Full length articleNatural hydrogel in American lobster: A soft armor with high toughness and strength
Graphical abstract
Introduction
The exoskeleton of the Homarus americanus, known as American lobster [1], is composed of segments of hard cuticles connected by soft arthrodial membranes and acts as a barrier between the internal organs and the external environment. More importantly, it provides a protective armor against predatory attack, thus making the lobster one of the most successful species existing for more than 100 million years [1]. The hard cuticles are composed of twisted plywood and honeycomb-like structures, incorporating the biomineral nanoparticles for adequate hardness [2], [3], [4]. However, the soft membranes are quite different, as they have negligible amounts of calcification, a higher content of water and chitin, and different types of proteins than the cuticles [2], [5]. Interestingly, these soft membranes cover a large portion of the lobster body, such as the abdomen, which is often subjected to wear and tear forces in sandy and rocky environments where lobsters typically live; this suggests that such soft membranes have a high mechanical reliability to protect the lobster tissue. Nevertheless, unlike the hard cuticles, the structure and mechanical function of the soft lobster membranes remain largely unknown, which may contain critical information to design a fully flexible body armor as well as other functional soft materials.
Although ancient armors are designed to be stiff enough to resist deformation under external loading force, modern armors such as ballistic vest aim to stop and deform a bullet and spread its force over a larger portion of the vest [6], [7]. It is more crucial to maximize the energy absorption during the penetration process than to completely prevent the deformation. Moreover, hard armors sacrifice limb mobility, which we believe is crucial when lobsters fight with each other to claim territory. Thus, we are interested in studying the role of soft lobster membranes in protection and their capability of absorbing energy during the material fracture under loading.
Herein, we investigate the microstructure, mechanical properties, and failure behavior of the lobster membranes and present our work in the following logic. We prepare samples of lobster membrane, visualize their microstructures, and characterize their mechanical properties. We build a large-scale coarse-grained model of the lobster membrane by following the geometric features as obtained from experimental images and mechanical measurement for chitin fibers and the lobster membrane. We thereafter use the model to simulate the mechanics of the cracked membrane in loading and obtain membrane strength as a function of the crack depth. The experimental and modeling methods are summarized in session 2. In session 3, we summarize our key findings. Our results unravel that the lobster membranes are soft hydrogels containing 90% water; surprisingly, they exhibit extremely high toughness and tensile strength as well as a high tolerance to structural damages [8], [9], [10]. We find that these membranes are composed of highly ordered multi-layer structures at the microscopic level, which is common for mineralized natural materials [2], [6], [11], [12], [13], [14] but rare for hydrogels. Our simulation based on the coarse-grained model reveals that this unique ordered structure strongly connects to the nonlinear mechanical and failure behaviors, which together give rise to the high toughness and damage tolerance of the lobster membranes. In session 4, we provide our main conclusion of the work.
Section snippets
Experimental preparation of lobster membranes
Joint and abdomen membranes are obtained from fresh American lobsters from Boston local fish markets. After carefully removing other attached tissues, the intact membranes are immersed in saline water with compositions similar to those of seawater (Na+ 0.469 mol/kg, Mg2+ 0.053 mol/kg, and Ca2+ 0.010 mol/kg) for 1 h. Rectangular samples of width 2–5 mm, thickness 0.3–0.5 mm, and length 10–20 mm are cut from the membranes using a pair of sharp scissors for mechanical measurements. Mechanical
Results and discussion
To investigate the chemical and mechanical properties of the lobster membranes, experimental samples of these membranes are collected from natural lobsters obtained at Boston local fish markets. Membranes at both the abdomen and the joint of lobsters are investigated in our study. These membranes are connected seamlessly to rigid cuticles (Fig. 2a) and play critical roles in the mobility of lobsters. Interestingly, after removing other tissues that connect these membranes, they appear to be
Conclusions
In summary, we show that the soft membranes from American lobster are natural hydrogels composed of 90% water and a small amount of chitin–protein fibers. These hydrogel membranes have remarkably high strength and toughness, which are comparable to those of natural rubber and carbon–rubber composites, and moreover, they are damage tolerant. By combining experiments and simulations, we demonstrate that the exceptional mechanical performance of the lobster membranes highly relies on their unique
Conflict of interest
The authors declare no conflict of interest.
