1932

Abstract

The term “bioconvection” describes hydrodynamic instabilities and patterns in suspensions of biased swimming microorganisms. Hydrodynamic instabilities arise from coupling between cell swimming behaviors; physical properties of the cells, such as density; and fluid flows. For instance, a combination of viscous and gravitational torques can lead to cells swimming toward downwelling fluid. If the cells are more dense than the fluid, then a gyrotactic instability results. Phototaxis describes the directed response of cells to light, which can also lead to instability. Bioconvection represents a classic system where macroscopic phenomena arise from microscopic cellular behavior in relatively dilute systems. There are ecological consequences for bioconvection and the mechanisms involved as well as potential for industrial exploitation. The focus of this review is on progress measuring and modeling gyrotactic and phototactic bioconvection. It builds on two earlier reviews of bioconvection and recent interest in active matter, describing progress and highlighting open problems.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-fluid-010518-040558
2020-01-05
2024-06-17
Loading full text...

Full text loading...

/deliver/fulltext/fluid/52/1/annurev-fluid-010518-040558.html?itemId=/content/journals/10.1146/annurev-fluid-010518-040558&mimeType=html&fmt=ahah

Literature Cited

  1. Abe T, Nakamura S, Kudo S 2017. Bioconvection induced by bacterial chemotaxis in a capillary assay. Biochem. Biophys. Res. Commun. 483:277–82
    [Google Scholar]
  2. Almahmud RAJ 2016. Wavelengths in bioconvection patterns PhD Thesis, Univ. Glasgow Glasgow:
    [Google Scholar]
  3. Alqarni MS, Bearon RN 2016. Transport of helical gyrotactic swimmers in channels. Phys. Fluids 28:071904
    [Google Scholar]
  4. Anderson DM, Cembella AD, Hallegraeff GM 2012. Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Annu. Rev. Mar. Sci. 4:143–76
    [Google Scholar]
  5. Ardekani MN, Sardina G, Brandt L, Karp-Boss L, Bearon RN, Variano EA 2017. Sedimentation of elongated non-motile prolate spheroids in homogenous isotropic turbulence. J. Fluid Mech. 831:655–74
    [Google Scholar]
  6. Bearon RN 2003. An extension of generalized Taylor dispersion in unbounded homogeneous shear flows to run-and-tumble chemotactic bacteria. Phys. Fluids 15:1552–63
    [Google Scholar]
  7. Bearon RN 2013. Helical swimming can provide robust upwards transport for gravitactic single-cell algae; a mechanistic model. J. Math. Biol. 66:1341–59
    [Google Scholar]
  8. Bearon RN, Bees MA, Croze OA 2012. Biased swimming cells do not disperse in pipes as tracers: a population model based on microscale behaviour. Phys. Fluids 24:121902
    [Google Scholar]
  9. Bearon RN, Grunbaum D 2006. Bioconvection in a stratified environment: experiments and theory. Phys. Fluids 18:127102
    [Google Scholar]
  10. Bearon RN, Hazel AL 2015. The trapping in high-shear regions of slender bacteria undergoing chemotaxis in a channel. J. Fluid Mech. 771:R3
    [Google Scholar]
  11. Bearon RN, Hazel AL, Thorn GJ 2011. The spatial distribution of gyrotactic swimming micro-organisms in laminar flow fields. J. Fluid Mech. 680:602–35
    [Google Scholar]
  12. Bees MA 1996. Non-linear pattern generation by swimming micro-organisms PhD Thesis, Univ. Leeds Leeds:
    [Google Scholar]
  13. Bees MA, Croze OA 2010. Dispersion of biased swimming micro-organisms in a fluid flowing through a tube. Proc. R. Soc. A Math. Phys. Eng. Sci. 466:2057–77
    [Google Scholar]
