Mammalian sperm motility: Observation and theory

Annual Review of Fluid Mechanics

Volumn 43, Issue , 2011, Pages 501-528

  Gaffney, E A ^a,c   Gadelha H ^a,c,d   Smith, D J ^b,c,e   Blake, J R ^b,c   Kirkman Brown, J C ^b,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c BIRMINGHAM CHILDREN S HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^d MINISTRY OF EDUCATION OF BRAZIL   (Brazil)

^e UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

flagellum; fluid filament interactions; microswimmer; slender body theory

Indexed keywords

BIOLOGICAL STRUCTURES; CONTINUUM DYNAMICS; FEMALE REPRODUCTIVE TRACT; FLAGELLUM; IN-VIVO; MICRO-SWIMMER; MODELING CAPABILITIES; SLENDER-BODY THEORY; SPECIALIZED CELLS; SPERM MOTILITY; SYNERGISTIC COMBINATIONS; THEORETICAL STUDY;

ECOLOGY; FLUIDS; MAMMALS;

MECHANICS;

CONTINUUM MECHANICS; FLAGELLATE; FLUID DYNAMICS; INFERTILITY; MOTILITY; SPERMATOPHORE; THEORETICAL STUDY;

ANIMALIA; MAMMALIA;

EID: 79951990947     PISSN: 00664189     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-fluid-121108-145442     Document Type: Article

References (156)

