A protocol for bioinspired design is described for a sampling device based on the jaws of a sea urchin. The bioinspiration process includes observing the sea urchins, characterizing the mouthpiece, 3D printing of the teeth and their assembly, and bioexploring the tooth structure.
Bioinspired design is an emerging field that takes inspiration from nature to develop high-performance materials and devices. The sea urchin mouthpiece, known as the Aristotle’s lantern, is a compelling source of bioinspiration with an intricate network of musculature and calcareous teeth that can scrape, cut, chew food and bore holes into rocky substrates. We describe the bioinspiration process as including animal observation, specimen characterization, device fabrication and mechanism bioexploration. The last step of bioexploration allows for a deeper understanding of the initial biology. The design architecture of the Aristotle’s lantern is analyzed with micro-computed tomography and individual teeth are examined with scanning electron microscopy to identify the microstructure. Bioinspired designs are fabricated with a 3D printer, assembled and tested to determine the most efficient lantern opening and closing mechanism. Teeth from the bioinspired lantern design are bioexplored via finite element analysis to explain from a mechanical perspective why keeled tooth structures evolved in the modern sea urchins we observed. This circular approach allows for new conclusions to be drawn from biology and nature.
The fields of biology, biological materials science, biomaterials, bioengineering and biochemistry employ the premiere scientific techniques and minds in an attempt to provide a deeper understanding of the incredible natural world. This research has explained many of the most amazing biological structures and organisms; from the intrinsic toughness of human bone1,2 to the large beak of the toucan3. However, much of this knowledge is difficult to employ in a manner that can provide a benefit to society. As a result, the tangential field of bioinspiration employs the lessons learned from nature to modern materials in order to solve common problems. Examples include superhydrophobic surfaces inspired by lotus leaves4-6, adhesive surfaces inspired by the feet of geckos and insects7,8, tough ceramics inspired by the nacre of abalone9-11 and biopsy harvesters inspired by the mouthpiece of the sea urchin, also known as the Aristotle's lantern12,13.
Sea urchins are invertebrate animals covered with spines whose habitat most commonly consists of the rocky beds on the ocean floor. The body (called a test) in the largest urchin species can be more than 18 cm in diameter; test size in pink sea urchins (Strongylocentrotus fragilis) examined in this study can grow to 10 cm diameter. The Aristotle's lantern is composed of five predominately calcium carbonate teeth supported by pyramid structures composed of mineralized tissue and arranged into a dome-like formation that enclose all but the distal grinding tips of the teeth (Figure 1A).
The muscle structure of the jaws is capable of efficient chewing and scraping even against hard ocean rocks and corals. When the jaws open, the teeth protrude outwards and when the jaws close, the teeth retract inwards in a single smooth motion. Comparison between primitive (above) and modern (below) sea urchin tooth cross-sections (Figure 1B) indicates that a keeled tooth evolved to strengthen the tooth when grinding against hard substrates. Each individual tooth has a slightly convex curvature and a T-shaped morphology in the transverse plane (normal to the growth direction) due to the longitudinally attached keel (Figure 1C, D).
Bioinspiration begins with observation of interesting natural phenomena, such as the efficient chewing motion of the Aristotle's lantern in sea urchins. This natural structure initially captivated Aristotle because it reminded him of a horn lantern with the panes of horn left out. More than two millennia later, Scarpa was fascinated by the complexity of the Aristotle's lantern that he and later Trogu mimicked the natural chewing motion using only paper and rubber bands (Figure 2A)15,16. Similarly, Jelinek was bioinspired by the chewing motion of the Aristotle's lantern and developed a better biopsy harvester that could safely isolate tumorous tissue without spreading cancerous cells (Figure 2B, C)12,13. In this case, bioinspired design was utilized to make a biomedical device that fit a specific need for a desired application.
The design protocol described here applies to a sediment sampler bioinspired by sea urchins. Through biological materials science, the natural structure of the Aristotle's lantern is characterized. Bioinspired design identifies potential applications where the natural mechanisms can be enhanced through the use of modern materials and fabrication techniques. The final design is re-examined through the prism of bioexploration to understand how the natural tooth structure evolved (Figure 3). The last bioexploration step, proposed by Porter17,18, uses engineering analysis methods to explore and explain biological phenomena. All the important steps of the bioinspiration process are presented as an example for harnessing technology, pre-approved by nature, which can be used for solving modern problems. Our protocol, motivated by previous bioinspiration procedures presented for specific applications by Arzt7, is targeted for biologists, engineers and anyone else who is inspired by nature.
1. Biological Materials Science
2. Bioinspired Design
3. Bioexploration
Bioinspired design of the Aristotle's lantern sampling device depends heavily upon the quality of the characterization methods used. Non-invasive techniques like µ-CT are helpful for analyzing the whole lantern and individual teeth to apply application specific enhancements for the bioinspired design (Figure 4). Meanwhile, the tooth microstructure can be explored via secondary electron and back-scattered electron micrographs of the polished cross-section of an individual tooth (Figure 5). The darker gray region is the harder stone part of the tooth grinding tip and consists of up to 40 mol % magnesium atoms that replace the calcium atoms.
