Abstract
This investigation reports mechanical properties of the exoskeleton of deep sea shrimp, Rimicaris exoculata, at temperatures ranging from 25 to 80 °C measured using nanoindentation experiments. The measured properties are compared with the corresponding shallow water shrimp (Pandalus platyceros) exoskeleton properties. Scanning electron microscopy suggests that both types of shrimp exoskeletons have the twisted plywood, Bouligand structure. However, they differ in the volume fraction and distribution of mineral content. The variations in the nanoindentation measured hardness values of the examined shrimp exoskeletons are found to be strongly correlated with the corresponding compositional difference between the two exoskeleton types. Nanoindentation creep strain rate measurements are performed to provide an assessment of the two types of exoskeleton for the role of proteins and minerals to cause difference in behavior and properties between the two shrimp species. The measured creep load–depth data are fitted with a viscoelastic creep function to find the creep compliance as a function of experimentally varying temperature and in the context of natural variations in mineral content.
Similar content being viewed by others
References
G. Mayer: New classes of tough composite materials—Lessons from natural rigid biological systems. Mater. Sci. Eng., C 26(8), 1261 (2006).
G. Mayer: New toughening concepts for ceramic composites from rigid natural materials. J. Mech. Behav. Biomed. Mater. 4(5), 670 (2011).
B. Chen, X. Peng, J.G. Wang, and X. Wu: Laminated microstructure of Bivalva shell and research of biomimetic ceramic/polymer composite. Ceram. Int. 30(7), 2011 (2004).
H.R. Hepburn, I. Joffe, N. Green, and K.J. Nelson: Mechanical properties of a crab shell. Comp. Biochem. Physiol., Part A: Physiol. 50(3), 551 (1975).
F. Barthelat, J.E. Rim, and H.D. Espinosa: A Review on the Structure and Mechanical Properties of Mollusk Shells–Perspectives on Synthetic Biomimetic Materials. In Applied Scanning Probe Methods XIII. B. Bhushan, H. Fuchs, eds. (Springer, Berlin Heidelberg, 2009); 17–44.
F. Boßelmann, P. Romano, H. Fabritius, D. Raabe, and M. Epple: The composition of the exoskeleton of two crustacea: The American lobster Homarus americanus and the edible crab Cancer pagurus. Thermochim. Acta 463(1–2), 65 (2007).
D. Raabe, P. Romano, C. Sachs, H. Fabritius, A. Al-Sawalmih, S-B. Yi, G. Servos, and H. Hartwig: Microstructure and crystallographic texture of the chitin–protein network in the biological composite material of the exoskeleton of the lobster Homarus americanus. Mater. Sci. Eng., A 421(1), 143 (2006).
D. Raabe, C. Sachs, and P. Romano: The crustacean exoskeleton as an example of a structurally and mechanically graded biological nanocomposite material. Acta Mater. 53(15), 4281 (2005).
Y. Bouligand: Twisted fibrous arrangements in biological materials and cholesteric mesophases. Tissue Cell 4(2), 189 (1972).
M.M. Giraud-Guille: Fine structure of the chitin-protein system in the crab cuticle. Tissue Cell 16(1), 75 (1984).
P-Y. Chen, A.Y.M. Lin, J. McKittrick, and M.A. Meyers: Structure and mechanical properties of crab exoskeletons. Acta Biomater. 4(3), 587 (2008).
Y. Seki, B. Kad, D. Benson, and M.A. Meyers: The toucan beak: Structure and mechanical response. Mater. Sci. Eng., C 26(8), 1412 (2006).
Y. Seki, M.S. Schneider, and M.A. Meyers: Structure and mechanical behavior of a toucan beak. Acta Mater. 53(20), 5281 (2005).
J. Lian and J. Wang: Microstructure and mechanical properties of Dungeness crab exoskeletons. In Mechanics of Biological Systems and Materials, Vol. 2, T. Proulx ed.; Springer: New York, 2011; pp. 93.
C.A. Melnick, Z. Chen, and J.J. Mecholsky: Hardness and toughness of exoskeleton material in the stone crab, Menippe mercenaria. J. Mater. Res. 11(11), 2903 (1996).
H. Fricke, O. Giere, K. Stetter, G.A. Alfredsson, J.K. Kristjansson, P. Stoffers, and J. Svavarsson: Hydrothermal vent communities at the shallow subpolar Mid-Atlantic ridge. Mar. Biol. 102(3), 425 (1989).
D. Desbruyères, M. Biscoito, J.C. Caprais, A. Colaço, T. Comtet, P. Crassous, Y. Fouquet, A. Khripounoff, N. Le Bris, K. Olu, R. Riso, P.M. Sarradin, M. Segonzac, and A. Vangriesheim: Variations in deep-sea hydrothermal vent communities on the Mid-Atlantic Ridge near the Azores plateau. Deep Sea Res., Part I 48(5), 1325 (2001).
