Elsevier

Acta Biomaterialia

Volume 88, 1 April 2019, Pages 102-110
Acta Biomaterialia

Full length article
Natural hydrogel in American lobster: A soft armor with high toughness and strength

https://doi.org/10.1016/j.actbio.2019.01.067Get rights and content

Abstract

Homarus americanus, known as American lobster, is fully covered by its exoskeleton composed of rigid cuticles and soft membranes. These soft membranes are mainly located at the joints and abdomen to connect the rigid cuticles and greatly contribute to the agility of the lobster in swimming and preying. Herein, we show that the soft membrane from American lobster is a natural hydrogel (90% water) with exceptionally high toughness (up to 24.98 MJ/m3) and strength (up to 23.36 MPa), and is very insensitive to cracks. By combining experimental measurements and large-scale computational modeling, we demonstrate that the unique multilayered structure in this membrane, achieved through the ordered arrangement of chitin fibers, plays a crucial role in dissipating energy during rupture and making this membrane tough and damage tolerant. The knowledge learned from the soft membrane of natural lobsters sheds light on designing synthetic soft, yet strong and tough materials for reliable usage under extreme mechanical conditions, including a flexible armor that can provide full-body protection without sacrificing limb mobility.

Statement of significance

A body armor to provide protection to people who are at risk of being hurt is only enabled by using a material that is tough and strong enough to prevent mechanical penetration. However, most modern body armors sacrifice limb protection to gain mobility, simply because none of the existing armor materials are flexible enough and they all inhibit movement of the arms and legs. Herein, we focus on the mechanics and mesoscopic structure of American lobsters’ soft membrane and explore how such a natural flexible armor is designed to integrate flexibility and toughness. The knowledge learned from this study is useful to design a flexible armor for full-body protection under extreme mechanical conditions.

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.

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