1. Antman S. 2005. Non-Linear Problems of Elasticity. New York: Springer
2. Austin CR. 1995. Evolution of human gametes: spermatozoa. See Grudzinskas & Yovich 1995, pp. 1-19
3. Baba SA, Mogami Y. 1985. An approach to digital image analysis of bending shapes of eukaryotic flagella and cilia. Cell Motil. Cytoskelet. 5(6):475-89
4. Baltz JM, Katz DF, Cone RA. 1988. Mechanics of sperm-egg interaction at the zona pellucida. Biophys. J. 54:643-54
5. Baltz JM, Williams PO, Cone RA. 1990. Dense fibers protect mammalian sperm against damage. Biol. Reprod. 43:485-91 (Pubitemid 20289498)
6. Barratt CLR, Kay V, Oxenham SK. 2009. The human spermatozoon: a stripped down but refined machine. J. Biol. 8:63
7. Barratt CLR, Kirkman-Brown J. 2006. Man-made versus female-made environment: Will the real capacitation please stand upHum. Reprod. Update 12:1-2 (Pubitemid 43013741)
8. Bedford JM. 1998. Mammalian fertilization misreadSperm penetration of the eutherian zona pellucida is unlikely to be a lytic event. Biol. Reprod. 59:1275-87 (Pubitemid 28549839)
9. Berke AP, Turner L, Berg HC, Lauga E. 2006. Hydrodynamic attraction of swimming microorganisms by surfaces. Phys. Rev. Lett. 101:038102
10. Blake JR. 1971. A note on the image system for a stokeslet in a no slip boundary. Proc. Camb. Philos. Soc. 70:303-10
11. Brennen C, Winet H. 1977. Fluid mechanics of propulsion by cilia and flagella. Annu. Rev. Fluid Mech. 9:339-98
12. Brokaw CJ. 1966. Effects of increased viscosity on the movements of some invertebrate spermatozoa. J. Exp. Biol. 45:113-39
13. Brokaw CJ. 1971. Bend propagation by a sliding filament model for flagella. J. Exp. Biol. 55:289-304
14. Brokaw CJ. 1972. Computer simulation of flagellar movement I. Demonstration of stable bend propagation and bend initiation by the sliding filament model. Biophys. J. 12:564-86
15. Brokaw CJ. 1975. Molecular mechanism for oscillation in flagella and muscle. Proc. Natl. Acad. Sci. USA 72:3102-6
16. Brokaw CJ. 1984. Automated methods for estimation of sperm flagellar bending parameters. Cell Motil. Cytoskelet. 4:417-30 (Pubitemid 15178400)
17. Brokaw CJ. 1994. Control of flagellar bending: a new agenda based on dynein diversity. Cell Motil. Cytoskelet. 28:199-204 (Pubitemid 24216011)
18. Brokaw CJ. 1999. Computer simulation of flagellar movement: VII. Conventional but functionally different cross-bridge models for inner and outer arm dyneins can explain the effects of outer arm removal. Cell Motil. Cytoskelet. 42:134-48 (Pubitemid 29142958)
19. Brokaw CJ. 2002. Computer simulation of flagellar movement VIII: Coordination of dynein by local curvature control can generate helical bending waves. Cell Motil. Cytoskelet. 53:103-24
20. Brokaw CJ. 2003. Swimming with three-dimensional flagellar bending waves. Presented at Int. Symp. Aqua-Biomech., 2nd, Honolulu, HI
21. Brokaw CJ. 2008. Thinking about flagellar oscillation. Cell Motil. Cytoskelet. 66:425-36
22. Brokaw CJ. 2009. Simulation of cyclic dynein-driven sliding, splitting, and reassociation in an outer doublet pair. Biophys. J. 97:2939-47
23. Burkman LJ. 1995. The motility of human spermatozoa before and after capacitation. See Grudzinskas & Yovich 1995, pp. 122-39
24. Camalet S, Julicher F. 2000. Generic aspects of axonemal beating. New J. Phys. 2:24
25. Childress S. 1981. Mechanics of Swimming and Flying. New York: Cambridge Univ. Press
26. Cortez R. 2001. The method of regularized stokeslets. SIAM J. Sci. Comput. 23:1204-25
27. CortezR, Fauci L, Cowen N,Dillon R. 2004. Simulationof swimming organisms: coupling internal mechanics with external fluid dynamics. Comput. Sci. Eng. 6:38-45
28. Cosson J, Huitorel P, Gagnon C. 2003. How spermatozoa come to be confined to surfaces. Cell Motil. Cytoskelet. 54:56-63 (Pubitemid 36033838)