S.T. Ahyong: New species and new records of hydrothermal vent shrimps from New Zealand (Caridea: Alvinocarididae, Hippolytidae). Crustaceana 82(7), 775 (2009).
R.C. Vrijenhoek: Genetic diversity and connectivity of deep-sea hydrothermal vent metapopulations. Mol. Ecol. 19(20), 4391 (2010).
D.P. Connelly, J.T. Copley, B.J. Murton, K. Stansfield, P.A. Tyler, C.R. German, C.L. Van Dover, D. Amon, M. Furlong, N. Grindlay, N. Hayman, V. Huhnerbach, M. Judge, T. Le Bas, S. McPhail, A. Meier, K-i. Nakamura, V. Nye, M. Pebody, R.B. Pedersen, S. Plouviez, C. Sands, R.C. Searle, P. Stevenson, S. Taws, and S. Wilcox: Hydrothermal vent fields and chemosynthetic biota on the world’s deepest seafloor spreading centre. Nat. Commun. 3, 620 (2012).
A. Clarke and K.P.P. Fraser: Why does metabolism scale with temperature?Funct. Ecol. 18(2), 243 (2004).
F. Smith, A. Brown, N.C. Mestre, A.J. Reed, and S. Thatje: Thermal adaptations in deep-sea hydrothermal vent and shallow-water shrimp. Deep Sea Res., Part II 92, 234 (2013).
M. Spanopoulos-Hernández, C.A. Martínez-Palacios, R.C. Vanegas-Pérez, C. Rosas, and L.G. Ross: The combined effects of salinity and temperature on the oxygen consumption of juvenile shrimps Litopenaeus stylirostris (Stimpson, 1874). Aquaculture 244(1–4), 341 (2005).
E.L. Allan, P.W. Froneman, and A.N. Hodgson: Effects of temperature and salinity on the standard metabolic rate (SMR) of the caridean shrimp Palaemon peringueyi. J. Exp. Mar. Biol. Ecol. 337(1), 103 (2006).
S. Hourdez and F. Lallier: Adaptations to hypoxia in hydrothermal-vent and cold-seep invertebrates. Rev. Environ. Sci. Bio/Technol. 6(1–3), 143 (2007).
A. Oliphant, S. Thatje, A. Brown, M. Morini, J. Ravaux, and B. Shillito: Pressure tolerance of the shallow-water caridean shrimp Palaemonetes varians across its thermal tolerance window. J. Exp. Biol. 214(7), 1109 (2011).
S. Ravichandran, G. Rameshkumar, and A.R. Prince: Biochemical composition of shell and flesh of the Indian white shrimp Penaeus indicus (H. milne Edwards 1837). Am.-Eurasian J. Sci. Res. 4(3), 191 (2009).
F. Ehigiator and E. Oterai: Chemical composition and amino acid profile of a caridean prawn (Macrobrachium vollenhovenii) from Ovia river and tropical periwinkle (Tympanotonus fuscatus) from Benin river, Edo state, Nigeria. Int. J. Res. Rev. Appl. Sci. 11(1), (2012).
I.A. Emmanuel, H.O. Adubiaro, and O.J. Awodola: Comparability of chemical composition and functional properties of shell and flesh of Penaeus notabilis Pakistan. J. Nutr. 7(6), 741 (2008).
F. Shahidi and J. Synowiecki: Isolation and characterization of nutrients and value-added products from snow crab (Chionoecetes opilio) and shrimp (Pandalus borealis) processing discards. J. Agric. Food Chem. 39(8), 1527 (1991).
M. Islam, S. Masum, M. Rahman, M. Moll, A. Shaikh, and S. Roy: Preparation of chitosan from shrimp shell and investigation of its properties. Int. J. Basic Appl. Sci. 11(1), 116 (2011).
R.H. Rødde, A. Einbu, and K.M. Vårum: A seasonal study of the chemical composition and chitin quality of shrimp shells obtained from northern shrimp (Pandalus borealis). Carbohydr. Polym. 71(3), 388 (2008).
H.M. Ibrahim, M.F. Salama, and H.A. El-Banna: Shrimp’s waste: Chemical composition, nutritional value and utilization. Food/Nahrung 43(6), 418 (1999).
W.C. Oliver and G.M. Pharr: Improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7(6), 1564 (1992).
G. Pharr: Measurement of mechanical properties by ultra-low load indentation. Mater. Sci. Eng., A 253(1), 151 (1998).
M. Gan and V. Tomar: Scale and temperature dependent creep modeling and experiments in materials. JOM 63(9), 27 (2011).
M. Gan and V. Tomar: Role of length scale and temperature in indentation induced creep behavior of polymer derived Si-C-O ceramics. Mater. Sci. Eng., A 527, 7615 (2010).
D. Verma and V. Tomar: Structural-nanomechanical property correlation of shallow water shrimp (Pandalus platyceros) exoskeleton at elevated temperature. J. Bionic Eng. 11(3), 360 (2014).
