Experiments and theory of undulatory locomotion in a simple structured medium

Journal of the Royal Society Interface

Volumn 9, Issue 73, 2012, Pages 1809-1823

  Majmudar, Trushant ^a   Keaveny, Eric E ^a,b   Zhang, Jun ^a   Shelley, Michael J ^a  

^a NEW YORK UNIVERSITY   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Biofluid dynamics; C. elegans; Complex media; Fluid structure interactions; Locomotion

Indexed keywords

BIPED LOCOMOTION; DYNAMICS; HYDRODYNAMICS;

BIOFLUID DYNAMICS; BIOLOGICAL SENSING; CAENORHABDITIS ELEGANS; COMPLEX MEDIA; COMPLEX TRAJECTORIES; CONTACT INTERACTION; ELEGANS; FLUID-FILLED; GEOMETRICAL CONSTRAINTS; HYDRODYNAMIC EFFECT; LATTICE SPACING; MECHANICAL INTERACTIONS; MECHANICAL MODEL; MICRO-PILLARS; UNDULATORY LOCOMOTION; VELOCITY FLUCTUATIONS;

MOTION PLANNING;

ARTICLE; BEHAVIOR; CAENORHABDITIS ELEGANS; DYNAMICS; EXPERIMENT; GAIT; HYDRODYNAMICS; LOCOMOTION; NONHUMAN; SWIMMING; THEORY; UNDULATORY LOCOMOTION; VELOCITY; WORM;

EID: 84863670001     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2011.0856     Document Type: Article

References (46)