29. Croxatto HB. 1995. Gamete transport. In Reproductive Endocrinology, Surgery and Technology, ed. J Adashi, Z Rosenwaks, pp. 395-98. New York: Raven
30. Croxatto HB. 2002. Physiology of gamete and embryo transport through the fallopian tube. Reprod. Biomed. Online 4:160-69
31. Cummings LM, Katz DF, Overstreet J, Hanson F. 1984. Sperm interactions in the penetration of cervical mucus. Proc. Am. Soc. Androl. 5:27
32. Cummins JM, Woodall PF. 1985. On mammalian sperm dimensions. J. Reprod. Fertil. 75:153-75 (Pubitemid 16253401)
33. Curry MR, Watson PF. 1995. Evolution of human gametes: spermatozoa. See Grudzinskas & Yovich 1995, pp. 45-69
34. Dam AHDM, Feenstra I, Westphal JR, Ramos L, van Golde RJT, Kremer JAM. 2007. Globozoospermia revisited. Hum. Reprod. Update 67:723-32
35. Dillon RH, Fauci LJ, Omoto C. 2003a. Mathematical modeling of axoneme mechanics and fluid dynamics in ciliary and sperm motility. Dyn. Contin. Discrete Impuls. Syst. A Math. Anal. 10:745-52
36. Dillon RH, Fauci LJ, Omoto C, Yang XZ. 2003b. Fluid dynamic models of flagellar and ciliary beating. Ann. N.Y. Acad. Sci. 1101:495-504
37. Dresdner RD, Katz DF. 1981. Relationships of mammalian sperm motility and morphology to hydrodynamic aspects of cell function. Biol. Reprod. 25:920-30 (Pubitemid 12139002)
38. Drobnis EZ, Yudin AI, Cherr GN, Katz DF. 1988. Kinematics of hamster sperm during penetration of the cumulus cell matrix. Gamete Res. 21:367-83 (Pubitemid 19185284)
39. Elfring GJ, Pak OS, Lauga E. 2010. Two-dimensional flagellar synchronization in viscoelastic fluids. J. Fluid Mech. 646:505-15
40. Fauci LJ, Dillon R. 2006. Biofluidmechanics of reproduction. Annu. Rev. Fluid Mech. 38:271-394
41. Fauci LJ, McDonald A. 1995. Sperm motility in the presence of boundaries. Bull. Math. Biol. 57:679-99
42. Fawcett DW. 1975. The mammalian sperm. Dev. Biol. 44:394-436
43. Fawcett DW. 1981. The Cell. Amsterdam: Elsevier Health Sci.
44. Florman HM, Jungnickel MK, Sutton KA. 2007. What can we learn about fertilization from cystic fibrosisProc. Natl. Acad. Sci. USA 104(27):11123-24 (Pubitemid 47175104)
45. Friedrich BM, Riedel-Kruse IH, Howard J, Julicher F. 2010. High-precision tracking of sperm swimming fine structure provides strong test of resistive force theory. J. Exp. Biol. 213:1226-34
46. Ford WCL. 2006. Glycolysis and sperm motility: Does a spoonful of sugar help the flagellum go roundHum. Reprod. Update 112:269-74
47. Fu HC, Wolgemuth CW, Powers TR. 2008. Beating patterns of filaments in viscoelastic fluids. Phys. Rev. E 78:041913
48. Fulford GR, Katz DF, Powell RL. 1999. Swimming of spermatozoa in a linear viscoelastic fluid. Biorheology 35:295-309
49. Gadêlha H, Gaffney EA, Smith DJ, Kirkman-Brown JC. 2010. Migrating the model: Non-linear instabilities in flagellar dynamics may affect cell behaviour. J. R. Soc. Int. In press; doi: 10.1098/rsif.2010.0136
50. Gillies E, Cannon RM, Green RB, Pacey AA. 2009. Hydrodynamic propulsion of human sperm. J. Fluid Mech. 625:445-74
51. Gray J, Hancock GJ. 1955. The propulsion of sea urchin spermatozoa. J. Exp. Biol. 32:802-14
52. Green DPL. 1988. Sperm thrusts and the problem of penetration. Biol. Rev. 63:79-105
53. Grudzinskas JG, Yovich JL, eds 1995 Gametes: The Spermatozoon. Cambridge, UK: Cambridge Univ. Press
54. Gueron S, Levit-Gurevich K, Liron N, Blum J. 1997. Cilia internal mechanism and metachronal coordination as the result of hydrodynamical coupling. Proc. Natl. Acad. Sci. USA 94:6001-6 (Pubitemid 27270625)
55. Hancock GJ. 1953. The self-propulsion of microscopic organisms through liquids. Proc. R. Soc. Lond. A 217:96-121
56. Hilfinger A, Chattopadhyay AK, Julicher F. 2009. Nonlinear dynamics of cilia and flagella. Phys. Rev. E. 79:051918
