Locomotion Through Complex Fluids: An Experimental View

Chapter
Part of the Biological and Medical Physics, Biomedical Engineering book series (BIOMEDICAL)

Abstract

Recently, there has been renewed interest in the swimming of microorganisms for applications that include artificial swimmers, novel materials, drug delivery, and micro-robotics. Due to small length scales, the fluid mechanics of swimming of microorganisms are governed by low Reynolds number hydrodynamics. In such a regime, linear viscous forces dominate over nonlinear inertial forces. While our current understanding of locomotion at low Reynolds numbers is derived mainly from investigations in simple, Newtonian fluids (e.g., water), many of the fluids in which locomotion occurs contain solids and/or (biological) polymers that are instead not Newtonian. Examples include wet soils, human mucus, and fluids in the cervix and female reproductive track. A major challenge is to understand the propulsion mechanisms in fluids that display complex rheological behavior such as viscoelasticity and shear-thinning viscosity. Here, we will briefly review a few notable swimming experiments in Newtonian fluids and then discuss the latest experimental results on swimming in complex fluids, focusing on viscoelastic fluids.

References

  1. 1.
    E.M. Purcell, Am. J. Phys. 45, 3 (1977)ADSGoogle Scholar
  2. 2.
    C. Brennen, H. Winet, Annu. Rev. Fluid Mech. 9(1), 339 (1977)ADSGoogle Scholar
  3. 3.
    J. Gray, J. Exp. Biol. 32(4), 775 (1955)Google Scholar
  4. 4.
    J. Gray, G. Hancock, J. Exp. Biol. 32(4), 802 (1955)Google Scholar
  5. 5.
    N. Cohen, J.H. Boyle, Contemp. Phys. 51(2), 103 (2010)ADSGoogle Scholar
  6. 6.
    J. Gray, H.W. Lissmann, J. Exp. Biol. 41(1), 135 (1964)Google Scholar
  7. 7.
    J. Sznitman, X. Shen, R. Sznitman, P.E. Arratia, Phys. Fluids (1994–present) 22, 121901 (2010)Google Scholar
  8. 8.
    E. Lauga, T.R. Powers, Rep. Prog. Phys. 72(9), 096601 (2009)MathSciNetADSGoogle Scholar
  9. 9.
    J. Lighthill, SIAM Rev. 18(2), 161 (1976)MATHMathSciNetGoogle Scholar
  10. 10.
    N.A. Croll, The Behaviour of Nematodes: Their Activity, Senses and Responses (Edward Arnold, London, 1970)Google Scholar
  11. 11.
    J.G. White, E. Southgate, J.N. Thomson, S. Brenner, Philos. Trans. R. Soc. Lond. B Biol. Sci. 314, 1 (1986)ADSGoogle Scholar
  12. 12.
    W.B. Wood, The Nematode Caenorhabditis elegans (Cold Spring Harbour Laboratory, New York, 1987)Google Scholar
  13. 13.
    H.C. Berg, E. coli in Motion (Springer, New York, 2004)Google Scholar
  14. 14.
    H.C. Berg, Phys. Today 53(1), 24 (2000)ADSGoogle Scholar
  15. 15.
    H.C. Berg, Biochemistry 72(1), 19 (2003)Google Scholar
  16. 16.
    H.C. Berg, Curr. Biol. 18(16), R689 (2008)Google Scholar
  17. 17.
    D. Bray, Cell Movements: From Molecules to Motility (Garland Science, New York, 2001)Google Scholar
  18. 18.
    D.R. Mitchell, J. Phycol. 36, 261 (2000)Google Scholar
  19. 19.
    M. Werner, L.W. Simmons, Biol. Rev. 83, 191 (2008)Google Scholar
  20. 20.
    I. Gibbons, J. Cell Biol. 91(3), 107s (1981)Google Scholar
  21. 21.
    R. Lyons, O. Djahanbakhch, T. Mahmood, E. Saridogan, S. Sattar, M. Sheaff, A. Naftalin, R. Chenoy, Hum. Reprod. 17, 584 (2002)Google Scholar
  22. 22.
