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Why the Seahorse Tail Is Square

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Why the Seahorse Tail Is Square RESEARCH ◥ RESEARCH ARTICLE SUMMARY BIOMECHANICS Why the seahorse tail is square Michael M. Porter,* Dominique Adriaens, Ross L. Hatton, Marc A. Meyers, Joanna McKittrick INTRODUCTION: Although the predominant shapes of most animal tails are cylindrical, seahorse tails are square prisms. The skeleton of their tails consists of a bony armor arranged into several ringlike segments composed of four L-shaped plates that surround a central vertebra. These plates articulate with special- ized joints that facilitate bending and twisting, as well as resist vertebral fracture from crush- ing. Muscles attached to the vertebral column transmit forces to the bony plates to provide motion for grasping and holding on to objects such as sea grasses, mangrove roots, and coral on October 13, 2016 reefs, which allows them to hide and rely on camouflage when evading predators and cap- turing prey. RATIONALE: We hypothesize that the square cross-sectionalarchitectureof a seahorse tail improves mechanical performance in prehen- sion (grasping ability) and armored functions (crushing resistance), relative to a cylindrical Engineering designs answer biological questions. 3D-printed models that mimic a seahorse tail one. To test this hypothesis, we evaluated the were designed not only for potential engineering applications but also to answer the biological mechanics of two three-dimensional (3D)– question, why might tails organized into square prisms be better than cylinders? A mechanical printed prototypes composed of articulating http://science.sciencemag.org/ comparison of the prototypes shows that articulated square prisms perform better than do cyl- plates and vertebrae that mimic the natural inders for grasping and resistance to crushing. (square prism) and a hypothetical (cylindrical) tail structure. We compared the bending, twist- ing, and compressive behavior of the biomi- excessive torsion and preserves articulatory the mechanical benefits for seahorses to have metic prototypes to show that the square profile organization, which could provide seahorses a evolved prehensile tails composed of ar- isbetterthanthecircularonefortwointe- natural safety factor against torsion-induced mored plates organized into square prisms. grated functions: grasping ability and crushing damage and assist in tail relaxation. Further, Beyond their intended practical applica- Downloaded from resistance. thesquarearchitectureisflat(increasingsur- tions, engineering designs are convenient face contact) and undergoes an exterior shape means to answer elusive biological questions RESULTS: Seahorse tails (and the prototypes) change when twisted, which could allow sea- when live animal data are unavailable (for have three primary joints that enable motion: horses to grasp objects with more control. Glid- example, seahorses do not have cylindrical ball-and-socket, peg-and-socket, and gliding. ing joints are present at the plate overlaps along tails). Understanding the role of mechanics in The ball-and-socket joints connect adjacent all four sides of both prototypes. Under trans- these prototypes may help engineers to de- ◥ vertebrae and constrain verse compression and impact (with a rubber velop future seahorse-inspired technologies ON OUR WEB SITE bendinginboththesquare mallet), the plates of the square prototype slide that mimic the prehensile and armored func- Read the full article and cylindrical prototypes past one another with one degree of translation tions of the natural appendage for a variety of at http://dx.doi. to the same degree, exhib- freedom (analogous to the crushing behavior of applications in robotics, defense systems, or org/10.1126/ iting a behavior similar to a natural seahorse tail), exhibiting a response biomedicine.▪ science.aaa6683 that of a natural seahorse that is stiffer, stronger, and more resilient .................................................. tail. The peg-and-socket than its cylindrical counterpart, whose plates joints connect the plates of adjacent segments translate and rotate on impact. and substantially restrict twisting in the pro- The list of author affiliations is available in the full article online. *Corresponding author. E-mail: [email protected] CONCLUSION: totype with a square profile, as compared with Exploration of these biologi- Cite this article as M. M. Porter et al., Science 349, aaa6683 the circular one. The square geometry limits cally inspired designs provides insight into (2015). DOI: 10.1126/science.aaa6683 46 3JULY2015• VOL 349 ISSUE 6243 sciencemag.org SCIENCE RESEARCH ◥ manders, marsupials, and rodents) (14–17), a pe- RESEARCH ARTICLE ripherally plated skeleton is not exclusive to fishes and is even an ancestral condition