1. Gray, J. 1953 Undulatory propulsion. Q. J. Microsc. Sci. 94, 551-578.
2. Gray, J. 1968 Animal locomotion. World Naturalist Series. London, UK: Weidenfeld & Nicolson.
3. Hu, D., Nirody, J., Scott, T. & Shelley, M. 2009 The mechanics of slithering locomotion. Proc. Natl Acad. Sci. USA 106, 10 081-10 085. (doi:10.1073/pnas.0812533106)
4. Lighthill, J. 1975 Mathematical biofluiddynamics. Philadelphia, PA: SIAM.
5. Childress, S. 1981 Mechanics of swimming and flying. Cambridge, UK: Cambridge University Press.
6. Maladen, R. D., Ding, Y., Li, C. & Goldman, D. I. 2009 Undulatory swimming in sand: subsurface locomotion of the sandfish lizard. Science 325, 314-318. (doi:10.1126/science.1172490)
7. Purcell, E. 1977 Life at low Reynolds number. Am. J. Phys. 45, 3-11. (doi:10.1119/1.10903)
8. Brennen, C. & Winet, H. 1977 Fluid mechanics of propulsion by cilia and flagella. Annu. Rev. Fluid Mech. 9, 339-398. (doi:10.1146/annurev.fl.09. 010177.002011)
9. Fauci, L. & Dillon, R. 2006 Biofluidmechanics of reproduction. Annu. Rev. Fluid Mech. 38, 371-394. (doi:10.1146/annurev.fluid.37.061903.175725)
10. Lauga, E. & Powers, T. 2009 The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72, 096601. (doi:10.1088/0034-4885/72/9/096601)
11. Rutllant, J., Lopez-Bejar, M. & Lopez-Gatius, F. 2005 Ultrastructural and rheological properties of bovine vaginal fluid and its relation to sperm motility and fertilization: a review. Reprod. Domest. Anim. 40, 79-86. (doi:10.1111/j.1439-0531.2004.00510.x)
12. Rikmenspoel, R. 1984 Movements and active moments of bull sperm flagella as a function of temperature and viscosity. J. Exp. Biol. 108, 205-230.
13. Paul, R., Brey, P. & Robert, V. 2002 Plasmodium sex determination and transmission to mosquitoes. Trends Parasitol. 18, 32-38. (doi:10.1016/S1471- 4922(01)02122-5)
14. Kuehn, A. & Pradel, G. 2010 The coming-out of malaria gametocytes. J. Biomed. Biotechnol. 2010, 976827. (doi:10.1155/2010/976827)
15. Jay, A. 1975 Geometry of human erythrocyte. 1. Effect of albumin on cell geometry. Biophys. J. 15, 205-222. (doi:10.1016/S0006-3495(75)85812-7)
16. Purves, W., Orians, G. & Heller, H. 2004 Life: science of biology, 7th edn. Sunderland, MA: Sinauer Associates.
17. Niebur, E. & Erdös, P. 1991 Theory of the locomotion of nematodes: dynamics of undulatory progression on a surface. Biophys. J. 60, 1132-1146. (doi:10.1016/S0006-3495(91)82149-X)
18. Berri, S., Boyle, J. H., Tassieri, M., Hope, I. A. & Cohen, N. 2009 Forward locomotion of the nematode C. elegans is achieved through modulation of a single gait. HFSP J. 3, 186-193. (doi:10.2976/1.3082260)
19. Sznitman, J., Purohit, P. K., Krajacic, P., Lamitina, T. & Arratia, P. E. 2010 Material properties of Caenorhabditis elegans swimming at low Reynolds number. Biophys. J. 98, 617-626. (doi:10.1016/j.bpj.2009.11.010)
20. Korta, J., Clark, D. A., Gabel, C. V., Mahadevan, L. & Samuel, A. D. T. 2007 Mechanosensation and mechanical load modulate the locomotory gait of swimming C. elegans. J. Exp. Biol. 210, 2383-2389. (doi:10.1242/jeb.004572)
21. Fang-Yen, C., Wyart, M., Xie, J., Kawai, R., Kodger, T., Chen, S., Wen, Q. & Samuel, A. D. T. 2010 Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 107, 20 323-20 328. (doi:10.1073/pnas.1003016107)
22. Hall, D. H. & Altun, Z. F. 2008 C. elegans atlas. New York, NY: Cold Spring Harbor Laboratory Press.
23. Pierce-Shimomura, J. T., Chen, B. L., Mun, J. J., Ho, R., Sarkis, R. & McIntire, S. L. 2008 Genetic analysis of crawling and swimming locomotory patterns in C. elegans. Proc. Natl Acad. Sci. USA 105, 20 982-20 987. (doi:10.1073/pnas.0810359105)
24. Karbowski, J., Cronin, C. J., Seah, A., Mendel, J. E., Cleary, D. & Sternberg, P. W. 2006 Conservation rules, their breakdown, and optimality in Caenorhabditis sinusoidal locomotion. J. Theor. Biol. 242, 652-669. (doi:10.1016/j.jtbi.2006.04.012)
25. Park, S., Hwang, H., Nam, S.-W., Martinez, F., Austin, R. H. & Ryu, W. S. 2008 Enhanced Caenorhabditis elegans locomotion in a structured microfluidic environment. PLoS ONE 3, e2550. (doi:10.1371/journal.pone.0002550)
26. Lockery, S. R. et al. 2008 Artificial dirt: microfluidic substrates for nematode neurobiology and behavior. J. Neurophysiol. 99, 3136-3143. (doi:10.1152/jn.91327.2007)
27. Qin, J. & Wheeler, A. R. 2007 Maze exploration and learning in C. elegans. Lab Chip 7, 186-192. (doi:10.1039/b613414a)
28. Jung, S. 2010 Caenorhabditis elegans swimming in a saturated particulate system. Phys. Fluids 22, 031903. (doi:10.1063/1.3359611)
29. Juarez, G., Lu, K., Sznitman, J. & Arratia, P. E. 2010 Motility of small nematodes in wet granular media. Europhys. Lett. 92, 44002. (doi:10.1209/0295-5075/92/44002)
30. Leshansky, A. M. 2009 Enhanced low-Reynolds-number propulsion in heterogeneous viscous environments. Phys. Rev. E 80, 051911. (doi:10.1103/PhysRevE.80.051911)
31. Teran, J., Fauci, L. & Shelley, M. 2010 Viscoelastic fluid response can increase the speed and efficiency of a free swimmer. Phys. Rev. Lett. 104, 038101. (doi:10.1103/PhysRevLett.104.038101)
32. Fu, H. C., Wolgemuth, C. W. & Powers, T. R. 2008 Beating patterns of filaments in viscoelastic fluids. Phys. Rev. E 78, 041913. (doi:10.1103/ PhysRevE.78.041913)
33. Fu, H. C., Wolgemuth, C. W. & Powers, T. R. 2009 Swimming speeds of filaments in nonlinearly viscoelastic fluids. Phys. Fluids 21, 033102. (doi:10.1063/1.3086320)
34. Fu, H. C., Shenoy, V. B. & Powers, T. R. 2010 Low-Reynolds-number swimming in gels. Europhys. Lett. 91, 24002. (doi:10.1209/0295-5075/91/24002)
35. Lauga, E. 2007 Propulsion in a viscoelastic fluid. Phys. Fluids 19, 083104. (doi:10.1063/1.2751388)
36. Duffy, D. C., McDonald, J. C., Schueller, O. J. A. & Whitesides, G. M. 1998 Rapid prototyping of microfluidic systems in poly(dimethylsiloxane). Anal. Chem. 70, 4974-4984. (doi:10.1021/ac980656z)
37. Goldstein, R. E. & Langer, S. A. 1995 Nonlinear dynamics of stiff polymers. Phys. Rev. Lett. 75, 1094-1097. (doi:10.1103/PhysRevLett.75.1094)
38. Maxey, M. & Patel, B. 2001 Localized force representation for particles sedimenting in Stokes flow. Int. J. Multiphase Flow 27, 1603-1626. (doi:10.1016/S0301-9322(01)00014-3)
39. Lomholt, S. & Maxey, M. 2003 Force-coupling method for particulate two-phase flow: Stokes flow. J. Comput. Phys. 184, 381-405. (doi:10.1016/S0021- 9991(02)00021-9)
40. Karniadakis, G., Israeli, M. & Orszag, S. A. 1991 High-order splitting methods for the incompressible Navier-Stokes equations. J. Comput. Phys. 97, 414-443. (doi:10.1016/0021-9991(91)90007-8)
41. Lowe, C. 2003 Dynamics of filaments: modelling the dynamics of driven microfilaments. Phil. Trans. R. Soc. Lond. B 358, 1543-1550. (doi:10.1098/rstb.2003.1340)
42. Wiggins, C. H. & Goldstein, R. E. 1998 Flexive and propulsive dynamics of elastica at low Reynolds number. Phys. Rev. Lett. 80, 3879-3882. (doi:10.1103/PhysRevLett.80.3879)
43. Anderson, A., Young, I., Sleeman, B., Griffiths, B. & Robertson, W. 1997 Nematode movement along a chemical gradient in a structurally heterogeneous environment. 1. Experiment. Fundam. Appl. Nematol. 20, 157-163.
44. Morales, P., Roco, M. & Vigil, P. 1993 Human cervical mucus: relationship between biochemical characteristics and ability to allow migration of spermatozoa. Hum. Reprod. 8, 78-83.
45. Suarez, S. & Pacey, A. 2006 Sperm transport in the female reproductive tract. Hum. Reprod. Update 12, 23-37. (doi:10.1093/humupd/dmi047)
46. Schmitt, J., Garcia, M., Razo, R. C., Holmes, P. & Full, R. J. 2002 Dynamics and stability of legged locomotion in the horizontal plane: a test case using insects. Biol. Cybern. 86, 343-353. (doi:10.1007/s00422-001-0300-3)