuttgar. Festschrift zur Feier des 400jährigen Jubiläums der Eberhard-Karls-Universät zu Tübingen, Wurttembergische naturwissenschaftliche jahreshefte 33(3):1–22.Google Scholar
Gasc, J. P. 1981. Axial musculature B. Crocodilia. In Gans, C., and Parsons, T. S., eds. Biology of the Reptilia 11:372–376. London.Google Scholar
Gilbert, S. F., Loredo, G. A., Brukman, A., and Burke, A. C.. 2001. Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution. Evolution and Development 3:47–58.Google Scholar
Groombridge, B. 1987. The distribution and status of world crocodilians. Pp. 9–21 in Webb, G. J. W., Manolis, S. C., and Whitehead, P. J., eds. Wildlife management—crocodiles and alligators. Surrey Beatty and Sons, Chipping Norton, NSW, Australia.Google Scholar
Hammer, Ø., Harper, D. A. T., and Ryan, P. D.. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1):9. http://palaeoelectronica.org/2001_1/past/issue1_01.htm.Google Scholar
Heckert, A. B., and Lucas, S. G.. 2000. Taxonomy, phylogeny, biostratigraphy, biochronology, paleobiogeography, andevolution of the Late Triassic Aetosauria (Archosauria:Crurotarsi). Zentralblatt für Geologie und Paläontologie 11–12:1539–1587.Google Scholar
Heckert, A. B., Fraser, C. N., and Schneider, V. P.. 2017. A new species of Coahomasuchus (Archosauria, Aetosauria) from the Upper Triassic Pekin Formation, Deep River Basin, North Carolina. Journal of Paleontology 91:162–178.Google Scholar
Iordansky, N. N. 1973. The skull of the Crocodilia. Pp. 201–262 in Gans, C., ed. Biology of the Reptilia. Academic, London.Google Scholar
Irmis, R. B., Nesbitt, S. J., and Sues, H. D.. 2013. Early Crocodylomorpha. Geological Society of London Special Publication 379:275–302.Google Scholar
Jackson, D. C. 2000. Living without oxygen: lessons from the freshwater turtle. Comparative Biochemistry and Physiology Part A 125:299–315.Google Scholar
Jackson, D. C., and Heisler, N.. 1982. Plasma ion balance in submerged anoxic turtles at 3°C: the role of calcium lactate formation. Respiration Physiology 49:159–174.Google Scholar
Jackson, D. C., Goldberger, Z., Visuri, S., and Armstrong, R. N.. 1999. Ionic exchanges of turtle shell in vitro and their relevance to shell function in the anoxic turtle. Journal of Experimental Biology 202:503–520.Google Scholar
Jackson, D. C., Crocker, C. E., and Ultsch, G. R.. 2000a. Bone and shell contribution to lactic acid buffering of submerged turtles Chrysemys picta bellii at 3°C. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 278:R1964–1571.Google Scholar
Jackson, D. C., Ramsey, A. L., Paulson, J. M., Crocker, C. E., and Ultsch, G. R.. 2000b. Lactic acid buffering by bone and shell in anoxic softshell and painted turtles. Physiological and Biochemical Zoology 73:290–297.Google Scholar
Jackson, D. C., Andrade, D., and Abe, A. S.. 2003. Lactate sequestration by osteoderms of the broadnose caiman, Caiman latirostris, following capture and forced submergence. Journal of Experimental Biology 206:3601–3606.Google Scholar
Kälin, J., 1955. Crocodilia. In Piveteau, J., ed. Traité de Paléontologie 5:695–784. Masson et Cie, Paris.Google Scholar
Kot, B. C. W., Zhang, Z. J., Lee, A. W. C., Leung, V. Y. F., and Fu, S. N.. 2012. Elastic modulus of muscle and tendon with shear wave ultrasound elastography: variations with different technical settings. PLoS ONE 7(8):e44348. doi: 10.1371/journal.pone.0044348.Google Scholar