    R. Lyons, E. Saridogan, O. Djahanbakhch, Hum. Reprod. Update 12, 363 (2006)Google Scholar
  23. 23.
    T. Nakahari, A. Nishimura, C. Shimamoto, A. Sakai, H. Kuwabara, T. Nakano, S. Tanaka, Y. Kohda, H. Matsumura, H. Mori, Biomed. Res. 32, 321 (2011)Google Scholar
  24. 24.
    P. Satir, M.A. Sleigh, Annu. Rev. Physiol. 52, 137 (1990)Google Scholar
  25. 25.
    A. Korngreen, Z. Priel, Biophys. J. 67(1), 377 (1994)ADSGoogle Scholar
  26. 26.
    A.L. Oldenburg, R.K. Chhetri, D.B. Hill, B. Button, Biomed. Opt. Express 3, 1978 (2012)Google Scholar
  27. 27.
    G. Taylor, Proc. R. Soc. Lond. Ser. A Math. Phys. Sci. 209, 447 (1951)Google Scholar
  28. 28.
    G. Taylor, Proc. R. Soc. Lond. Ser. A Math. Phys. Sci. 211, 225 (1952)Google Scholar
  29. 29.
    I. Aranson, Physics 6, 61 (2013)Google Scholar
  30. 30.
    J.S. Guasto, R. Rusconi, R. Stocker, Annu. Rev. Fluid Mech. 44, 373 (2012)MathSciNetADSGoogle Scholar
  31. 31.
    S. Chattopadhyay, R. Moldovan, C. Yeung, X. Wu, Proc. Natl. Acad. Sci. 103(37), 13712 (2006)ADSGoogle Scholar
  32. 32.
    D. Katz, J. Blake, S. Paveri-Fontana, J. Fluid Mech. 72(03), 529 (1975)MATHADSGoogle Scholar
  33. 33.
    J. Happel, H. Brenner, Low Reynolds Number Hydrodynamics: With Special Applications to Particulate Media, vol. 1 (Springer, Berlin, 1983)Google Scholar
  34. 34.
    D. Saintillan, Physics 3, 84 (2010)Google Scholar
  35. 35.
    S.A. Koehler, T.R. Powers, Phys. Rev. Lett. 85(22), 4827 (2000)ADSGoogle Scholar
  36. 36.
    B. Qian, T.R. Powers, K.S. Breuer, Phys. Rev. Lett. 100, 078101 (2008)ADSGoogle Scholar
  37. 37.
    S.Y. Tony, E. Lauga, A. Hosoi, Phys. Fluids (1994–present) 18, 091701 (2006)Google Scholar
  38. 38.
    M.S. Sakar, C. Lee, P.E. Arratia, Phys. Fluids 21, 91107 (2009)Google Scholar
  39. 39.
    S. Zhong, K.W. Moored, V. Pinedo, J. Garcia-Gonzalez, A.J. Smits, Exp. Therm. Fluid Sci. 46, 1 (2013)Google Scholar
  40. 40.
    M. Kim, J.C. Bird, A.J. Van Parys, K.S. Breuer, T.R. Powers, Proc. Natl. Acad. Sci. 100(26), 15481 (2003)ADSGoogle Scholar
  41. 41.
    M.J. Kim, M.J. Kim, J.C. Bird, J. Park, T.R. Powers, K.S. Breuer, Exp. Fluids 37(6), 782 (2004)Google Scholar
  42. 42.
    E. Setter, I. Bucher, S. Haber, Phys. Rev. E 85, 066304 (2012)ADSGoogle Scholar
  43. 43.
    P. Weiss, Sci. News 169, 107 (2006)Google Scholar
  44. 44.
    R. Trouilloud, S.Y. Tony, A. Hosoi, E. Lauga, Phys. Rev. Lett. 101, 048102 (2008)ADSGoogle Scholar
  45. 45.
