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Annual Review of Marine Science

Volume 13, 2021

The Hydrodynamics of Jellyfish Swimming

Abstract

Jellyfish have provided insight into important components of animal propulsion, such as suction thrust, passive energy recapture, vortex wall effects, and the rotational mechanics of turning. These traits are critically important to jellyfish because they must propel themselves despite severe limitations on force production imposed by rudimentary cnidarian muscular structures. Consequently, jellyfish swimming can occur only by careful orchestration of fluid interactions. Yet these mechanics may be more broadly instructive because they also characterize processes shared with other animal swimmers, whose structural and neurological complexity can obscure these interactions. In comparison with other animal models, the structural simplicity, comparative energetic efficiency, and ease of use in laboratory experimentation allow jellyfish to serve as favorable test subjects for exploration of the hydrodynamic bases of animal propulsion. These same attributes also make jellyfish valuable models for insight into biomimetic or bioinspired engineeringof swimming vehicles. Here, we review advances in understanding of propulsive mechanics derived from jellyfish models as a pathway toward the application of animal mechanics to vehicle designs.

Keyword(s): biomechanics, biomimetic, propulsion, rowing propulsion, zooplankton
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2021-01-03
2024-04-18
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Literature Cited

  1. Alexander RM. 2003. Principles of Animal Locomotion Princeton, NJ: Princeton Univ. Press
  2. Anderson PA, Schwab WE. 1981. The organization and structure of nerve and muscle in the jellyfish Cyanea capillata (Coelenterata; Scyphozoa). J. Morphol. 170:383–99
     [Google Scholar]
  3. Bale R, Neveln ID, Bhalla APS, MacIver MA, Patankar NA 2015. Convergent evolution of mechanically optimal locomotion in aquatic invertebrates and vertebrates. PLOS Biol 13:e1002123
     [Google Scholar]
  4. Baudinette R, Schmidt-Nielsen K. 1974. Energy cost of gliding flight in herring gulls. Nature 248:83–84
     [Google Scholar]
  5. Biewener A, Patek S. 2018. Animal Locomotion Oxford, UK: Oxford Univ. Press
  6. Blake R. 1979. The energetics of hovering in the mandarin fish (Synchropus picturatus). J. Exp. Biol. 82:25–33
     [Google Scholar]
  7. Blake R. 1983. Mechanics of gliding in birds with special reference to the influence of the ground effect. J. Biomech. 16:649–54
     [Google Scholar]
  8. Boelsterli U. 1977. An electron microscopic study of early developmental stages, myogenesis, oogenesis and cnidogenesis in the anthomedusa, Podocoryne carnea M. Sars. J. Morphol. 154:259–89
     [Google Scholar]
  9. Bone Q, Trueman E. 1982. Jet propulsion of the calycophoran siphonophores Chelophyes and Abylopsis. J. Mar. Biol. Assoc. UK 62:263–76
     [Google Scholar]
  10. Bonner JT. 1965. Size and Cycles: An Essay on the Structure of Biology Princeton, NJ: Princeton Univ. Press
  11. Chapman DM. 1974. Cnidarian Histology New York: Academic
  12. Colin SP, Costello JH, Dabiri JO, Villanueva A, Blottman JB et al. 2012. Biomimetic and live medusae reveal the mechanistic advantages of a flexible bell margin. PLOS ONE 7:e48909
     [Google Scholar]
  13. Collins AG, Schuchert P, Marques AC, Jankowski T, Medina M, Schierwater B 2006. Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst. Biol. 55:97–115
     [Google Scholar]
  14. Costello JH, Colin SP, Dabiri JO 2008. Medusan morphospace: phylogenetic constraints, biomechanical solutions, and ecological consequences. Invertebr. Biol. 127:265–90
     [Google Scholar]
  15. Costello JH, Colin SP, Gemmell BJ, Dabiri JO 2019. Hydrodynamics of vortex generation during bell contraction by the hydromedusa Eutonina indicans (Romanes, 1876). Biomimetics 4:44
     [Google Scholar]
  16. Dabiri JO, Bose S, Gemmell BJ, Colin SP, Costello JH 2014. An algorithm to estimate unsteady and quasi-steady pressure fields from velocity field measurements. J. Exp. Biol. 217:331–36