  14. Bees MA, Croze OA 2014. Mathematics for streamlined biofuel production from unicellular algae. Biofuels 5:53–65
    [Google Scholar]
  15. Bees MA, Hill NA 1997. Wavelengths of bioconvection patterns. J. Exp. Biol. 200:1515–26
    [Google Scholar]
  16. Bees MA, Hill NA 1998. Linear bioconvection in a suspension of randomly swimming, gyrotactic micro-organisms. Phys. Fluids 10:1864–81
    [Google Scholar]
  17. Bees MA, Hill NA 1999. Non-linear bioconvection in a deep suspension of gyrotactic swimming micro-organisms. J. Math. Biol. 38:135–68
    [Google Scholar]
  18. Bees MA, Hill NA, Pedley TJ 1998. Analytical approximations for the orientation distribution of small dipolar particles in steady shear flows. J. Math. Biol. 36:269–98
    [Google Scholar]
  19. Bennett RR, Golestanian R 2015. A steering mechanism for phototaxis in chlamydomonas. J. R. Soc. Interface 12:20141164
    [Google Scholar]
  20. Cencini M, Franchino M, Santamaria E, Boffetta G 2016. Centripetal focusing of gyrotactic phytoplankton. J. Theor. Biol. 399:62–70
    [Google Scholar]
  21. Chakraborty S, Ivancic F, Solovchuk M, Sheu TW-S 2018. Stability and dynamics of a chemotaxis system with deformed free-surface in a shallow chamber. Phys. Fluids 30:071904
    [Google Scholar]
  22. Chertock A, Fellner K, Kurganov A, Lorz A, Markowich PA 2012. Sinking, merging and stationary plumes in a coupled chemotaxis-fluid model: a high-resolution numerical approach. J. Fluid Mech. 694:155–90
    [Google Scholar]
  23. Childress S, Levandowsky M, Spiegel EA 1975. Pattern formation in a suspension of swimming micro-organisms: equations and stability theory. J. Fluid Mech. 69:595–613
    [Google Scholar]
  24. Clifton W, Bearon R, Bees MA 2018. Enhanced sedimentation of elongated plankton in simple flows. IMA J. Appl. Math. 83:743–66
    [Google Scholar]
  25. Colabrese S, Gustavsson K, Celani A, Biferale L 2017. Flow navigation by smart microswimmers via reinforcement learning. Phys. Rev. Lett. 118:158004
    [Google Scholar]
  26. Cortez R, Fauci L, Medovikov A 2005. The method of regularized Stokeslets in three dimensions: analysis, validation, and application to helical swimming. Phys. Fluids 17:031504
    [Google Scholar]
  27. Croze OA, Ashraf EE, Bees MA 2010. Sheared bioconvection in a horizontal tube. Phys. Biol. 7:046001
    [Google Scholar]
  28. Croze OA, Bearon RN, Bees MA 2017. Gyrotactic swimmer dispersion in pipe flow: testing the theory. J. Fluid Mech. 816:481–506
    [Google Scholar]
  29. Croze OA, Martinez VA, Jakuszeit T, Dell'Arciprete D, Poon WC, Bees MA 2019. Helical and oscillatory microswimmer motility statistics from differential dynamic microscopy. New J. Phys. 21:6063012
    [Google Scholar]
  30. Croze OA, Sardina G, Ahmed M, Bees MA, Brandt L 2013. Dispersion of swimming algae in laminar and turbulent channel flows: consequences for photobioreactors. J. R. Soc. Interface 10:20121041
    [Google Scholar]
  31. Czirok A, Janosi IM, Kessler JO 2000. Bioconvective dynamics: dependence on organism behaviour. J. Exp. Biol. 203:3345–54
    [Google Scholar]
  32. Daniels R, Vanderleyden J, Michiels J 2004. Quorum sensing and swarming migration in bacteria. FEMS Microbiol. Rev. 28:261–89
    [Google Scholar]
  33. Delcourt J, Bode NWF, Denoel M 2016. Collective vortex behaviors: diversity, proximate, and ultimate causes of circular animal group movements. Q. Rev. Biol. 91:1–24
    [Google Scholar]
  34. Demetsmets R, Tomson A, Stegwee D, Van den Ende H 1990. Cell-cell coordination in conjugating Chlamydomonas gametes. Protoplasma 155:188–99