    C.H. Wiggins, D. Riveline, A. Ott, R.E. Goldstein, Biophys. J. 74, 1043 (1998)ADSGoogle Scholar
  46. 46.
    M. Leoni, J. Kotar, B. Bassetti, P. Cicuta, M.C. Lagomarsino, Soft Matter 5(2), 472 (2009)ADSGoogle Scholar
  47. 47.
    J.J. Abbott, K.E. Peyer, M.C. Lagomarsino, L. Zhang, L. Dong, I.K. Kaliakatsos, B.J. Nelson, Int. J. Rob. Res. 28(11), 1434 (2009)Google Scholar
  48. 48.
    H.C. Berg, Rev. Sci. Instrum. 42(6), 868 (1971)ADSGoogle Scholar
  49. 49.
    H.C. Berg, Adv. Opt. Elect. Microsc. 7, 1 (1978)Google Scholar
  50. 50.
    H.C. Berg, D.A. Brown, Nature 239(5374), 500 (1972)ADSGoogle Scholar
  51. 51.
    L. Turner, W.S. Ryu, H.C. Berg, J. Bacteriol. 182, 2793 (2000)Google Scholar
  52. 52.
    S.C. Lenaghan, C.A. Davis, W.R. Henson, Z. Zhang, M. Zhang, Proc. Natl. Acad. Sci. 108(34), E550 (2011)ADSGoogle Scholar
  53. 53.
    K. Drescher, K.C. Leptos, R.E. Goldstein, Rev. Sci. Instrum. 80(1), 014301 (2009)ADSGoogle Scholar
  54. 54.
    E. Lauga, W.R. DiLuzio, G.M. Whitesides, H.A. Stone, Biophys. J. 90(2), 400 (2006)ADSGoogle Scholar
  55. 55.
    R. Di Leonardo, D. Dell’Arciprete, L. Angelani, V. Iebba, Phys. Rev. Lett. 106(3), 038101 (2011)ADSGoogle Scholar
  56. 56.
    A.P. Berke, L. Turner, H.C. Berg, E. Lauga, Phys. Rev. Lett. 101(3), 038102 (2008)ADSGoogle Scholar
  57. 57.
    J. Cosson, P. Huitorel, C. Gagnon, Cell Motil. Cytoskeleton 54(1), 56 (2003)Google Scholar
  58. 58.
    L. Rothchild, Nature 198, 1221 (1963)ADSGoogle Scholar
  59. 59.
    D. Woolley, Reproduction 126, 259 (2003)Google Scholar
  60. 60.
    S. Jana, S.H. Um, S. Jung, Phys. Fluids (1994–present) 24(4), 041901 (2012)Google Scholar
  61. 61.
    P. Denissenko, V. Kantsler, D.J. Smith, J. Kirkman-Brown, Proc. Natl. Acad. Sci. 109(21), 8007 (2012)ADSGoogle Scholar
  62. 62.
    R. Ghosh, J. Sznitman, J. Vis. 15, 1–3 (2012)Google Scholar
  63. 63.
    F. Lebois, P. Sauvage, C. Py, O. Cardoso, B. Ladoux, P. Hersen, J.M. Di Meglio, Biophys. J. 102(12), 2791 (2012)ADSGoogle Scholar
  64. 64.
    K. Konig, L. Svaasand, Y. Liu, G. Sonek, P. Patrizio, Y. Tadir, M. Berns, B. Tromberg, Cell. Mol. Biol. (Noisy-le-Grand, France) 42(4), 501 (1996)Google Scholar
  65. 65.
    Y. Tadir, W. Wright, O. Vafa, T. Ord, R. Asch, M. Berns, Fertil. Steril. 53, 944 (1990)Google Scholar
  66. 66.
    Z. Teff, Z. Priel, L.A. Gheber, Biophys. J. 92, 1813 (2007)ADSGoogle Scholar
  67. 67.
    S. Chattopadhyay, X.L. Wu, Biophys. J. 96(5), 2023 (2009)ADSGoogle Scholar
  68. 68.