Acknowledgment
We thank Hengyi Li for helping in experiments on rubber composites and also Xuanhe Zhao, Hyunwoo Yuk, and Jiliang Hu for their valuable discussions. M.G. acknowledges the support from the Department of Mechanical Engineering at MIT, and Z.Q. acknowledges NVIDIA for donating computing accelerators. This work is supported by the National Natural Science Foundation of China (Grant No.: 51673120 to J.W.) and State Key Laboratory of Polymer Materials Engineering (Grant No. sklpme2017-3-05 to J.W.).
Author contributions
J.W. proposed the study. J.W., M.G., and Z.Q. designed the research. J.W., M.G., and Z.Q. prepared the membrane sample. J.W., F.D., and M.G. performed and analyzed most of the mechanical tests. J.W., L.Q., H.Z., and M.G. performed structural characterizations. Z.Q. performed and analyzed the simulation. M.G. coordinated the study. J.W., Z.Q., and M.G. wrote the manuscript, and all authors revised and approved the manuscript.
References (37)
Characterization of proteins from arthrodial membranes of the lobster, Homarus americanus
Compar. Biochem. Physiol. a-Mol. Integrative Physiol.
(1998)- et al.
Protective role of Arapaima gigas fish scales: structure and mechanical behavior
Acta Biomater.
(2014) - et al.
The tensile properties of alginate hydrogels
Biomaterials
(2004) - et al.
Multifunctional properties of graphene/rubber nanocomposites fabricated by a modified latex compounding method
Compos. Sci. Tech.
(2014) - et al.
Transparent, elastomeric and tough hydrogels from poly(ethylene glycol) and silicate nanoparticles
Acta Biomaterialia
(2011) - et al.
Hoploparia albertaensis, a new species of clawed lobster (Nephropidae) from the late Coniacian, shallow-marine bad heart formation of northwestern Alberta, Canada
J. Paleontol.
(2005) - et al.
Chitin in the Exoskeletons of Arthropoda: From Ancient Design to Novel Materials Science
(2011) - et al.
Influence of Structural principles on the mechanics of a biological fiber-based composite material with hierarchical organization: the exoskeleton of the lobster Homarus americanus
Adv. Mater.
(2009) - et al.
Revealing the design principles of high-performance biological composites using ab initio and multiscale simulations: the example of lobster cuticle
Adv. Mater.
(2010) - et al.
The stomatopod dactyl club: a formidable damage-tolerant biological hammer
Science
(2012)
Protection mechanisms of the iron-plated armor of a deep-sea hydrothermal vent gastropod
P. Natl. Acad. Sci. USA
Flaw tolerance of nuclear intermediate filament lamina under extreme mechanical deformation
Acs Nano
On the tear resistance of skin
Nature Commun.
Stiff, strong, and tough hydrogels with good chemical stability
J. Mater. Chem. B
Materials become insensitive to flaws at nanoscale: lessons from nature
P. Natl. Acad. Sci. USA
Nanotwin-governed toughening mechanism in hierarchically structured biological materials
Nature Commun.
Thickness of hydroxyapatite nanocrystal controls mechanical properties of the collagen-hydroxyapatite interface
Langmuir
Elastic modulus of the crystalline regions of chitin and chitosan
J. Polym. Sci. Part B-Polym. Phys.
Cited by (44)
Mechanical design principles of avian eggshells for survivability
2024, Acta BiomaterialiaAll-cellulose hydrogel with ultrahigh stretchability exceeding 40000%
2024, Materials TodayAnti-impact performance of bionic tortoiseshell-like composites
2023, Composite Structures