Skip to main content

Advertisement

SpringerLink
Collagen Fibers in Crocodile Skin and Teeth: A Morphological Comparison Using Light and Scanning Electron Microscopy
Download PDF
Download PDF
  • Open Access
  • Published: 07 July 2020

Collagen Fibers in Crocodile Skin and Teeth: A Morphological Comparison Using Light and Scanning Electron Microscopy

  • Piotr Krzysztof Szewczyk1 &
  • Urszula Stachewicz1 

Journal of Bionic Engineering volume 17, pages 669–676 (2020)Cite this article

  • 753 Accesses

  • 6 Citations

  • Metrics details

Abstract

Collagen is one of the most versatile tissues of living organisms that comes in many shapes and sizes, providing functions ranging from tissue matrix through, ligament formation up to enabling mineralization in teeth. The detailed light microscopy and Scanning Electron Microscopy (SEM) observations conducted in this study, allowed us to investigate morphology, sizes and crimp patterns of collagen fibers observed in crocodile skin and teeth. Moreover, the microscopy study revealed that although two completely different tissues were investigated, many similarities in their structure based on collagen fibers were observed. Collagen type I is present in crocodile skin and teeth, showing the flexibility in naturally constructed tissues to obtain various functions. The crimp size investigation of collagen fibers confirmed experimentally the theoretical 67 nm D-periodicity expected for collagen type I. The collagen in teeth provides a matrix for crystal growth and in the skin provides flexibility and is a precursor for corneous scales. Importantly, these observations of the collagen in the skin and tooth structure in crocodiles play an important role in designing biomimetic materials with similar functions and properties.

Download to read the full article text

Working on a manuscript?

Avoid the most common mistakes and prepare your manuscript for journal editors.

Learn more

References

  1. Metwally S, Martínez Comesaña S, Zarzyka M, Szewczyk P K, Karbowniczek J E, Stachewicz U. Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair. Acta Biomaterialia, 2019, 91, 270–283.

    Google Scholar 

  2. Römer L, Scheibel T. The elaborate structure of spider silk: Structure and function of a natural high performance fiber. Prion, 2008, 2, 154–161.

    Google Scholar 

  3. Szewczyk P K, Knapczyk-Korczak J, Ura D P, Metwally S, Gruszczyński A, Stachewicz U. Biomimicking wetting properties of spider web from Linothele megatheloides with electrospun fibers. Materials Letters, 2018, 233, 211–214.

    Google Scholar 

  4. Kadler K E, Holmes D F, Trotter J A, Chapman J A. Collagen fibril formation. Biochemical Journal, 1996, 316, 1–11.

    Google Scholar 

  5. Canty E G, Kadler K E. Procollagen trafficking, processing and fibrillogenesis. Journal of Cell Science, 2005, 118, 1341–1353.

    Google Scholar 

  6. Fratzl P, Misof K, Zizak I, Rapp G. Amenitsch H, Bernstorff S. Fibrillar structure and mechanical properties of collagen. Journal of Structural Biology, 1998, 122, 119–122.

    Google Scholar 

  7. Chintapalli R K, Mirkhalaf M, Dastjerdi A K, Barthelat F. Fabrication, testing and modeling of a new flexible armor inspired from natural fish scales and osteoderms. Bioinspiration & Biomimetics, 2014, 9, 036005.

    Google Scholar 

  8. Bernth J E, Ho V A, Liu H B. Morphological computation in haptic sensation and interaction: From nature to robotics. Advanced Robotics, 2018, 32, 340–362.

    Google Scholar 

  9. Kanhere E, Wang N, Kottapalli A G P, Asadnia M. Subramaniam V. Miao J, Triantafyllou M. Crocodile-inspired dome-shaped pressure receptors for passive hydrodynamic sensing. Bioinspiration & Biomimetics, 2016, 11, 056007.

    Google Scholar 

  10. Elkan E, Cooper J E. Skin biology of reptiles and amphibians. Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences, 1980, 79, 115–126.

    Google Scholar 

  11. Dubansky B H, Close M. A review of alligator and snake skin morphology and histotechnical preparations. Journal of Histotechnology, 2019, 42, 31–51.

    Google Scholar 

  12. Lin C P, Douglas W H, Erlandsen S L. Scanning electron microscopy of type I collagen at the dentin-enamel junction of human teeth. Journal of Histochemistry & Cytochemistry, 1993, 41, 381–388.

    Google Scholar 

  13. Erickson G M, Brochu C A. How the ‘terror crocodile’ grew so big. Nature, 1999, 398, 205–206.

    Google Scholar 

  14. Sennikov A G. The first ctenosauriscid (Reptilia: Archosauromorpha) from the lower triassic of eastern europe. Paleontological Journal, 2012, 46, 499–511.