    B. Rodenborn, C.H. Chen, H.L. Swinney, B. Liu, H. Zhang, Proc. Natl. Acad. Sci. 110, E338 (2013)ADSGoogle Scholar
  69. 69.
    G. Batchelor, J. Fluid Mech. 44(03), 419 (1970)MATHMathSciNetADSGoogle Scholar
  70. 70.
    A.T. Chwang, T. Wu, J. Fluid Mech. 67(04), 787 (1975)MATHMathSciNetADSGoogle Scholar
  71. 71.
    J.B. Keller, S.I. Rubinow, J. Fluid Mech. 75(04), 705 (1976)MATHADSGoogle Scholar
  72. 72.
    R.E. Johnson, J. Fluid Mech. 99(02), 411 (1980)MATHMathSciNetADSGoogle Scholar
  73. 73.
    J. Higdon, J. Fluid Mech. 90(04), 685 (1979)MATHMathSciNetADSGoogle Scholar
  74. 74.
    J. Higdon, J. Fluid Mech. 94(02), 331 (1979)MATHMathSciNetADSGoogle Scholar
  75. 75.
    H. Kurtuldu, D. Tam, A. Hosoi, K. Johnson, J. Gollub, Phys. Rev. E 88(1), 013015 (2013)ADSGoogle Scholar
  76. 76.
    S.T. Wereley, C.D. Meinhart, Annu. Rev. Fluid Mech. 42, 557 (2010)ADSGoogle Scholar
  77. 77.
    D. Murphy, D. Webster, J. Yen, Limnol. Oceanogr. Methods 10, 1096 (2012)Google Scholar
  78. 78.
    K. Drescher, R.E. Goldstein, N. Michel, M. Polin, I. Tuval, Phys. Rev. Lett. 105(16), 168101 (2010)ADSGoogle Scholar
  79. 79.
    J.S. Guasto, K.A. Johnson, J.P. Gollub, Phys. Rev. Lett. 105(16), 168102 (2010)ADSGoogle Scholar
  80. 80.
    L.J. Fauci, R. Dillon, Annu. Rev. Fluid Mech. 38, 371 (2006)MathSciNetADSGoogle Scholar
  81. 81.
    S. Suarez, H. Ho, Reprod. Domest. Anim. 38, 119 (2003)Google Scholar
  82. 82.
    E.R. Trueman, Locomotion of Soft-Bodied Animals (Edward Arnold, London, 1975)Google Scholar
  83. 83.
    E. Lauga, Phys. Fluids 19(8), 083104 (2007)MathSciNetADSGoogle Scholar
  84. 84.
    T.D. Montenegro-Johnson, D.J. Smith, D. Loghin, Phys. Fluids (1994–present) 25, 081903 (2013)Google Scholar
  85. 85.
    J.R. Vélez-Cordero, E. Lauga, J. Non-Newtonian Fluid Mech. 199, 37 (2013)Google Scholar
  86. 86.
    D. Katz, R. Mills, T. Pritchett, J. Reprod. Fertil. 53(2), 259 (1978)Google Scholar
  87. 87.
    T. Chaudhury, J. Fluid Mech. 95(01), 189 (1979)MATHMathSciNetADSGoogle Scholar
  88. 88.
    H.C. Fu, C.W. Wolgemuth, T.R. Powers, Phys. Fluids 21(3), 033102 (2009)ADSGoogle Scholar
  89. 89.
    J. Teran, L. Fauci, M. Shelley, Phys. Rev. Lett. 104, 038101 (2010)ADSGoogle Scholar
  90. 90.
    B. Liu, T.R. Powers, K.S. Breuer, Proc. Natl. Acad. Sci. 108, 19516 (2011)ADSGoogle Scholar
  91. 91.
    X. Shen, P.E. Arratia, Phys. Rev. Lett. 106, 208101 (2011)ADSGoogle Scholar
  92. 92.
    N.C. Keim, M. Garcia, P.E. Arratia, Phys. Fluids (1994–present) 24(8), 081703 (2012)Google Scholar
  93. 93.