Analysis of the tooth microstructure with BSE-SEM (Figure 5) confirmed the structural importance of the Mg-enriched stone part in the tooth grinding tip. Plate and fiber primary elements (calcite monocrystals, lighter gray in Figure 5C) are connected together by a matrix of secondary elements (calcite and magnesium carbonate polycrystals, darker gray in Figure 5C), that make up the hardest stone region of the tooth grinding tip.
The bioinspired lantern was designed with CAD software, 3D printed and assembled (Figure 6) for collection of sand at the beach (Figure 7). Stress analysis tests were used to calculate the von Mises stress of two tooth designs, one without the keel (Figure 8A) and the other with the keel (Figure 8B). A solid mesh composed of tetrahedrons was employed over the geometry of the tooth. The force value chosen (45 N) matched measurements from tests at the beach to penetrate 1 cm deep into hard sand with lantern teeth perpendicular to the surface.
The mass of the keeled tooth design (12.72 g) was compared with that of the non-keeled tooth design (12.26 g) to find a ~4% increase for the added keel. For 45 N applied force, the maximum stress experienced by the keeled tooth design (10.6 MPa) versus the non-keeled tooth design (12.6 MPa) was ~16% less for the keeled tooth (Figures 7A, B). The mass increase is small compared with the decrease in stress that the keel provides. The decrease in stress demonstrates the effectiveness of this bioinspired design for concentration of stress within the keeled region.
Figure 1. Sea urchin Aristotle's lantern and tooth morphology. (A) Close-up of the ventral view of a sea urchin (left) and the Aristotle's lantern (right)13. (B) Cross-sections of the grooved tooth of a primitive cidaroid urchin (top) and the keeled tooth of a modern camarodont urchin (bottom)14. (C) An isolated tooth seen from its side with the tip (bottom) and indicated keel (left side)20. (D) SEM image of a polished tooth cross-section with the indicated keel (bottom)20. Images adapted from indicated references for (A), (B), (C) and (D). Please click here to view a larger version of this figure.
Figure 2. Bioinspired designs based on the Aristotle's lantern. (A) Isometric view of a drawing for a bionic model of the Aristotle's lantern, which has 3D printed plastic parts connected by rubber bands (not shown) for the attached musculature16. (B, C) The Aristotle's lantern served as a biological inspiration for a biopsy harvester13. Please click here to view a larger version of this figure.
Figure 3. Four steps of the bioinspiration process. (clockwise from left) The bioinspiration process begins with learning from nature through observation of the pink sea urchin and the Aristotle's lantern. (top) Analysis of the sea urchin and the Aristotle's lantern structure from µ-CT scans (left). (right) Collected results are used to generate a bioinspired design prototype. (bottom) Engineering analysis methods were applied to explore biological phenomena and the bioinspired design17,18. Please click here to view a larger version of this figure.
Figure 4. Micro-computed tomography analysis of the Aristotle's lantern structure. (A) Side view of the pyramid structures that help to support the teeth. (B) Sea urchin teeth stack on top of each other and exhibit five-fold symmetry. (C) Distal tip portions are removed to show the longitudinally attached keel structures for all five teeth. (D) An individual tooth and keel (blue) with corresponding pyramid (yellow) are shown and also indicated in (C). Please click here to view a larger version of this figure.
Figure 5. Scanning electron microscopy (SEM) analysis of the sea urchin tooth microstructure. (A) SEM micrograph of a polished tooth cross-section with the faint stone stripe region and keel (bottom) indicated. (B, C) Backscattered electron SEM micrographs of the purple and orange boxes from (A) show curved plate and round fiber calcite primary elements situated above a denser Mg-enriched polycrystalline matrix (darker gray). Please click here to view a larger version of this figure.
Figure 6. Assembled 3D printed bioinspired Aristotle's lantern parts. (A) E-retaining rings and link rods are used to fasten the 3D printed tooth parts at three joint positions. (B) Assembled bioinspired Aristotle's lantern with one tooth removed. (C) View of the keel for individual teeth and the changing joint positions when the lantern is partially (left) and fully open (right). Please click here to view a larger version of this figure.
Figure 7. Bioinspired Aristotle's lantern design and usage at the beach. (A, B) Computer aided design images of the bioinspired Aristotle's lantern while closed and fully open, respectively. (C) The 3D printed bioinspired Aristotle's lantern collected different types of sand on the beach. Please click here to view a larger version of this figure.
Figure 8. Bioinspired sea urchin tooth stress analysis test. (A, B) Finite element analysis shows the non-keeled (A) versus keeled (B) tooth when force is applied at the tooth edges. The keeled tooth design experienced ~16% less stress due to addition of the keel. Please click here to view a larger version of this figure.