Legendre, L., Guénard, G., Botha-Brink, J., and Cubo, J.. 2016. Palaeohistological evidence for ancestral high metabolic rate in archosaurs. Systematic Biology 65:989–996.Google Scholar
Linnaeus, Cv. 1758. Amphibia Lacerta. In Systema naturae. Tome 1:1057–1058.Google Scholar
Long, R. A., and Ballew, K. L.. 1985. Aetosaur dermal armor from the Late Triassic of southwestern North America, with special reference to material from the Chinle Formation of Petrified Forest National Park. In Colbert, E. H. and Johnson, R. R., eds. The petrified forest through the ages. Museum of Northern Arizona Bulletin 54:45–68. Flagstaff, Ariz.Google Scholar
Main, R. P., Ricqlès, Ade., Horner, J. R., and Padian, K.. 2005. The evolution and function of thyreophoran dinosaur scutes: implications for plate function in stegosaurs. Paleobiology 31:291–314.Google Scholar
McKee, C. T., Last, J. A., Russell, P., and Murphy, C. J.. 2011. Indentation versus tensile measurements of Young's modulus for soft biological tissues. Tissue Engineering Part B 17:155–164.Google Scholar
Mises, R. von. 1913. Mechanik der festen Körper im plastisch deformablen Zustand. Göttingen Mathematisch-Physikalische Klasse 1:582–592.Google Scholar
Nesbitt, S. J. 2011. The early evolution of archosaurs: relationships and the origin of major clades. Bulletin of the American Museum National History 352:1–292.Google Scholar
Nesbitt, S. J., Desojo, J. B., and Irmis, R. B.. 2013. Anatomy, phylogeny and palaeobiology of early archosaurs and their kin. Geological Society of London Special Publication 379:1–7.Google Scholar
Owen, R. 1849. Notes on remains of fossil reptiles discovered by Prof. Henry Rogers of Pennsylvania, U. S., in Greensand formation of New Jersey. Quarterly Journal of the Geological Society of London 5:380–383.Google Scholar
Parrish, J. M. 1994. Cranial osteology of Longosuchus meadei and the phylogeny and distribution of the Aetosauria. Journal of Vertebrate Paleontology 14:196–209.Google Scholar
Pithioux, M., Lasaygues, P., and Chabrand, P.. 2002. An alternative ultrasonic method for measuring the elastic properties of cortical bone. Journal of Biomechanics 35:961–968.Google Scholar
Ross, F. D., and Mayer, G. C.. 1983. On the dorsal armor of the Crocodilia. Pp. 305–331 in Rhodin, A. G. J., ed. Advances in herpetology and evolutionary biology. Museum of Comparative Zoology. Cambridge, Mass.Google Scholar
Rinehart, L. F., and Lucas, S. G.. 2013. The functional morphology of dermal bone ornamentation in temnospondyl amphibians. In Tanner, L. H., Spielmann, J. A., and Lucas, S. G., eds. The Triassic System 61:524–532. New Mexico Museum of Natural History and Science, Albuquerque, N.M.Google Scholar
Scheyer, T. M., and Desojo, J. B.. 2011. Palaeohistology and external microanatomy of rauisuchian osteoderms (Archosauria: Pseudosuchia). Palaeontology 54:1289–1302.Google Scholar
Scheyer, T. M., and Sander, P. M.. 2004. Histology of ankylosaur osteoderms: implications for systematics and function. Journal of Vertebrate Paleontology 24:874–893.Google Scholar
Scheyer, T. M., Sander, M. P., Joyce, W. G., Böhme, W., and Witzel, U.. 2007. A plywood structure in the shell of fossil and living soft-shelled turtles (Trionychidae) and its evolutionary implications. Organism Diversity and Evolution 7:136–144.Google Scholar
Scheyer, T. M., Mörs, T., and Einarsson., E. 2012. First record of softshelled turtles (Cryptodira, Tryonychidae) from the Late Cretaceous of Europe. Journal of Vertebrate Paleontology 32:1027–1032.Google Scholar