    [Google Scholar]
  35. Denissenko P, Lukaschuk S 2007. Velocity profiles and discontinuities propagation in a pipe flow of suspension of motile microorganisms. Phys. Lett. A 362:298–304
    [Google Scholar]
  36. Dervaux J, Resta MC, Brunet P 2017. Light-controlled flows in active fluids. Nat. Phys. 13:306–13
    [Google Scholar]
  37. Desai N, Ardekani AM 2017. Modeling of active swimmer suspensions and their interactions with the environment. Soft Matter 13:6033–50
    [Google Scholar]
  38. Diehn B, Feinleib M, Haupt W, Hildebrand E, Lenci F, Nultsch W 1977. Terminology of behavioral responses of motile microorganisms. Photochem. Photobiol. 26:559–60
    [Google Scholar]
  39. Drescher K, Goldstein RE, Michel N, Polin M, Tuval I 2010. Direct measurement of the flow field around swimming microorganisms. Phys. Rev. Lett. 105:168101
    [Google Scholar]
  40. Dunkel J, Heidenreich S, Drescher K, Wensink HH, Bär M, Goldstein RE 2013. Fluid dynamics of bacterial turbulence. Phys. Rev. Lett. 110:228102
    [Google Scholar]
  41. Durham WM, Climent E, Barry M, Lillo FD, Boffetta G, et al 2013. Turbulence drives microscale patches of motile phytoplankton. Nat. Commun. 4:2148
  42. Durham WM, Kessler JO, Stocker R 2009. Disruption of vertical motility by shear triggers formation of thin phytoplankton layers. Science 323:1067–70
    [Google Scholar]
  43. Elias S, Banin E 2012. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol. Rev. 36:990–1004
    [Google Scholar]
  44. Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S 2016. Biofilms: an emergent form of bacterial life. Nat. Rev. Microbiol. 14:563–75
    [Google Scholar]
  45. Garcia X, Rafaï S, Peyla P 2013. Light control of the flow of phototactic microswimmer suspensions. Phys. Rev. Lett. 110:138106
    [Google Scholar]
  46. Gentien P, Lunven M, Lazure P, Youenou A, Crassous MP 2007. Motility and autotoxicity in Karenia mikimotoi (Dinophyceae). Philos. Trans. R. Soc. B Biol. Sci. 362:1937–46
    [Google Scholar]
  47. Ghorai S 2016. Gyrotactic trapping: a numerical study. Phys. Fluids 28:041901
    [Google Scholar]
  48. Ghorai S, Hill NA 2000. Periodic arrays of gyrotactic plumes in bioconvection. Phys. Fluids 12:5–22
    [Google Scholar]
  49. Ghorai S, Hill NA 2002. Axisymmetric bioconvection in a cylinder. J. Theor. Biol. 219:137–52
    [Google Scholar]
  50. Ghorai S, Hill NA 2005. Penetrative phototactic bioconvection. Phys. Fluids 17:074101
    [Google Scholar]
  51. Ghorai S, Hill NA 2007. Gyrotactic bioconvection in three dimensions. Phys. Fluids 19:054107
    [Google Scholar]
  52. Ghorai S, Panda MK 2013. Bioconvection in an anisotropic scattering suspension of phototactic algae. Eur. J. Mech. B Fluids 41:81–93
    [Google Scholar]
  53. Ghorai S, Panda MK, Hill NA 2010. Bioconvection in a suspension of isotropically scattering phototactic algae. Phys. Fluids 22:071901
    [Google Scholar]
  54. Ghorai S, Singh R 2009. Linear stability analysis of gyrotactic plumes. Phys. Fluids 21:081901
    [Google Scholar]
  55. Ghorai S, Singh R, Hill NA 2015. Wavelength selection in gyrotactic bioconvection. Bull. Math. Biol. 77:1166–84
    [Google Scholar]
  56. Giometto A, Altermatt F, Maritan A, Stocker R, Rinaldo A 2015. Generalized receptor law governs phototaxis in the phytoplankton Euglena gracilis. PNAS 112:7045–50
    [Google Scholar]
  57. Guasto JS, Johnson KA, Gollub JP 2010. Oscillatory flows induced by microorganisms swimming in two dimensions. Phys. Rev. Lett. 105:168102
    [Google Scholar]