    Google Scholar 

  15. Drymala S M, Zanno L E. Osteology of carnufex carolinensis (archosauria: psuedosuchia) from the pekin formation of north carolina and its implications for early crocodylomorph evolution. PLOS ONE, 2016, 11, e0157528.

    Google Scholar 

  16. Webb G J W, Manolis S C, Brien M L. Crocodiles: Status Survey and Conservation Action Plan, 3rd ed, Crocodile Specialist Group: Darwin, Darwin, Australia, 2010.

    Google Scholar 

  17. Alibardi L. Keratinization in crocodilian scales and avian epidermis: Evolutionary implications for the region of avian apteric epidermis. Belgian Journal of Zoology, 2005, 135, 9–20.

    Google Scholar 

  18. Alibardi L. Histology, ultrastructure, and pigmentation in the horny scales of growing crocodilians. Acta Zoologica, 2011, 92, 187–200.

    Google Scholar 

  19. Holthaus K B, Strasser B, Lachner J, Sukseree S, Sipos W, Weissenbacher A, Tschachler E, Alibardi L, Eckhart L. Comparative analysis of epidermal differentiation genes of crocodilians suggests new models for the evolutionary origin of avian feather proteins. Genome Biology and Evolution, 2018, 10, 694–704.

    Google Scholar 

  20. Pressinotti L N, Borges R M, Alves De Lima A P, Aleixo V M, Iunes R S, Borges J C S, Cogliati B, Cunha Da Silva J R M. Low temperatures reduce skin healing in the Jacare do Pantanal (Caiman yacare, Daudin 1802). Biology Open, 2013, 2, 1171–1178.

    Google Scholar 

  21. Dalla Valle L, Nardi A, Gelmi C, Toni M, Emera D, Alibardi L. β-keratins of the crocodilian epidermis: Composition, structure, and phylogenetic relationships. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2009, 312B, 42–57.

    Google Scholar 

  22. Alibardi L, Toni M. Cytochemical, biochemical and molecular aspects of the process of keratinization in the epidermis of reptilian scales. Progress in Histochemistry and Cytochemistry, 2006, 40, 73–134.

    Google Scholar 

  23. Alibardi L, Thompson M B. Keratinization and ultrastructure of the epidermis of late embryonic stages in the alligator (Alligator mississippiensis). Journal of Anatomy, 2002, 201, 71–84.

    Google Scholar 

  24. Alibardi L. Adaptation to the land: The skin of reptiles in comparison to that of amphibians and endotherm amniotes. Journal of Experimental Zoology, 2003, 298B, 12–41.

    Google Scholar 

  25. Baden H P, Maderson P F. Morphological and biophysical identification of fibrous proteins in the amniote epidermis. Journal of Experimental Zoology, 1970, 174, 225–232.

    Google Scholar 

  26. Alibardi L. Sauropsids cornification is based on corneous beta-proteins, a special type of keratin-associated corneous proteins of the epidermis. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2016, 326, 338–351.

    Google Scholar 

  27. Holthaus K B, Eckhart L, Dalla Valle L, Alibardi L. Review: Evolution and diversification of corneous beta-proteins, the characteristic epidermal proteins of reptiles and birds. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2019, 330, 438–453.

    Google Scholar 

  28. Berthod F, Germain L, Li H, Xu W, Damour O, Auger F A. Collagen fibril network and elastic system remodeling in a reconstructed skin transplanted on nude mice. Matrix Biology, 2001, 20, 463–473.

    Google Scholar 

  29. Matoltsy A G, Huszar T. Keratinization of the reptilian epidermis: An ultrastructural study of the turtle skin. Journal of Ultrastructure Research, 1972, 38, 87–101.

    Google Scholar 

  30. Cheema U, Ananta M, Muder V. Collagen: Applications of a natural polymer in regenerative medicine regenerative medicine and tissue engineering, in: Cells and Biomaterials, InTech, London, UK, 2011, 13, 287–300.

    Google Scholar 

  31. Enax J, Fabritius H O, Rack A, Prymak O, Raabe D, Epple M. Characterization of crocodile teeth: Correlation of composition, microstructure, and hardness. Journal of Structural Biology, 2013, 184, 155–163.

    Google Scholar 

  32. Weiner S, Wagner H D. The material bone: Structure-mechanical function relations. Annual Review of Materials Science, 1998, 28, 271–298.

    Google Scholar 

  33. Gupta H S, Stachewicz U, Wagermaier W, Roschger P, Wagner H D, Fratzl P. Mechanical modulation at the lamellar level in osteonal bone. Journal of Materials Research, 2006, 21, 1913–1921.