57. Hines M, Blum JJ. 1978. Bend propagation in flagella I. Derivation of equations of motion and their simulation. Biophys. J. 23:41-57 (Pubitemid 8378707)
58. Hines M, Blum JJ. 1979. Bend propagation in flagella II. Incorporation of dynein cross-bridge kinetics into the equations of motion. Biophys. J. 25:421-42
59. Hines M, Blum JJ. 1983. Three-dimensional mechanics of eukaryotic flagella. Biophys. J. 41:67-79 (Pubitemid 13114322)
60. Hines M, Blum JJ. 1984. On the contribution of moment-bearing links to bending and twisting in a three-dimensional sliding filament model. Biophys. J. 46:559-65
61. Hines M, Blum JJ. 1985. On the contribution of dynein-like activity to twisting in a three-dimensional sliding filament model. Biophys. J. 47:705-8 (Pubitemid 15004609)
62. Hsu C, Dillon RH. 2009. A 3D motile rod-shaped monotrichous bacterial model. Bull. Math. Biol. 71:1228-63
63. Hunter RHF. 1995. Human sperm reservoirs and Fallopian tube function: a role for the intra-mural portionActa Obstet. Gynaecol. Scand. 74:677-81
64. Ierardi V, Niccolini A, Alderighi M, Gazzano A, Martelli F, Roberto S. 2008. AFM characterization of rabbit spermatozoa. Microsc. Res. Tech. 71:529-35 (Pubitemid 351991098)
65. Immler S, Moore HDM, Breed WG, Birkhead TR. 2007. By hook or by crookMorphometry, competition and cooperation in rodent sperm. PLoS One 2(1):e170
66. Johnson RE. 1980. An improved slender-body theory for Stokes flow. J. Fluid Mech. 99:411-31
67. Johnson RE, Brokaw CJ. 1979. Flagellar hydrodynamics: a comparison between resistive-force theory and slender-body theory. Biophys. J. 25:113-27 (Pubitemid 9107850)
68. Julicher F, Prost J. 1997. Spontaneous oscillations of collective molecular motors. Phys. Rev. Lett. 78:4510-13 (Pubitemid 127655536)
69. Katz DF, Drobnis EZ, Overstreet JW. 1989. Factors regulating mammalian sperm migration through the female reproductive tract and oocyte vestments. Gamete Res. 22:443-69 (Pubitemid 19187919)
70. Katz DF, Pedrotti L. 1977. Geotaxis by motile spermatozoa: hydrodynamic reorientation. J. Theor. Biol. 13:63-75
71. Katz DF, Phillips DM. 1986. The response of rhesus monkey sperm motility to cervical mucus and solid surfaces. Gamete Res. 13:231-39 (Pubitemid 16168364)
72. Katz DF, Yanagimachi R. 1980. Movement characteristics of hamster spermatozoa within the oviduct. Biol. Reprod. 22:759-64 (Pubitemid 10055072)
73. Kido A, Togashi K, Kataoka ML, Nakai A, Koyama T, Fujii S. 2008. Intrauterine devices and uterine peristalsis: evaluation with MRI. Magn. Reson. Imaging 26:54-58 (Pubitemid 350299731)
74. Kim E, Yamashita M, Kimura M, Honda A, Kashiwabara S, Baba T. 2008. Sperm penetration through cumulus mass and zona pellucida. Int. J. Dev. Biol. 52:677-82
75. Kinukawa M, Ohmuro J, Baba S, Murashige S, Okuno M, et al. 2005. Analysis of flagellar bending in hamster spermatozoa: characterization of an effective stroke. Reproduction 72:1269-74 (Pubitemid 41698618)
76. Kunz G, Beil D, Deininger H, Wildt L, Leyendecker G. 1996. The dynamics of rapid sperm transport through the female genital tract: evidence from vaginal sonography of uterine peristalsis and hysteros-alpingoscintigraphy. Hum. Reprod. 11:627-32 (Pubitemid 26126092)
77. Kunz G, Beil D, Huppert P, Leyendecker G. 2007. Oxytocin: a stimulator of directed sperm transport in humans. Reprod. Biomed. Online 14(1):32-39 (Pubitemid 46156561)
78. Lai SK, Wang Y, Wirtz D, Hanes J. 2009. Micro-and macrorheology of mucus. Adv. Drug Deliv. Rev. 61:86-100
79. Lauga E, Powers TR. 2009. The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72:096601
80. Leisch KA, Pelle DW, Dominic W, Lindemann CB. 2008. Insights into the mechanism of ADP action on flagellar motility derived from studies on bull sperm. Biophys. J. 95:472-82