  58. Häder DP, Hemmersbach R, Lebert M 2005. Gravity and the Behavior of Unicellular Organisms Dev. Cell Biol. Ser. 40. Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  59. Hill NA, Bees MA 2002. Taylor dispersion of gyrotactic swimming micro-organisms in a linear flow. Phys. Fluids 14:2598–605
    [Google Scholar]
  60. Hill NA, Häder DP 1997. A biased random walk model for the trajectories of swimming micro-organisms. J. Theor. Biol. 186:503–26
    [Google Scholar]
  61. Hill NA, Pedley TJ 2005. Bioconvection. Fluid Dyn. Res. 37:1–20
    [Google Scholar]
  62. Hill NA, Pedley TJ, Kessler JO 1989. Growth of bioconvection patterns in a suspension of gyrotactic microorganisms in a layer of finite depth. J. Fluid Mech. 208:509–43
    [Google Scholar]
  63. Hillesdon AJ, Pedley TJ 1996. Bioconvection in suspensions of oxytactic bacteria: linear theory. J. Fluid Mech. 324:223–59
    [Google Scholar]
  64. Hoecker-Martinez MS, Smyth WD 2012. Trapping of gyrotactic organisms in an unstable shear layer. Cont. Shelf Res. 36:8–18
    [Google Scholar]
  65. Hope A, Croze OA, Poon WCK, Bees MA, Haw MD 2016. Resonant alignment of microswimmer trajectories in oscillatory shear flows. Phys. Rev. Fluids 1:051201
    [Google Scholar]
  66. Hopkins M, Fauci L 2002. A computational model of the collective fluid dynamics of motile micro-organisms. J. Fluid Mech. 455:149–74
    [Google Scholar]
  67. Hosoya C, Akiyama A, Kage A, Baba SA, Mogami Y 2010. Reverse bioconvection of Chlamydomonas in the hyper-density medium. Biol. Sci. Space 24:145–52
    [Google Scholar]
  68. Hwang Y, Pedley T 2014a. Bioconvection under uniform shear: linear stability analysis. J. Fluid Mech. 738:522–62
    [Google Scholar]
  69. Hwang Y, Pedley T 2014b. Stability of downflowing gyrotactic microorganism suspensions in a two-dimensional vertical channel. J. Fluid Mech. 749:750–77
    [Google Scholar]
  70. Ishikawa T 2009. Suspension biomechanics of swimming microbes. J. R. Soc. Interface 6:815–34
    [Google Scholar]
  71. Ishikawa T, Pedley TJ 2014. Dispersion of model microorganisms swimming in a nonuniform suspension. Phys. Rev. E 90:033008
    [Google Scholar]
  72. Janosi IM, Czirok A, Silhavy D, Holczinger A 2002. Is bioconvection enhancing bacterial growth in quiescent environments?. Environ. Microbiol. 4:525–31
    [Google Scholar]
  73. Janosi IM, Kessler J, Horvath V 1998. Onset of bioconvection in suspensions of Bacillus subtilis. Phys. Rev. E 58:4793–800
    [Google Scholar]
  74. Jones MS, Le Baron L, Pedley TJ 1994. Biflagellate gyrotaxis in a shear flow. J. Fluid Mech. 281:137–58
    [Google Scholar]
  75. Kage A, Asato E, Chiba Y, Wada Y, Katsu-Kimura Y et al. 2011. Gravity-dependent changes in bioconvection of Tetrahymena and Chlamydomonas during parabolic flight: increases in wave number induced by pre- and post-parabola hypergravity. Zool. Sci. 28:206–14
    [Google Scholar]
  76. Kage A, Hosoya C, Baba SA, Mogami Y 2013. Drastic reorganization of the bioconvection pattern of Chlamydomonas: quantitative analysis of the pattern transition response. J. Exp. Biol. 216:4557–66
    [Google Scholar]
  77. Karimi A, Ardekani AM 2013. Gyrotactic bioconvection at pycnoclines. J. Fluid Mech. 733:245–67
    [Google Scholar]
  78. Karimi A, Paul MR 2013. Bioconvection in spatially extended domains. Phys. Rev. E 87:053016
    [Google Scholar]
  79. Kessler JO 1984. Gyrotactic buoyant convection and spontaneous pattern formation in algal cell cultures. Nonequilibrium Cooperative Phenomena in Physics and Related Fields MG Velarde241–48 New York: Plenum