D. Verma and V. Tomar: An investigation into environment dependent nanomechanical properties of shallow water shrimp (Pandalus platyceros) exoskeleton. Mater. Sci. Eng., C 44, 371 (2014).
D. Verma and V. Tomar: An investigation into mechanical strength of exoskeleton of hydrothermal vent shrimp (Rimicaris exoculata) and shallow water shrimp (Pandalus platyceros) at elevated temperatures. Mater. Sci. Eng., C 49, 243 (2015).
G. Feng and A. Ngan: Effects of creep and thermal drift on modulus measurement using depth-sensing indentation. J. Mater. Res. 17(3), 660 (2002).
R. Saha and W.D. Nix: Effects of the substrate on the determination of thin film mechanical properties by nanoindentation. Acta Mater. 50(1), 23 (2002).
C. Gamonpilas and E.P. Busso: On the effect of substrate properties on the indentation behaviour of coated systems. Mater. Sci. Eng., A 380(1–2), 52 (2004).
D. Kramer, A. Volinsky, N. Moody, and W. Gerberich: Substrate effects on indentation plastic zone development in thin soft films. J. Mater. Res. 16(11), 3150 (2001).
J. Koyanagi, S. Yoneyama, A. Nemoto, and J.D.D. Melo: Time and temperature dependence of carbon/epoxy interface strength. Compos. Sci. Technol. 70(9), 1395 (2010).
R.F. Tilton, Jr., J.C. Dewan, and G.A. Petsko: Effects of temperature on protein structure and dynamics: X-ray crystallographic studies of the protein ribonuclease-A at nine different temperatures from 98 to 320 K. Biochemistry 31(9), 2469 (1992).
H. Frauenfelder, G.A. Petsko, and D. Tsernoglou: Temperature-dependent x-ray diffraction as a probe of protein structural dynamics. Nature 280(5723), 558 (1979).
Y-T. Cheng, W. Ni, and C-M. Cheng: Determining the instantaneous modulus of viscoelastic solids using instrumented indentation measurements. J. Mater. Res. 20(11), 3061 (2005).
B. Tang and A. Ngan: Accurate measurement of tip–sample contact size during nanoindentation of viscoelastic materials. J. Mater. Res. 18(05), 1141 (2003).
A.H.W. Ngan, H.T. Wang, B. Tang, and K.Y. Sze: Correcting power-law viscoelastic effects in elastic modulus measurement using depth-sensing indentation. Int. J. Solids Struct. 42(5–6), 1831 (2005).
M. Oyen: Analytical techniques for indentation of viscoelastic materials. Philos. Mag. 86(33–35), 5625 (2006).
M.L. Oyen and R.F. Cook: Load–displacement behavior during sharp indentation of viscous–elastic–plastic materials. J. Mater. Res. 18(01), 139 (2003).
R.F. Cook and M.L. Oyen: Nanoindentation behavior and mechanical properties measurement of polymeric materials. Int. J. Mater. Res. 98(5), 370 (2007).
H. Lu, B. Wang, J. Ma, G. Huang, and H. Viswanathan: Measurement of creep compliance of solid polymers by nanoindentation. Mech. Time-Depend. Mater. 7(3–4), 189 (2003).
A. Shokuhfar, A. Zare-Shahabadi, A-A. Atai, S. Ebrahimi-Nejad, and M. Termeh: Predictive modeling of creep in polymer/layered silicate nanocomposites. Polym. Test. 31(2), 345 (2012).
A.K. Nikolaidis, D.S. Achilias, and G.P. Karayannidis: Effect of the type of organic modifier on the polymerization kinetics and the properties of poly(methyl methacrylate)/organomodified montmorillonite nanocomposites. Eur. Polym. J. 48(2), 240 (2012).
A. Leszczyńska, J. Njuguna, K. Pielichowski, and J.R. Banerjee: Polymer/montmorillonite nanocomposites with improved thermal properties: Part I. Factors influencing thermal stability and mechanisms of thermal stability improvement. Thermochim. Acta 453(2), 75 (2007).
ACKNOWLEDGMENTS
The authors express their sincere thanks to Dr. Juliette Ravaux, Université Pierre et Marie Curie for providing the samples of Rimicaris exoculata. Also, the authors would like to acknowledge the excellent technical assistance of Dr. Christopher J. Gilpin, Chia-Ping Huang, and Laurie Mueller with the scanning electron microscopy at Purdue University. Lastly, Devendra Verma would like to thank his colleagues Dr. Devendra Dubey, Dr. Ming Gan, Dr. You Sung Han, Dr. Hongsuk Lee, Tao Qu, and Yang Zhang for helpful discussions. This research was supported by US-NSF grant CMMI-1131112.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Verma, D., Tomar, V. A comparison of nanoindentation creep deformation characteristics of hydrothermal vent shrimp (Rimicaris exoculata) and shallow water shrimp (Pandalus platyceros) exoskeletons. Journal of Materials Research 30, 1110–1120 (2015). https://doi.org/10.1557/jmr.2015.69
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1557/jmr.2015.69