     [Google Scholar]
  17. Dabiri JO, Colin SP, Costello JH 2006. Fast-swimming hydromedusae exploit velar kinematics to form an optimal vortex wake. J. Exp. Biol. 209:2025–33
     [Google Scholar]
  18. Dabiri JO, Colin SP, Costello JH 2007. Morphological diversity of medusan lineages constrained by animal–fluid interactions. J. Exp. Biol. 210:1868–73
     [Google Scholar]
  19. Dabiri JO, Colin SP, Costello JH, Gharib M 2005. Flow patterns generated by oblate medusan jellyfish: field measurements and laboratory analyses. J. Exp. Biol. 208:1257–65
     [Google Scholar]
  20. Dabiri JO, Colin SP, Gemmell BJ, Lucas KN, Leftwich M, Costello JH 2019. Primitive and modern swimmers solve the challenges of turning similarly to achieve high maneuverability. bioRxiv 706762. https://doi.org/10.1101/706762
    [Crossref]
  21. Daniel TL. 1983. Mechanics and energetics of medusan jet propulsion. Can. J. Zool. 61:1406–20
     [Google Scholar]
  22. Daniel TL. 1984. Unsteady aspects of aquatic locomotion. Am. Zool. 24:121–34
     [Google Scholar]
  23. DeMont ME, Gosline JM. 1988a. Mechanics of jet propulsion in the hydromedusan jellyfish, Polyorchis penicillatus: I. Mechanical properties of the locomotor structure. J. Exp. Biol. 134:313–32
     [Google Scholar]
  24. DeMont ME, Gosline JM. 1988b. Mechanics of jet propulsion in the hydromedusan jellyfish, Polyorchis penicillatus: II. Energetics of the jet cycle. J. Exp. Biol. 134:333–45
     [Google Scholar]
  25. Drucker EG, Lauder GV. 2000. A hydrodynamic analysis of fish swimming speed: wake structure and locomotor force in slow and fast labriform swimmers. J. Exp. Biol. 203:2379–93
     [Google Scholar]
  26. Dular M, Bajcar T, Širok B 2009. Numerical investigation of flow in the vicinity of a swimming jellyfish. Eng. Appl. Comput. Fluid Mech. 3:258–70
     [Google Scholar]
  27. Feitl K, Millett A, Colin SP, Dabiri JO, Costello JH 2009. Functional morphology and fluid interactions during early development of the scyphomedusa Aurelia aurita. Biol. . Bull 217:283–91
     [Google Scholar]
  28. Fernández-Prats R, Raspa V, Thiria B, Huera-Huarte F, Godoy-Diana R 2015. Large-amplitude undulatory swimming near a wall. Bioinspir. Biomim. 10:016003
     [Google Scholar]
  29. Fish FE, Lauder GV. 2017. Control surfaces of aquatic vertebrates: active and passive design and function. J. Exp. Biol. 220:4351–63
     [Google Scholar]
  30. Floryan D, Van Buren T, Smits AJ 2019. Swimmers’ wakes are not reliable indicators of swimming performance. arXiv:1906.10826 [physics.flu-dyn]
  31. Frame J, Lopez N, Curet O, Engeberg ED 2018. Thrust force characterization of free-swimming soft robotic jellyfish. Bioinspir. Biomim. 13:064001
     [Google Scholar]
  32. Gemmell BJ, Colin SP, Costello JH 2018. Widespread utilization of passive energy recapture in swimming medusae. J. Exp. Biol. 221:jeb168575
     [Google Scholar]
  33. Gemmell BJ, Colin SP, Costello JH, Dabiri JO 2015a. Suction-based propulsion as a basis for efficient animal swimming. Nat. Commun. 6:8790
     [Google Scholar]
  34. Gemmell BJ, Costello JH, Colin SP, Stewart CJ, Dabiri JO et al. 2013. Passive energy recapture in jellyfish contributes to propulsive advantage over other metazoans. PNAS 110:17904–9
     [Google Scholar]
  35. Gemmell BJ, Du Clos KT, Colin SP, Sutherland KR, Costello JH 2020. The most efficient metazoan swimmer creates a ‘virtual wall’ to enhance performance. bioRxiv 2020.05.01.069518. https://doi.org/10.1101/2020.05.01.069518
    [Crossref]
  36. Gemmell BJ, Troolin DR, Costello JH, Colin SP, Satterlie RA 2015b. Control of vortex rings for manoeuvrability. J. R. Soc. Interface 12:20150389
     [Google Scholar]
  37. Gladfelter W. 1972. Structure and function of the locomotory system of the Scyphomedusa Cyanea capillata. Mar. Biol 14:150–60
     [Google Scholar]
  38. Gladfelter W. 1973. A comparative analysis of the locomotory systems of medusoid Cnidaria. Helgol. Wiss. Meeresunters. 25:228–72
     [Google Scholar]