    [Google Scholar]
  80. Kessler JO 1985a. Co-operative and concentrative phenomena of swimming micro-organisms. Contemp. Phys. 26:147–66
    [Google Scholar]
  81. Kessler JO 1985b. Hydrodynamic focussing of motile algal cells. Nature 313:218–20
    [Google Scholar]
  82. Kessler JO 1986. Individual and collective dynamics of swimming cells. J. Fluid Mech. 173:191–205
    [Google Scholar]
  83. Kitsunezaki S, Komori R, Harumoto T 2007. Bioconvection and front formation of Paramecium tetraurelia. Phys. Rev. E 76:046301
    [Google Scholar]
  84. Kuznetsov AV, Avramenko A 2005. Effect of fouling on stability of bioconvection of gyrotactic microorganisms in a porous medium. J. Porous Media 8:45–53
    [Google Scholar]
  85. Kuznetsov AV, Jiang N 2001. Numerical investigation of bioconvection of gravitactic microorganisms in an isotropic porous medium. Int. Commun. Heat Mass Transfer 28:877–86
    [Google Scholar]
  86. Lauga E, Powers TR 2009. The hydrodynamics of swimming microorganisms. Rep. Progress Phys. 72:096601
    [Google Scholar]
  87. Lee HG, Kim J 2015. Numerical investigation of falling bacterial plumes caused by bioconvection in a three-dimensional chamber. Eur. J. Mech. B Fluids 52:120–30
    [Google Scholar]
  88. Levandowsky M, Childress WS, Spiegel EA, Hutner SH 1975. A mathematical model of pattern formation by swimming microorganisms. J. Protozool. 22:296–306
    [Google Scholar]
  89. Lewis DM 2003. The orientation of gyrotactic spheroidal micro-organisms in a homogeneous isotropic turbulent flow. Proc. R. Soc. A Math. Phys. Eng. Sci. 459:1293–323
    [Google Scholar]
  90. Loeffer JB, Mefferd RB 1952. Concerning pattern formation by free-swimming microorganisms. Am. Nat. 86:325–29
    [Google Scholar]
  91. Manela A, Frankel I 2003. Generalized Taylor dispersion in suspensions of gyrotactic swimming micro-organisms. J. Fluid Mech. 490:99–127
    [Google Scholar]
  92. Marcos, Fu HC, Powers TR, Stocker R 2009. Separation of microscale chiral objects by shear flow. Phys. Rev. Lett. 102:158103
    [Google Scholar]
  93. Martinez VA, Besseling R, Croze OA, Tailleur J, Reufer M et al. 2012. Differential dynamic microscopy: a high-throughput method for characterizing the motility of microorganisms. Biophys. J. 103:1637–47
    [Google Scholar]
  94. Mathijssen AJTM, Shendruk TN, Yeomans JM, Doostmohammadi A 2016. Upstream swimming in microbiological flows. Phys. Rev. Lett. 116:028104
    [Google Scholar]
  95. Mendelson N 1999. Bacillus subtilis macrofibres, colonies and bioconvection patterns use different strategies to achieve multicellular organization. Environ. Microbiol. 1:471–77
    [Google Scholar]
  96. Metcalfe AM, Pedley TJ 1998. Bacterial bioconvection: weakly nonlinear theory for pattern selection. J. Fluid Mech. 370:249–70
    [Google Scholar]
  97. Metcalfe AM, Pedley TJ 2001. Falling plumes in bacterial bioconvection. J. Fluid Mech. 445:121–49
    [Google Scholar]
  98. Mogami Y, Ishii J, Baba SA 2001. Theoretical and experimental dissection of gravity-dependent mechanical orientation in gravitactic microorganisms. Biol. Bull. 201:26–33
    [Google Scholar]
  99. Mogami Y, Yamane A, Gino A, Baba S 2004. Bioconvective pattern formation of Tetrahymena under altered gravity. J. Exp. Biol. 207:3349–59
    [Google Scholar]
  100. Nägeli C 1860. Ortsbewegungen der Pflanzenzellen und ihrer Theile (Strömungen). Beitr. Wiss. Bot. 2:59–108
    [Google Scholar]
  101. Nonaka Y, Kikuchi K, Numayama-Tsuruta K, Kage A, Ueno H, Ishikawa T 2016. Inhomogeneous distribution of Chlamydomonas in a cylindrical container with a bubble plume. Biol. Open 5:154–60