Sea urchins use the Aristotle's lantern (Figure 1A) for a variety of functions (feeding, boring, pivoting, etc.). The fossil record indicates that the lantern has evolved in shape and function from the most primitive cidaroid type to the camarodont type of modern sea urchins14. Cidaroid lanterns have longitudinally grooved teeth (Figure 1B, top) and non-separated muscle attachment to its pyramid structure. This limits their up and down movement and robs them of the greater scraping power generated by lateral movement, which is observed in the more modern camarodont lanterns (Figure 1B, bottom). Biologists have speculated that the keeled tooth (Figure 1C, D) evolved in camarodonts to reinforce the tooth under the strong tensile forces generated by scraping hard substrates18,20,23.
The bioinspired design protocol in this work combined biology, biological materials science, bioinspired design and bioexploration (Figure 3) to develop a bioinspired device with a specific function for sampling sediment. The µ-CT scan of the Aristotle's lantern (Figure 4) was imported as an STL file for reference only since the final sampler design did not mimic the complex muscle attachment in the natural structure. Instead the bioinspired design employed a simpler opening and closing mechanism with parts that could be manufactured easily by a 3D printer for assembly into the Aristotle's lantern sampler. Overall, we used a circular approach for bioinspired design since the bioexploration step allowed for new conclusions to be drawn from the natural biology. Potential modifications of the bioinspired design can address different applications besides sampling sediment. A limitation of this protocol is that it is focused on one specific application of the bioinspired process for a device based on the Aristotle's lantern. However, the protocol outlined here can be applied to the analysis, development and ultimate fabrication of other bioinspired designs based upon biological samples.
The primary application for this assembled bioinspired Aristotle's lantern sampler (Figure 6) was for collecting loose and compacted sand (Figure 7). Looking ahead, NASA has a plan to bring back Martian samples to Earth using a sample-return rover after a succession of missions over many years29. A sample-return rover outfitted with a bioinspired Aristotle's lantern sampler may be beneficial to future missions. A smaller sampler that resembles the size of a natural Aristotle's lantern may also be useful for other applications. The anisotropy of hardness in natural urchin teeth, while interesting in its own right, was not incorporated in this bioinspired design.
Bioexploration of keeled versus non-keeled teeth confirmed the important structural purpose of the keel in natural sea urchins (Figure 8). The bioexploration result provides data that helps explain why modern sea urchins evolved keel structures. We acknowledge that Porter17,18 was the first to propose the bioexploration step applied in this work, which was essential for using engineering analysis methods to quantify the mechanical advantage of the keel structure in the sea urchin tooth. Future bioinspired design that connects natural observation, biological materials science, bioinspired design and bioexploration can be beneficial for incorporating a deeper rooted familiarity with natural design principles.
The authors have nothing to disclose.
This work is supported by Multi-University Research Initiative through the Air Force Office of Scientific Research of the United States (AFOSR-FA9550-15-1-0009) (M. B. F., S. E. N., J.-Y. J., J. M). Collection of pink sea urchins was supported by the University of California Ship Funds and the US National Marine Fisheries Service (K.N.S., J.R.A.T). The authors acknowledge the following people: Prof. Jerry Tustaniwskyj for helpful suggestions during development of the bioinspired Aristotle’s lantern sampler, Prof. Marc A. Meyers (UCSD, Dept. of Mechanical and Aerospace Engineering, Materials Science and Engineering Program), Prof. Robert L. Sah and Esther Cory (UCSD, Dept. of Bioengineering), and Dr. Maya deVries (Marine Biology Research Division, Scripps Institution of Oceanography). We also thank undergraduate students Sze Hei Siu, Jerry Ng and Ivan Torres for polishing urchin teeth cross-sections.
BUEHLERMET II 8 PLN 600/P1200 | Buehler | 305308600102 | Abrasive paper for polishing |
TRIDENT POLISH CLOTH 8" PSA | Buehler | 407518 | Polish cloth for 3 um suspension |
METADI SUPREME POLY SUSP,3MIC | Buehler | 406631 | Polish suspension (3 um) |
MICROCLOTH FOR 8 IN WHEEL PSA | Buehler | 407218 | Polish cloth for 50 nm suspension |
MASTERPREP SUSPENSION, 6 OZ | Buehler | 636377006 | Polish suspension (50 nm) |
Skyscan 1076 micro-CT Scanner | Bruker | Micro-CT scanner equipment | |
Amira software | FEI Visualization Sciences Group | Software for 3D manipulation of Micro-CT scans | |
FEI Philips XL30 | FEI Philips | ESEM equipment for characterization of polished tooth cross-sections | |
SolidWorks Design software | Dassault Systems | Design software for CAD drawing bioinspired device | |
SolidWorks Simulation software | Dassault Systems | Simulation software for stress test of CAD drawing bioinspired device | |
Dimension 1200es | Stratasys | 3D printer for fabrication of bioinspired device from CAD drawing | |
ABSplus | Stratasys | 3D printer plastic |