81. Lighthill J. 1976. Flagellar hydrodynamics: JV Neumann lecture. SIAM Rev. 18:161-230
82. Lin Y, Mahan K, Lathrop WE, Myles DG, Primakoff P. 1994. A hyaluronidase activity of the sperm plasma membrane protein ph-20 enables sperm to penetrate the cumulus cell layer surrounding the egg. J. Cell Biol. 125:1157-63 (Pubitemid 24177217)
83. Lindemann CB. 1994a. A geometric clutch hypothesis to explain oscillations of the axoneme of cilia and flagella. J. Theor. Biol. 168:175-89
84. Lindemann CB. 1994b. A model of flagellar and ciliary functioning which uses the forces transverse to the axoneme as the regulator of dynein activation. Cell Motil. Cytoskelet. 29:141-54 (Pubitemid 24303013)
85. Lindemann CB. 1996. Functional significance of the outer dense fibers of mammalian sperm examined by computer simulations with the geometric clutch model. Cell Motil. Cytoskelet. 34:258-70 (Pubitemid 26269743)
86. Lindemann CB. 2002. Geometric clutch model version 3: the role of the inner and outer arm dyneins in the ciliary beat. Cell Motil. Cytoskelet. 52:242-54 (Pubitemid 34803844)
87. Lindemann CB. 2004. Testing the geometric clutch hypothesis. Biol. Cell 96:681-90 (Pubitemid 39618875)
88. Lindemann CB. 2009. Heart of the beat (the flagellar beat, that is). Biophys. J. 97:2865-66
89. Lindemann CB, Leisch KA. 2010. Flagellar and ciliary beating: the proven and the possible. J. Cell Sci. 123:519-28
90. Lindemann CB, Mitchell DR. 2007. Evidence for axonemal distortion during the flagellar beat of chlamy-domonas. Cell Motil. Cytoskelet. 64:580-89 (Pubitemid 47106163)
91. Lindemann CB, Orlando A, Kanous KS. 1992. The flagellar beat of rat sperm is organized by the interaction of two functionally distinct populations of dynein bridges with a stable central axonemal partition. J. Cell Sci. 102:249-60
92. Liron N. 2001. The LGL (Lighthill-Gueron-Liron) theorem: historical perspective and critique. Math. Meth. Appl. Sci. 24:1533-40
93. Lopez-Garcia MDC, Monson RL, Haubert K, Wheeler MB, Beebe DJ. 2008. Sperm motion in a microfluidic fertilization device. Biomed. Microdevices 10:709-18
94. Machin KE. 1958. Wave propagation along flagella. J. Exp. Biol. 35:796-806
95. Mitchison TJ, Mitchison HM. 2010. How cilia beat. Nature 463:308-9
96. Mitran SM. 2007. Metachronal wave formation in a model of pulmonary cilia. Comput. Struct. 85:763-74 (Pubitemid 46719353)
97. Murase M, Hines M, Blum JJ. 1989. Properties of an excitable dynein model for bend propagation in cilia and flagella. J. Theor. Biol. 139:413-30
98. Nakanishi T, Isotani A, Yamaguchi R, Ikawa M, Baba T, et al. 2004. Selective passage through the uterotubal junction of sperm from a mixed population produced by chimeras of calmegin-knockout and wild-type male mice. Biol. Reprod. 71:959-65 (Pubitemid 39108659)
99. Nascimento JM, Shi LZ, Tam J, Chandsawangbhuwana C, Durrant B, et al. 2008. Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J. Cell. Physiol. 217:745-51
100. Normand T, Lauga E. 2008. Flapping motion and force generation in a viscoelastic fluid. Phys. Rev. E78:061907
101. Ohmuro J, Ishijima S. 2006. Hyperactivation is the mode conversion from constant-curvature beating to constant-frequency beating under a constant rate of microtubule sliding. Mol. Reprod. Dev. 73:1412-21 (Pubitemid 44423730)
102. Okuno M, Asai DJ, Ogawa K, Brokaw CJ. 1981. Effects of antibodies against dynein and tubulin on the stiffness of flagellar axonemes. J. Cell Biol. 91:689-94 (Pubitemid 12211158)
103. Oldroyd JG. 1950. On the formulation of rheological equations of state. Proc. R. Soc. Lond. A 200:523-41
104. Olson GE, Linck RW. 1977. Observations of the structural components of flagellar axonemes and central pair microtubules from rat sperm. J. Ultrastruct. Res. 61:21-43 (Pubitemid 8204366)