  39. Hainsworth FR. 1988. Induced drag savings from ground effect and formation flight in brown pelicans. J. Exp. Biol. 135:431–44
     [Google Scholar]
  40. Higgins J III, Ford M, Costello JH 2008. Transitions in morphology, nematocyst distribution, fluid motions, and prey capture during development of the scyphomedusa Cyanea capillata. Biol. Bull 214:29–41
     [Google Scholar]
  41. Hoover AP, Griffith BE, Miller LA 2017. Quantifying performance in the medusan mechanospace with an actively swimming three-dimensional jellyfish model. J. Fluid Mech. 813:1112–55
     [Google Scholar]
  42. Hoover AP, Porras AJ, Miller LA 2019. Pump or coast: the role of resonance and passive energy recapture in medusan swimming performance. J. Fluid Mech. 863:1031–61
     [Google Scholar]
  43. Joshi A, Kulkarni A, Tadesse Y 2019. FludoJelly: experimental study on jellyfish-like soft robot enabled by soft pneumatic composite (SPC). Robotics 8:56
     [Google Scholar]
  44. Jusufi A, Vogt DM, Wood RJ, Lauder GV 2017. Undulatory swimming performance and body stiffness modulation in a soft robotic fish-inspired physical model. Soft Robot 4:202–10
     [Google Scholar]
  45. Kim H-S, Lee J-Y, Chu W-S, Ahn S-H 2017. Design and fabrication of soft morphing ray propulsor: undulator and oscillator. Soft Robot 4:49–60
     [Google Scholar]
  46. Liao JC, Beal DN, Lauder GV, Triantafyllou MS 2003. Fish exploiting vortices decrease muscle activity. Science 302:1566–69
     [Google Scholar]
  47. Lipinski D, Mohseni K. 2009. Flow structures and fluid transport for the hydromedusae Sarsia tubulosa and Aequorea victoria. J. Exp. Biol 212:2436–47
     [Google Scholar]
  48. Lucas KN, Dabiri JO, Lauder GV 2017. A pressure-based force and torque prediction technique for the study of fish-like swimming. PLOS ONE 12:e0189225
     [Google Scholar]
  49. McHenry MJ. 2007. Comparative biomechanics: the jellyfish paradox resolved. Curr. Biol. 17:R632–33
     [Google Scholar]
  50. McHenry MJ, Jed J. 2003. The ontogenetic scaling of hydrodynamics and swimming performance in jellyfish (Aurelia aurita). J. Exp. Biol. 206:4125–37
     [Google Scholar]
  51. Megill WM, Gosline JM, Blake RW 2005. The modulus of elasticity of fibrillin-containing elastic fibres in the mesoglea of the hydromedusa Polyorchis penicillatus. J. Exp. Biol 208:3819–34
     [Google Scholar]
  52. Miles JG, Battista NA. 2019. Naut your everyday jellyfish model: exploring how tentacles and oral arms impact locomotion. Fluids 4:169
     [Google Scholar]
  53. Nagata RM, Morandini AC, Colin SP, Migotto AE, Costello JH 2016. Transitions in morphologies, fluid regimes, and feeding mechanisms during development of the medusa Lychnorhiza lucerna. Mar. Ecol. Prog. . Ser 557:145–59
     [Google Scholar]
  54. Najem J, Sarles SA, Akle B, Leo DJ 2012. Biomimetic jellyfish-inspired underwater vehicle actuated by ionic polymer metal composite actuators. Smart Mater. Struct. 21:094026
     [Google Scholar]
  55. Nawroth JC, Feitl K, Colin SP, Costello JH, Dabiri JO 2010. Phenotypic plasticity in juvenile jellyfish medusae facilitates effective animal–fluid interaction. Biol. Lett. 6:389–93
     [Google Scholar]
  56. Nawroth JC, Lee H, Feinberg AW, Ripplinger CM, McCain ML et al. 2012. A tissue-engineered jellyfish with biomimetic propulsion. Nat. Biotechnol. 30:792
     [Google Scholar]
  57. Neil TR, Askew GN. 2018. Jet-paddling jellies: swimming performance in the Rhizostomeae jellyfish Catostylus mosaicus. . J. Exp. Biol 221:jeb191148
     [Google Scholar]
  58. Nowroozi BN, Strother JA, Horton JM, Summers AP, Brainerd EL 2009. Whole-body lift and ground effect during pectoral fin locomotion in the northern spearnose poacher (Agonopsis vulsa). Zoology 112:393–402
     [Google Scholar]
  59. O'Dor R, Hoar J. 2000. Does geometry limit squid growth. ? ICES J. Mar. Sci. 57:8–14
     [Google Scholar]
  60. Park H, Choi H. 2010. Aerodynamic characteristics of flying fish in gliding flight. J. Exp. Biol. 213:3269–79
     [Google Scholar]
  61. Park SG, Chang CB, Huang W-X, Sung HJ 2014. Simulation of swimming oblate jellyfish with a paddling-based locomotion. J. Fluid Mech. 748:731–55
