Efficient nematode swimming in a shear thinning colloidal suspension.

The swimming behavior of a nematode Caenorhabditis elegans (C. elegans) is investigated in a non-Newtonian shear thinning colloidal suspension. At the onset value (ϕ∼ 8%), the suspension begins to exhibit shear thinning behavior, and the average swimming speed of worms jumps by approximately 12% more than that measured in a Newtonian solution exhibiting no shear dependent viscosity. In the shear thinning regime, we observe a gradual yet significant improvement in swimming efficiency with an increase in ϕ while the swimming speed remains nearly constant. We postulate that this enhanced swimming can be explained by the temporal change in the stroke form of the nematode that is uniquely observed in a shear thinning colloidal suspension: the nematode features a fast and large stroke in its head to overcome the temporally high drag imposed by the viscous medium, whose effective viscosity (ηs) is shown to drop drastically, inversely proportional to the strength of its stroke. Our results suggest new insights into how nematodes efficiently maneuver through the complex fluid environment in their natural habitat.

[1]  S. Brenner.  The genetics of Caenorhabditis elegans. , 1974, Genetics.

[2]  Henry C. Fu,et al.  Low-Reynolds-number swimming in gels , 2010, 1004.1339.

[3]  Joseph Teran,et al.  Viscoelastic fluid response can increase the speed and efficiency of a free swimmer. , 2010, Physical review letters.

[4]  Dilhan M. Kalyon,et al.  Apparent slip and viscoplasticity of concentrated suspensions , 2005 .

[5]  P. Arratia,et al.  Undulatory swimming in viscoelastic fluids. , 2011, Physical review letters.

[6]  L. Fauci,et al.  Biofluidmechanics of Reproduction , 2006 .

[7]  Philipp Kanehl,et al.  Fluid mechanics of swimming bacteria with multiple flagella. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  Bin Liu,et al.  Locomotion of helical bodies in viscoelastic fluids: enhanced swimming at large helical amplitudes. , 2013, Physical review letters.

[9]  Yukio Magariyama,et al.  A mathematical explanation of an increase in bacterial swimming speed with viscosity in linear-polymer solutions. , 2002, Biophysical journal.

[10]  N. Wagner,et al.  Shear thickening in colloidal dispersions , 2009 .

[11]  J. Gray,et al.  The Propulsion of Sea-Urchin Spermatozoa , 1955 .

[12]  Y. Magariyama,et al.  Improvement in motion efficiency of the spirochete Brachyspira pilosicoli in viscous environments. , 2006, Biophysical journal.

[13]  P. Arratia,et al.  Propulsive force measurements and flow behavior of undulatory swimmers at low Reynolds number , 2010 .

[14]  Xiang Cheng,et al.  Imaging the Microscopic Structure of Shear Thinning and Thickening Colloidal Suspensions , 2011, Science.

[15]  Sunghwan Jung,et al.  Caenorhabditis elegans swimming in a saturated particulate system , 2010 .

[16]  P. Arratia,et al.  Undulatory swimming in shear-thinning fluids: experiments with Caenorhabditis elegans , 2014, Journal of Fluid Mechanics.

[17]  Eric Lauga,et al.  Enhanced active swimming in viscoelastic fluids , 2014, 1410.1720.

[18]  Sean Gart,et al.  The collective motion of nematodes in a thin liquid layer , 2010, 1012.4798.

[19]  Patricio A. Vela,et al.  Locomotor benefits of being a slender and slick sand swimmer , 2015, Journal of Experimental Biology.

[20]  Josué Sznitman,et al.  Motility of small nematodes in disordered wet granular media , 2010 .

[21]  E A Gaffney,et al.  Bend propagation in the flagella of migrating human sperm, and its modulation by viscosity. , 2009, Cell motility and the cytoskeleton.

[22]  L. Christophorou.  Science , 2018, Emerging Dynamics: Science, Energy, Society and Values.

[23]  Damon A. Clark,et al.  Mechanosensation and mechanical load modulate the locomotory gait of swimming C. elegans , 2007, Journal of Experimental Biology.

[24]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[25]  E. Lauga,et al.  Small-amplitude swimmers can self-propel faster in viscoelastic fluids. , 2015, Journal of theoretical biology.

[26]  T. Powers,et al.  The hydrodynamics of swimming microorganisms , 2008, 0812.2887.

[27]  P. Arratia,et al.  Motility of small nematodes in wet granular media , 2010, 1006.0990.

[28]  Becca Thomases,et al.  Mechanisms of elastic enhancement and hindrance for finite-length undulatory swimmers in viscoelastic fluids. , 2014, Physical review letters.

[29]  Gaojin Li,et al.  Undulatory swimming in non-Newtonian fluids , 2015, Journal of Fluid Mechanics.

[30]  Daniel I Goldman,et al.  Environmental interaction influences muscle activation strategy during sand-swimming in the sandfish lizard Scincus scincus , 2013, Journal of Experimental Biology.

[31]  E. Lauga.  Life around the scallop theorem , 2010, 1011.3051.

[32]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]／Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[33]  U. Ko,et al.  A sorting strategy for C. elegans based on size-dependent motility and electrotaxis in a micro-structured channel. , 2012, Lab on a Chip.

[34]  A. Leshansky,et al.  Enhanced low-Reynolds-number propulsion in heterogeneous viscous environments. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[35]  P. Arratia,et al.  Undulatory swimming in fluids with polymer networks , 2013, 1310.2630.

[36]  D. Smith,et al.  Physics of rheologically enhanced propulsion: Different strokes in generalized Stokes , 2013, 1309.1076.

[37]  Eric Lauga,et al.  Phase-separation models for swimming enhancement in complex fluids. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[38]  Michael Berhanu,et al.  Speed of a swimming sheet in Newtonian and viscoelastic fluids. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[39]  P. Arratia,et al.  Undulatory locomotion of Caenorhabditis elegans on wet surfaces. , 2011, Biophysical journal.

[40]  S. Wereley,et al.  soft matter , 2019, Science.

[41]  A. Pacey,et al.  Sperm transport in the female reproductive tract. , 2006, Human reproduction update.

[42]  S. Suarez,et al.  Hyperactivation enhances mouse sperm capacity for penetrating viscoelastic media. , 1992, Biology of reproduction.

[43]  Aravinthan D. T. Samuel,et al.  Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans , 2010, Proceedings of the National Academy of Sciences.

[44]  Jana Schwarz-Linek,et al.  Flagellated bacterial motility in polymer solutions , 2014, Proceedings of the National Academy of Sciences.

[45]  Eric Lauga,et al.  Waving transport and propulsion in a generalized Newtonian fluid , 2013, 1403.4260.

[46]  P. Arratia,et al.  The Effects of Fluid Viscosity on the Kinematics and Material Properties of C. elegans Swimming at Low Reynolds Number , 2009, 0912.3402.

[47]  Chen Li,et al.  Undulatory Swimming in Sand: Subsurface Locomotion of the Sandfish Lizard , 2009, Science.