Scheyer, T. M., Desojo, J. B., and Cerda, I. A.. 2014. Bone histology of phytosaur, aetosaur, and other archosauriform osteoderms (Eureptilia, Archosauromorpha). Anatomical Record 297:240–260.Google Scholar
Schoch, R. R., and Desojo, J. B.. 2016. Cranial anatomy of the aetosaur Paratypothorax andressorum from the Upper Triassic of Germany and its bearing on aetosaur phylogeny. Neues Jahrbuch für Geologie und Paläontologie 279:73–95.Google Scholar
Seidel, M. R. 1979. The osteoderms of the American alligator and their functional significance. Herpetologica 35:375–380.Google Scholar
Sereno, P. C., Larsson, H. C., Sidor, C. A., and Gado, B.. 2001. The giant crocodyliform Sarcosuchus from the Cretaceous of Africa. Science 294:1516–1519.Google Scholar
Small, B. J. 2002. Cranial anatomy of Desmatosuchus haplocerus (Reptilia: Archosauria: Stagonolepididae). Zoological Journal of the Linnean Society 136:97–111.Google Scholar
Staton, M. A., and Dixon, J. R.. 1975. Studies on dry season biology of Caiman crocodilus crocodiles from the Venezuela Llanos. Memoria de la Sociedad de Ciencias Naturales La Salle 101:237–265.Google Scholar
Stocker, M. R., and Butler, R. J.. 2013. Phytosauria. In Nesbitt, S. J., Desojo, J. B., and Irmis, R. B., eds. Anatomy, phylogeny and palaeobiology of early archosaurs and their kin. Geological Society Special Publication 379:91.Google Scholar
Sun, C. Y., and Chen, P. Y.. 2013. Structural design and mechanical behavior of alligator (Alligator mississippiensis) osteoderms. Acta Biomaterialia 9:9049–9064.Google Scholar
Trutnau, L., and Sommerlad, R.. 2006. Crocodilians their natural history and captive husbandry. Edition Chimaira, Frankfurt am Main, Germany.Google Scholar
Vickaryous, M. K., and Hall, B. K.. 2006. Osteoderm morphology and development in the nine-banded armadillo, Dasypus novemcinctus (Mammalia, Xenarthra, Cingulata). Journal of Morphology 267:1273–1283.Google Scholar
Vickaryous, M. K., and Hall, B. K.. 2008. Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms. Journal of Morphology 269:398–422.Google Scholar
Vickaryous, M. K., and Sire, J. Y.. 2009. The integumentary skeleton of tetrapods: origin, evolution and development. Journal of Anatomy 214:441–464.Google Scholar
Walker, A. D. 1961. Triassic reptiles from the Elgin area: Stagonolepis, Dasygnathus and their allies. Philosophical Transactions of the Royal Society of London B 244:103–204.Google Scholar
Witzmann, F. 2009. Comparative histology of sculptured dermal bones in basal tetrapods, and the implications for the soft tissue dermis. Palaeodiversity 2:233–270.Google Scholar
Wolf, D., Kalthof, D. C., and Sander, P. M.. 2012. Osteoderm histology of the Pampatheriidae (Cingulata, Xenarthra, Mammalia): implications for systematics, osteoderm growth, and biomechanical adaptation. Journal of Morphology 273:388–404.Google Scholar
Yang, W., Chen, I. H., Gludovatz, B., Zimmermann, E. A., Ritchie, R. O., and Meyers, M. A.. 2013a. Natural flexible dermal armor. Advanced Material 25:31–48.Google Scholar
Yang, W., Gludovatz, B., Zimmermann, E. A., Bale, H. A., Ritchie, R. O., and Meyers, M. A.. 2013b. Structure and fracture resistance of alligator gar (Atractosteus spatula) armored fish scales. Acta Biomaterialia 9:5876–5889.Google Scholar
Zylberberg, L., and Castanet, J.. 1985. New data on the structure and the growth of the osteoderms in the reptile Anguis fragilis (Anguidae, Squamata). Journal of Morphology 186:327–342.Google Scholar