     [Google Scholar]
  62. Pauly D. 1997. Geometrical constraints on body size. Trends Ecol. Evol. 12:442
     [Google Scholar]
  63. Quinn DB, Lauder GV, Smits AJ 2014. Scaling the propulsive performance of heaving flexible panels. J. Fluid Mech. 738:250–67
     [Google Scholar]
  64. Rayner JM. 1991. On the aerodynamics of animal flight in ground effect. Philos. Trans. R. Soc. Lond. B 334:119–28
     [Google Scholar]
  65. Ren Z, Hu W, Dong X, Sitti M 2019. Multi-functional soft-bodied jellyfish-like swimming. Nat. Commun. 10:2703
     [Google Scholar]
  66. Ruiz LA, Whittlesey RW, Dabiri JO 2011. Vortex-enhanced propulsion. J. Fluid Mech. 668:5–32
     [Google Scholar]
  67. Satterlie RA. 2002. Neuronal control of swimming in jellyfish: a comparative story. Can. J. Zool. 80:1654–69
     [Google Scholar]
  68. Satterlie RA. 2011. Do jellyfish have central nervous systems. ? J. Exp. Biol. 214:1215–23
     [Google Scholar]
  69. Satterlie RA. 2015. The search for ancestral nervous systems: an integrative and comparative approach. J. Exp. Biol. 218:612–17
     [Google Scholar]
  70. Schmid S, Lutz T, Krämer E 2009. Impact of modelling approaches on the prediction of ground effect aerodynamics. Eng. Appl. Comput. Fluid Mech. 3:419–29
     [Google Scholar]
  71. Schuchert P, Reber-Müller S, Schmid V 1993. Life stage specific expression of a myosin heavy chain in the hydrozoan Podocoryne carnea. . Differentiation 54:11–18
     [Google Scholar]
  72. Seipel K, Schmid V. 2005. Evolution of striated muscle: jellyfish and the origin of triploblasty. Dev. Biol. 282:14–26
     [Google Scholar]
  73. Simmons SL, Satterlie RA. 2018. Tentacle musculature in the cubozoan jellyfish Carybdea marsupialis. Biol. . Bull 235:91–101
     [Google Scholar]
  74. Tytell ED, Lauder GV. 2004. The hydrodynamics of eel swimming: I. Wake structure. J. Exp. Biol. 207:1825–41
     [Google Scholar]
  75. Villanueva A, Bresser S, Chung S, Tadesse Y, Priya S 2009. Jellyfish inspired underwater unmanned vehicle. Electroactive Polymer Actuators and Devices (EAPAD) 2009 Y Bar-Cohen, T Wallmersperger 458–69 Proc. SPIE 7287 Bellingham, WA: Soc. Photo-Opt. Instrum. Eng.
     [Google Scholar]
  76. Villanueva A, Smith C, Priya S 2011. A biomimetic robotic jellyfish (Robojelly) actuated by shape memory alloy composite actuators. Bioinspir. Biomim. 6:036004
     [Google Scholar]
  77. Vogel S. 2013. Comparative Biomechanics: Life's Physical World Princeton, NJ: Princeton Univ. Press
  78. Webb PW. 1993. The effect of solid and porous channel walls on steady swimming of steelhead trout Oncorhynchus mykiss. J. Exp. Biol 178:97–108
     [Google Scholar]
  79. Whittlesey RW, Dabiri JO. 2013. Optimal vortex formation in a self-propelled vehicle. J. Fluid Mech. 737:78–104
     [Google Scholar]
  80. Willert CE, Gharib M. 1991. Digital particle image velocimetry. Exp. Fluids 10:181–93
     [Google Scholar]
  81. Xu NW, Dabiri JO. 2020. Low-power microelectronics embedded in live jellyfish enhance propulsion. Sci. Adv. 6:eaaz3194
     [Google Scholar]
  82. Yu J, Li X, Pang L, Wu Z 2019. Design and attitude control of a novel robotic jellyfish capable of 3D motion. Sci. China Inf. Sci. 62:194201
     [Google Scholar]
  83. Yu J, Xiao J, Li X, Wang W 2016. Towards a miniature self-propelled jellyfish-like swimming robot. Int. J. Adv. Robot. Syst. 13:5 https://doi.org/10.1177/1729881416666796
    [Crossref] [Google Scholar]
  84. Zimmerman KL, Jamshidi AD, Buckenberger A, Satterlie RA 2019. Organization of the subumbrellar musculature in the ephyra, juvenile, and adult stages of Aurelia aurita Medusae. Invertebr. Biol. 138:e12260
     [Google Scholar]
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The Hydrodynamics of Jellyfish Swimming
Annual Review of Marine Science 13, 375 (2021); https://doi.org/10.1146/annurev-marine-031120-091442
/content/journals/10.1146/annurev-marine-031120-091442
/content/journals/10.1146/annurev-marine-031120-091442
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