    [Google Scholar]
  102. Ochiai N, Dragiila MI, Parke JL 2011. Pattern swimming of Phytophthora citricola zoospores: an example of microbial bioconvection. Fungal Biol. 115:228–35
    [Google Scholar]
  103. Ogawa T, Shoji E, Suematsu NJ, Nishimori H, Izumi S et al. 2016. The flux of Euglena gracilis cells depends on the gradient of light intensity. PLOS ONE 11:e0168114
    [Google Scholar]
  104. O'Malley S 2011. Bi-flagellate swimming dynamics PhD thesis, Univ. Glasgow Glasgow:
    [Google Scholar]
  105. O'Malley S, Bees MA 2012. The orientation of swimming biflagellates in shear flows. Bull. Math. Biol. 74:232–55
    [Google Scholar]
  106. Panda MK, Ghorai S 2013. Penetrative phototactic bioconvection in an isotropic scattering suspension. Phys. Fluids 25:071902
    [Google Scholar]
  107. Panda MK, Singh R 2016. Penetrative phototactic bioconvection in a two-dimensional non-scattering suspension. Phys. Fluids 28:054105
    [Google Scholar]
  108. Panda MK, Singh R, Mishra AC, Mohanty SK 2016. Effects of both diffuse and collimated incident radiation on phototactic bioconvection. Phys. Fluids 28:124104
    [Google Scholar]
  109. Pedley TJ 2010. Instability of uniform micro-organism suspensions revisited. J. Fluid Mech. 647:335–59
    [Google Scholar]
  110. Pedley TJ 2015. Gyrotaxis in uniform vorticity. J. Fluid Mech. 762:R6
    [Google Scholar]
  111. Pedley TJ, Hill NA, Kessler J 1988. The growth of bioconvection patterns in a uniform suspension of gyrotactic microorganisms. J. Fluid Mech. 195:223–37
    [Google Scholar]
  112. Pedley TJ, Kessler JO 1987. The orientation of spheroidal micro-organisms swimming in a flow field. Proc. R. Soc. Lond. Ser. B 231:47–70
    [Google Scholar]
  113. Pedley TJ, Kessler JO 1990. A new continuum model for suspensions of gyrotactic micro-organisms. J. Fluid Mech. 212:155–82
    [Google Scholar]
  114. Pedley TJ, Kessler JO 1992. Hydrodynamic phenomena in suspensions of swimming microorganisms. Annu. Rev. Fluid Mech. 24:313–58
    [Google Scholar]
  115. Persson A, Smith BC 2013. Cell density-dependent swimming patterns of Alexandrium fundyense early stationary phase cells. Aquat. Microb. Ecol. 68:251–58
    [Google Scholar]
  116. Platt JR 1961. Bioconvection patterns in cultures of free-swimming organisms. Science 133:1766–67
    [Google Scholar]
  117. Plesset M, Winet H 1974. Bioconvection patterns in swimming microorganism cultures as an example of Rayleigh-Taylor instability. Nature 248:441–43
    [Google Scholar]
  118. Polin M, Tuval I, Drescher K, Gollub JP, Goldstein RE 2009. Chlamydomonas swims with two gears in a eukaryotic version of run-and-tumble locomotion. Science 325:487–90
    [Google Scholar]
  119. Ramaswamy S 2010. The mechanics and statistics of active matter. Annu. Rev. Condens. Matter Phys. 1:323–45
    [Google Scholar]
  120. Richardson SH, Baggaley A, Hill N 2018. Gyrotactic suppression and emergence of chaotic trajectories of swimming particles in three-dimensional flows. Phys. Rev. Fluids 3:023102
    [Google Scholar]
  121. Roberts A 1970. Geotaxis in motile micro-organisms. J. Exp. Biol. 53:687–99
    [Google Scholar]
  122. Roberts A, Deacon F 2002. Gravitaxis in motile micro-organisms: the role of fore–aft body asymmetry. J. Fluid Mech. 452:405–23
    [Google Scholar]
  123. Sachs J 1876. Ueber Emulsionsfiguren und Gruppirung der Schwarmsporen im Wasser. Flora 59:273–75
    [Google Scholar]
  124. Saintillan D 2014. Swimming in shear. J. Fluid Mech. 744:1–4