105. Olson SD, Suarez SS, Fauci LJ. 2010. A model of CatSper channel mediated calcium dynamics in mammalian spermatozoa. Bull. Math. Biol. In press; doi: 10.1007/s11538-010-9516-5
106. Pedley TJ, Kessler JO. 1992. Hydrodynamic phenomena in suspensions of swimming microorganisms. Annu. Rev. Fluid Mech. 24:313-58
107. Pelle DW, Brokaw CJ, Lesich KA, Lindemann CB. 2009. Mechanical properties of the passive sea urchin sperm flagellum. Cell Motil. Cytoskelet. 66:721-35
108. Powers TR. 2010. Dynamics of filaments and membranes in a viscous fluid. Rev. Mod. Phys. 82:1607-31
109. Pozrikidis C. 2002. A Practical Guide to Boundary Element Methods with the Software Library BEMLIB. Boca Raton, FL: CRC
110. Purcell EM. 1977. Life at low Reynolds number. Am. J. Phys. 45:3-11
111. Riedel-Kruse IH, Hilfinger A, Howard J, Julicher F. 2007. How molecular motors shape the flagellar beat. HFSP J. 1:192-208
112. Rikmenspoel R. 1965. The tail movement of bull spermatozoa: observations and model calculations. Biophys. J. 5:365-92
113. Rikmenspoel R. 1984. Movements and active moments of bull sperm flagella as a function of temperature and viscosity. J. Exp. Biol. 108:205-30
114. Rothschild L. 1963. Non-random distribution of bull spermatozoa in a drop of sperm suspension. Nature 198:1221-22
115. Sale WS, Satir P. 1977. Direction of active sliding of microtubules in tetrahymena cilia. Proc. Natl. Acad. Sci. USA 74:2045-49 (Pubitemid 8123606)
116. Schmitz-Leisch KA, Lindemann CB. 2004. Direct measurement of the passive stiffness of rat sperm and implications to the mechanism of the calcium response. Cell Motil. Cytoskelet. 59:169-79 (Pubitemid 39435200)
117. Seo D, Agca Y, Feng ZC, Critser JK. 2007. Development of sorting, aligning, and orienting motile sperm using microfluidic device operated by hydrostatic pressure. Microfluid. Nanofluid. 3:561-70 (Pubitemid 47249362)
118. Shao B, Shi LZ, Nascimento JM, Botvinick EL, Ozkan M, et al. 2007. High-throughput sorting and analysis of human sperm with a ring-shaped laser trap. Microfluid. Nanofluid. 3:561-70
119. Shum H, Gaffney EA, Smith DJ. 2010. Modelling bacterial behaviour close to a no-slip plane boundary: the influence of bacterial geometry. Proc. R. Soc. Lond. A 466:1725-48
120. Sleigh MA. 1991. Hydrodynamic propulsion of human sperm. Protoplasma 164:45-53
121. Smith DJ, Blake JR. 2009. Surface accumulation of spermatozoa: a fluid dynamic phenomenon. Math. Sci. 34:74-87
122. Smith DJ, Gaffney EA, Blake JR. 2007. Discrete cilia modelling with singularity distributions: application to the embryonic node and the airway surface liquid. Bull. Math. Biol. 69:1477-510 (Pubitemid 46955663)
123. Smith DJ, Gaffney EA, Blake JR. 2009a. Mathematical modelling of cilia-driven transport of biological fluids. Proc. R. Soc. Lond. A 465:2417-29
124. Smith DJ, Gaffney EA, Blake JR, Kirkman-Brown JC. 2009b. Human sperm accumulation near surfaces: a simulation study. J. Fluid Mech. 621:289-320
125. Smith DJ, Gaffney EA, Gadêlha H, Kapur N, Kirkman-Brown JC. 2009c. Bend propagation in the flagella of migrating human sperm, and its modulation by viscosity. Cell Motil. Cytoskelet. 66:220-36
126. Sobrero A, MacLeod J. 1962. The immediate postcoital test. Fertil. Steril. 13:184-89
127. Spagnolie SE, Lauga E. 2010. The optimal elastic flagellum. Phys. Fluids. 22:081902
128. Steptoe PC, Edwards RG. 1978. Birth after reimplantation of a human embryo. Lancet 38:366
129. Storey BT. 2008. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int. J. Dev. Biol. 52:427-37
130. Suarez SS. 2002. Gamete transport. In Fertilization, ed. DM Hardy, pp. 3-28. New York: Academic
131. Suarez SS. 2008. Control of hyperactivation in sperm. Hum. Reprod. Update 14:647-57