    S.E. Spagnolie, B. Liu, T.R. Powers, Phys. Rev. Lett. 111, 068101 (2013)ADSGoogle Scholar
  94. 94.
    R.B. Bird, R.C. Armstrong, O. Hassager, Dynamics of Polymeric Liquids. Vol. 1: Fluid Mechanics (Wiley, New York, 1987)Google Scholar
  95. 95.
    R.G. Larson, The Structure and Rheology of Complex Fluids, vol. 4 (Oxford University Press New York, 1999)Google Scholar
  96. 96.
    E.S. Shaqfeh, Annu. Rev. Fluid Mech. 28, 129 (1996)MathSciNetADSGoogle Scholar
  97. 97.
    H.C. Ho, S.S. Suarez, Reproduction 122(4), 519 (2001)Google Scholar
  98. 98.
    D. Katz, T. Bloom, R. Bondurant, Biol. Reprod. 25(5), 931 (1981)Google Scholar
  99. 99.
    L.A. McPartlin, S.S. Suarez, C.A. Czaya, K. Hinrichs, S. Bedford-Guaus, Biol. Reprod. 81, 199 (2009)Google Scholar
  100. 100.
    A. Houry, M. Gohar, J. Deschamps, E. Tischenko, S. Aymerich, A. Gruss, R. Briandet, Proc. Natl. Acad. Sci. 109(32), 13088 (2012)ADSGoogle Scholar
  101. 101.
    S. Yazdi, A.M. Ardekani, Biomicrofluidics 6 (2012)Google Scholar
  102. 102.
    S. Jung, A.G. Winter, A. Hosoi, Int. J. Non-Linear Mech. 46(4), 602 (2011)ADSGoogle Scholar
  103. 103.
    A.G. Winter, R.L. Deits, A.E. Hosoi, J. Exp. Biol. 215, 2072 (2012)Google Scholar
  104. 104.
    G.R. Fulford, D.F. Katz, R.L. Powell, Biorheology 35(4), 295 (1998)Google Scholar
  105. 105.
    M.J. Kim, K.S. Breuer, Small 4(1), 111 (2008)Google Scholar
  106. 106.
    D. Boger, J. Non-Newtonian Fluid Mech. 3(1), 87 (1977)Google Scholar
  107. 107.
    H.C. Fu, T.R. Powers, C.W. Wolgemuth, Phys. Rev. Lett. 99(25), 258101 (2007)ADSGoogle Scholar
  108. 108.
    S.K. Lai, Y.Y. Wang, D. Wirtz, J. Hanes, Adv. Drug Deliv. Rev. 61(2), 86 (2009)Google Scholar
  109. 109.
    S. Brenner, Genetics 77(1), 71 (1974)Google Scholar
  110. 110.
    L. Byerly, R. Cassada, R. Russell, Dev. Biol. 51(1), 23 (1976)Google Scholar
  111. 111.
    X. Shen, J. Sznitman, P. Krajacic, T. Lamitina, P. Arratia, Biophys. J. 102, 2772 (2012)ADSGoogle Scholar
  112. 112.
    F.T. Trouton, Proc. R. Soc. London Ser. A 77, 426 (1906)ADSGoogle Scholar
  113. 113.
    S.L. Anna, G.H. McKinley, J. Rheol. (1978–present) 45(1), 115 (2001)Google Scholar
  114. 114.
    G.H. McKinley, T. Sridhar, Annu. Rev. Fluid Mech. 34, 375 (2002)MathSciNetADSGoogle Scholar
  115. 115.
    P.E. Arratia, C. Thomas, J. Diorio, J.P. Gollub, Phys. Rev. Lett. 96(14), 144502 (2006)ADSGoogle Scholar
  116. 116.
    D.S. Guzick, J.W. Overstreet, P. Factor-Litvak, C.K. Brazil, S.T. Nakajima, C. Coutifaris, S.A. Carson, P. Cisneros, M.P. Steinkampf, J.A. Hill, New England J. Med. 345(19), 1388 (2001)Google Scholar
  117. 117.