    Google Scholar 

  34. Datta P, Vyas V, Dhara S, Chowdhury A R, Barui, A. Anisotropy properties of tissues: A basis for fabrication of biomimetic anisotropic scaffolds for tissue engineering. Journal of Bionic Engineering, 2019, 16, 842–868.

    Google Scholar 

  35. De Leeuw N H, Rabone J A L. Molecular dynamics simulations of the interaction of citric acid with the hydroxyapatite (0001) and (0110) surfaces in an aqueous environment. CrystEngComm, 2007, 9, 1178–1186.

    Google Scholar 

  36. Boskey A L. Mineralization of bones and teeth. Elements, 2007, 3, 385–391.

    Google Scholar 

  37. Erickson G M, Gignac P M, Steppan S J, Lappin A K, Vliet K A, Brueggen J D, Inouye B D, Kledzik D, Webb G J W. Insights into the ecology and evolutionary success of crocodilians revealed through bite-force and tooth-pressure experimentation. PLOS ONE, 2012, 7, e31781.

    Google Scholar 

  38. He G, George A. Dentin matrix protein 1 immobilized on type I collagen fibrils facilitates apatite deposition in vitro. Journal of Biological Chemistry, 2004, 279, 11649–11656.

    Google Scholar 

  39. Lodish H F, Berk A, Zipursky S L, Matsudaira P, Baltimore D, Darnell J. Molecular Cell Biology. W. H. Freeman, New York, USA, 2000, 1084.

    Google Scholar 

  40. Parry D A D, Barnes G R G, Craig A S. A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proceedings of the Royal Society of London, Series B, Biological Sciences, 1978, 203, 305–321.

    Google Scholar 

  41. Franchi M, Raspanti M, Dell’Orbo C, Quaranta M, De Pasquale V, Ottani V, Ruggeri A. Different crimp patterns in collagen fibrils relate to the subfibrillar arrangement. Connective Tissue Research, 2008, 49, 85–91.

    Google Scholar 

  42. Franchi M, Fini M, Quaranta M, De Pasquale V, Raspanti M, Giavaresi G, Ottani V, Ruggeri A. Crimp morphology in relaxed and stretched rat Achilles tendon. Journal of Anatomy, 2007, 210, 1–7.

    Google Scholar 

  43. Raspanti M, Manelli A, Franchi M, Ruggeri A. The 3D structure of crimps in the rat Achilles tendon. Matrix Biology, 2005, 24, 503–507.

    Google Scholar 

Download references

Acknowledgment

The authors thank Adam Hryniewicz from Warsaw Zoo for crocodile skin and teeth samples used in this study. This study was conducted as part of the “Nanofiber-based sponges for atopic skin treatment” project, which is carried out within the First TEAM programme of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund, Project No. POIR. 04.04.00-00-4571/18-00. This study was supported by the infrastructure at the International Centre of Electron Microscopy for Materials Science (IC-EM) at AGH University of Science and Technology.

Author information

Authors and Affiliations

  1. Metals Engineering and Industrial Computer Science and International Centre of Electron Microscopy for Materials Science, AGH University of Science and Technology, Kraków, 30-059, Al. Mickiewicza 30, Poland

    Piotr Krzysztof Szewczyk & Urszula Stachewicz

Authors
  1. Piotr Krzysztof Szewczyk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Urszula Stachewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Urszula Stachewicz.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.

The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Szewczyk, P.K., Stachewicz, U. Collagen Fibers in Crocodile Skin and Teeth: A Morphological Comparison Using Light and Scanning Electron Microscopy. J Bionic Eng 17, 669–676 (2020). https://doi.org/10.1007/s42235-020-0059-7

Download citation

  • Published: 07 July 2020

  • Issue Date: July 2020

  • DOI: https://doi.org/10.1007/s42235-020-0059-7

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

Keywords

  • crocodile skin
  • collagen
  • crimp
  • fiber
  • crocodile tooth
  • SEM
Download PDF

Working on a manuscript?

Avoid the most common mistakes and prepare your manuscript for journal editors.

Learn more

Advertisement

Over 10 million scientific documents at your fingertips

Switch Edition
  • Academic Edition
  • Corporate Edition
  • Home
  • Impressum
  • Legal information
  • Privacy statement
  • California Privacy Statement
  • How we use cookies
  • Manage cookies/Do not sell my data
  • Accessibility
  • FAQ
  • Contact us
  • Affiliate program

Not affiliated

Springer Nature

© 2023 Springer Nature Switzerland AG. Part of Springer Nature.