132. Suarez SS. 2010. How do sperm get to the eggBioengineering expertise needed! Exp. Mech. In press; doi: 10.1007/s11340-009-9312-z
133. Suarez SS, Dai X. 1992. Hyperactivation enhances mouse sperm capacity for penetrating viscoelastic media. Biol. Reprod. 46(4):686-91
134. Suarez SS, Pacey AA. 2006. Sperm transport in the female reproductive tract. Hum. Reprod. Update 12:23-37 (Pubitemid 43013744)
135. Takao D, Kamimura S. 2008. FRAP analysis of molecular diffusion inside sea-urchin spermatozoa. J. Exp. Biol. 211:3594-600
136. Tam D. 2008. Motion at low Reynolds number. PhD thesis. Mass. Inst. Technol.
137. Taylor GI. 1951. Analysis of the swimming of microscopic organisms. Proc. R. Soc. Lond. A 209:447-61
138. Taylor GI. 1952. The action of waving cylindrical tails in propelling microscopic organisms. Proc. R. Soc. Lond. A 211:225-39
139. Taylor GI. 1960. G.I. Taylor's film clip illustrating the hydrodynamic reversibility of viscous flows. Available at http://www.physics.nyu.edu/pine/ research/hydroreverse.html
140. 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
141. Turner RM. 2003. Tales from the tail: What do we really know about sperm motilityJ. Androl. 24(6):790-803 (Pubitemid 37370531)
142. Vernon GG, Woolley DM. 2004. Basal sliding and the mechanics of oscillation in a mammalian sperm flagellum. Biophys. J. 87:3934-44 (Pubitemid 39602899)
143. Williams M, Hill CJ, Scudamore I, Dunphy B, Cooke ID, Barratt CLR. 1993. Sperm numbers and distribution within the human fallopian tube around ovulation. Hum. Reprod. 8:2019-26 (Pubitemid 24012796)
144. Winet H, Bernstein GS, Head J. 1984. Observations on the response of human spermatozoa to gravity, boundaries and fluid shear. J. Reprod. Fertil. 70:511-23 (Pubitemid 14157722)
145. Wolf DP, Blasco L, Khan MA, Litt M. 1978. Human cervical mucus. IV. Viscoelasticity and sperm penetrability during ovulatory menstrual cycle. Fertil. Steril. 30(2):163-69 (Pubitemid 8383001)
146. Woolley DM. 2003. Motility of spermatozoa at surfaces. Reproduction 126:259-70 (Pubitemid 36987170)
147. Woolley DM. 2007. A novel motility pattern in quail spermatozoa with implications for the mechanism of flagellar beating. Biol. Cell 99:663-75 (Pubitemid 350201917)
148. Woolley DM, Carter DA, Tilly GN. 2008. Compliance in the neck structures of the guinea pig spermatozoon, as indicated by rapid freezing and electron microscopy. J. Anatomy 213:336-41
149. Woolley DM, Crockett RF, Groom WDI, Revell SG. 2009. A study of synchronisation between the flagella of bull spermatozoa, with related observations. J. Exp. Biol. 212:2215-23
150. Woolley DM, Vernon GG. 2001. A study of helical and planar waves on sea urchin sperm flagella, with a theory of how they are generated. J. Exp. Biol. 204:1333-45 (Pubitemid 34853552)
151. Yanagimachi R. 1994. Mammalian fertilization. In The Physiology of Reproduction, ed. E Knobil, JD Neil, pp. 189-317. New York: Raven
152. Yaniv S, Jaffa A, Eytan O, Elad D. 2009. Simulation of embryo transport in a closed uterine cavity model. Eur. J. Obstet. Gynecol. Reprod. Biol. 144:50-60
153. Yeung WSB, Ng VKH, Lay EYL, Ho PC. 1994. Human oviductal cells and their conditioned medium maintain the motility and hyperactivation of human spermatozoa in vitro. Hum. Reprod. 9:656-60 (Pubitemid 24132343)
154. Youngren GK, Acrivos A. 1975. Stokes flow past a particle of arbitrary shape: numerical method of solution. J. Fluid Mech. 69:377-403
155. Yudin AI, Hanson FW, Katz DF. 1989. Human cervical mucus and its interaction with sperm: a fine-structural view. Biol. Reprod. 40:661-71 (Pubitemid 19149772)
156. Yundt AP, Shack WJ, Lardner TJ. 1975. Applicability of hydrodynamic analyses of spermatozoan motion. J. Exp. Biol. 62:27-41