    C. Josenhans, S. Suerbaum, Int. J. Med. Microbiol. 291(8), 605 (2002)Google Scholar
  118. 118.
    M. Alexander, Introduction to Soil Microbiology (Wiley, New York, 1991)Google Scholar
  119. 119.
    H.C. Berg, L. Turner, Nature 278, 349 (1979)ADSGoogle Scholar
  120. 120.
    W.R. Schneider, R. Doetsch, J. Bacteriol. 117, 696 (1974)Google Scholar
  121. 121.
    Y. Magariyama, S. Kudo, Biophys. J. 83, 733 (2002)ADSGoogle Scholar
  122. 122.
    H.C. Fu, V.B. Shenoy, T.R. Powers, EPL (Europhys. Lett.) 91(2), 24002 (2010)Google Scholar
  123. 123.
    J. Du, J.P. Keener, R.D. Guy, A.L. Fogelson, Phys. Rev. E 85(3), 036304 (2012)ADSGoogle Scholar
  124. 124.
    S. Nakamura, Y. Adachi, T. Goto, Y. Magariyama, Biophys. J. 90, 3019 (2006)ADSGoogle Scholar
  125. 125.
    A. Leshansky, Phys. Rev. E 80(5), 051911 (2009)ADSGoogle Scholar
  126. 126.
    D. Gagnon, X. Shen, P. Arratia, EPL (Europhys. Lett.) 104(1), 14004 (2013)Google Scholar
  127. 127.
    A. Rodd, D. Dunstan, D. Boger, Carbohydr. Polym. 42, 159 (2000)Google Scholar
  128. 128.
    M. Doi, The Theory of Polymer Dynamics (Oxford university press, Oxford, 1988)Google Scholar
  129. 129.
    D.A. Gagnon, N.C. Keim, X. Shen, P.E. Arratia, Fluid-induced propulsion of rigid particles in wormlike micellar solutions. Phys. Fluids 26, 103101 (2014)ADSGoogle Scholar
  130. 130.
    T. Normand, E. Lauga, Phys. Rev. E 78, 061907 (2008)ADSGoogle Scholar
  131. 131.
    O.S. Pak, T. Normand, E. Lauga, Phys. Rev. E 81, 036312 (2010)ADSGoogle Scholar
  132. 132.
    R. Dreyfus, J. Baudry, M.L. Roper, M. Fermigier, H.A. Stone, J. Bibette, Nature 437(7060), 862 (2005)ADSGoogle Scholar
  133. 133.
    S. Zhou, A. Sokolov, O.D. Lavrentovich, I.S. Aranson, Proc. Natl. Acad. Sci. 111, 1265 (2014)ADSGoogle Scholar
  134. 134.
    P.C. Mushenheim, R.R. Trivedi, H.H. Tuson, D.B. Weibel, N.L. Abbott, Soft Matter 10, 88 (2014)ADSGoogle Scholar
  135. 135.
    A. Kumar, T. Galstian, S.K. Pattanayek, S. Rainville, Mol. Cryst. Liq. Cryst. 574(1), 33 (2013)Google Scholar
  136. 136.
    L.H. Cisneros, R. Cortez, C. Dombrowski, R.E. Goldstein, J.O. Kessler, Exp. Fluids 43(5), 737 (2007)Google Scholar
  137. 137.
    A. Sokolov, I.S. Aranson, Phys. Rev. Lett. 103, 148101 (2009)ADSGoogle Scholar
  138. 138.
    V. Narayan, S. Ramaswamy, N. Menon, Science 317, 105 (2007)ADSGoogle Scholar
  139. 139.
    H. Kurtuldu, J.S. Guasto, K.A. Johnson, J.P. Gollub, Proc. Natl. Acad. Sci. 108(26), 10391 (2011)ADSGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringTechnion-Israel Institute of TechnologyHaifaIsrael
  2. 2.Department of Mechanical Engineering and Applied MechanicsUniversity of PennsylvaniaPhiladelphiaUSA

Personalised recommendations