    [Google Scholar]
  125. Santamaria F, De Lillo F, Cencini M, Boffetta G 2014. Gyrotactic trapping in laminar and turbulent Kolmogorov flow. Phys. Fluids 26:111901
    [Google Scholar]
  126. Sato N, Sato K, Toyoshima M 2018. Analysis and modeling of the inverted bioconvection in Chlamydomonas reinhardtii: emergence of plumes from the layer of accumulated cells. Heliyon 4:e00586
    [Google Scholar]
  127. Simha RA, Ramaswamy S 2002. Hydrodynamic fluctuations and instabilities in ordered suspensions of self-propelled particles. Phys. Rev. Lett. 89:058101
    [Google Scholar]
  128. Smayda TJ 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42:1137–53
    [Google Scholar]
  129. Sommer T, Danza F, Berg J, Sengupta A, Constantinescu G et al. 2017. Bacteria-induced mixing in natural waters. Geophys. Res. Lett. 44:9424–32
    [Google Scholar]
  130. Straughan B 2013. The Energy Method, Stability, and Nonlinear Convection Appl. Math. Ser. 91. New York: Springer-Verlag
    [Google Scholar]
  131. Suematsu NJ, Awazu A, Izumi S, Noda S, Nakata S, Nishimori H 2011. Localized bioconvection of Euglena caused by phototaxis in the lateral direction. J. Phys. Soc. Jpn. 80:064003
    [Google Scholar]
  132. Thiffeault JL, Childress S 2010. Stirring by swimming bodies. Phys. Lett. A 374:3487–90
    [Google Scholar]
  133. Thorn GJ, Bearon RN 2010. Transport of spherical gyrotactic organisms in general three-dimensional flow fields. Phys. Fluids 22:041902
    [Google Scholar]
  134. Tuval I, Cisneros L, Dombrowski C, Wolgemuth CW, Kessler J, Goldstein RE 2005. Bacterial swimming and oxygen transport near contact lines. PNAS 102:2277–82
    [Google Scholar]
  135. Vincent RV, Hill NA 1996. Bioconvection in a suspension of phototactic algae. J. Fluid Mech. 327:343–71
    [Google Scholar]
  136. Vladimirov VA, Wu MSC, Pedley TJ, Denissenko PV, Zakhidova SG 2004. Measurement of cell velocity distributions in populations of motile algae. J. Exp. Biol. 207:1203–16
    [Google Scholar]
  137. Wager H 1911. VII. On the effect of gravity upon the movements and aggregation of Euglena viridis, Ehrb., and other micro-organisms. Philos. Trans. R. Soc. Lond. B 201:333–90
    [Google Scholar]
  138. Wille JJ Jr., Ehret CF 1968. Circadian rhythm of pattern formation in populations of a free-swimming organism, Tetrahymena. J. Protozool. 15:789–92
    [Google Scholar]
  139. Williams CR, Bees MA 2011a. Photo-gyrotactic bioconvection. J. Fluid Mech. 678:41–86
    [Google Scholar]
  140. Williams CR, Bees MA 2011b. A tale of three taxes: photo-gyro-gravitactic bioconvection. J. Exp. Biol. 214:2398–408
    [Google Scholar]
  141. Williams CR, Bees MA 2014. Mechanistic modeling of sulfur-deprived photosynthesis and hydrogen production in suspensions of Chlamydomonas reinhardtii. Biotechnol. Bioeng. 111:320–35
    [Google Scholar]
  142. Winet H, Jahn TL 1972. On the origin of bioconvective fluid instabilities in Tetrahymena culture systems. Biorheology 9:87–104
    [Google Scholar]
  143. Yamamoto Y, Okayama T, Sato K, Takaoki T 1992. Relation of pattern formation to external conditions in the flagellate, Chlamydomonas reinhardtii. Eur. J. Protistol. 28:415–20
    [Google Scholar]
  144. Zöttl A, Stark H 2013. Periodic and quasiperiodic motion of an elongated microswimmer in Poiseuille flow. Eur. Phys. J. E 36:4
    [Google Scholar]
/content/journals/10.1146/annurev-fluid-010518-040558
Loading
/content/journals/10.1146/annurev-fluid-010518-040558
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error