of the vertebral lineages (18, 19), with different patterns BIOMECHANICS having arisen independently (such as ostracoderms, polypterids, gasterosteids, loricariids, and pegasids) (20). One recurrent pattern is where consecutive Why the seahorse tail is square plates articulate through a peg-and-socket con- nection, combining some level of flexibility with Michael M. Porter,1* Dominique Adriaens,2 Ross L. Hatton,3 strength. Such a joint is also present in seahorses, Marc A. Meyers,4,5,6 Joanna McKittrick4,5 as well as closely related species from the same family of Syngnathidae (pipehorses, pipefishes, Whereas the predominant shapes of most animal tails are cylindrical, seahorse tails are and seadragons). What differs among them, how- square prisms. Seahorses use their tails as flexible grasping appendages, in spite of a ever, is that there is notable variation in the size rigid bony armor that fully encases their bodies. We explore the mechanics of two of pegs and shape of sockets, as has recently been three-dimensional–printed models that mimic either the natural (square prism) or observed (12). The ancestral syngnathid configu- hypothetical (cylindrical) architecture of a seahorse tail to uncover whether or not the ration is a rather rigid nonprehensile tail that is square geometry provides any functional advantages. Our results show that the square completely enclosed by strongly abutting but prism is more resilient when crushed and provides a mechanism for preserving articulatory articulating (peg-and-socket) bony plates, such organization upon extensive bending and twisting, as compared with its cylindrical as those found in pipefishes (12). Seahorses and counterpart. Thus, the square architecture is better than the circular one in the context pipehorses are the only lineages that use their of two integrated functions: grasping ability and crushing resistance. tails as prehensile organs. Yet, they share with other syngnathids, and closely related seamoths eahorses do not use their tails for swim- could have helped promote this adaptation, es- (Pegasidae), a similar tail cross section that is not ming because they lack a caudal fin (1), but pecially when compared with other grasping ap- ovally shaped (as would be expected for fishes), instead as flexible prehensile appendages pendages in unrelated animal species and other but approximately square (5–13). Because the lat- S that allow them to hide and rely on body plated (nonsquare) skeletons in unrelated fish ter (pipefishes, seadragons, and seamoths) do not on October 13, 2016 crypsis to evade predators (2)andcapture species. have flexible tails, this suggests that the square prey (3) by holding on to objects such as sea Whereas several animals have developed grasp- morphology may not reflect a structural adapta- grasses, mangrove roots, and coral reefs (4). The ing appendages that are cylindrical and com- tion directly related to tail prehensility but could skeleton of a seahorse consists of a rigid, sub- posed of soft tissues surrounding a central axis of provide some form of protection. Although it is dermal armor of articulating bony plates, formed articulating skeletal elements (for example, tails likely that larger fish may swallow seahorses and within the skin, that fully encase its body (Fig. 1A) of New World monkeys and some lizards, sala- other syngnathids whole, the peripherally plated (5–13). The tail armor is arranged into several ring-like segments composed of four L-shaped plates that surround a central vertebra (Fig. 1B). Muscles attached to the vertebrae transmit forces to the bony plates to control motion (10–12). Recent studies on the musculoskeletal structure, http://science.sciencemag.org/ biomechanics, and kinematics of seahorse tails suggest that this bony-plated armor actively fa- cilitates tail bending and twisting (Fig. 1B) (10–12) as well as resists vertebral fracture due to impact and crushing (Fig. 1C) (13). Selective pres- sures related to the defensive strategies [bony plates make eating seahorses difficult (2)] and feeding behavior [tail-attached, sit-and-wait suc- Downloaded from tion feeding (3)] of seahorses may have driven the evolution of an ancestral plated system (square in cross section, but rather rigid and nonpre- hensile) into a more flexible system of similar plate organization for an added grasping func- tionality. Accordingly, we hypothesize that the cross-sectional square architecture of a seahorse tail possesses several mechanical advantages that 1Department of Mechanical Engineering, Clemson University, Clemson, SC 29634, USA. 2Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, B-9000 Ghent, Belgium. 3School of Mechanical, Industrial, and Manufacturing Engineering, Oregon State University, Corvallis, OR 97330, USA. 4Materials Science and Fig. 1.
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