Advertisement

The European Physical Journal Special Topics

, Volume 225, Issue 4, pp 629–649 | Cite as

Entangled active matter: From cells to ants

  • D.L. HuEmail author
  • S. Phonekeo
  • E. Altshuler
  • F. Brochard-Wyart
Regular Article
Part of the following topical collections:
  1. Cooperative Particles: Patchy Colloids, Active Matter and Nanofluids

Abstract

Both cells and ants belong to the broad field of active matter, a novel class of non-equilibrium materials composed of many interacting units that individually consume energy and collectively generate motion or mechanical stresses. However cells and ants differ from fish and birds in that they can support static loads. This is because cells and ants can be entangled, so that individual units are bound by transient links. Entanglement gives cells and ants a set of remarkable properties usually not found together, such as the ability to flow like a fluid, spring back like an elastic solid, and self-heal. In this review, we present the biology, mechanics and dynamics of both entangled cells and ants. We apply concepts from soft matter physics and wetting to characterize these systems as well as to point out their differences, which arise from their differences in size. We hope that our viewpoints will spur further investigations into cells and ants as active materials, and inspire the fabrication of synthetic active matter.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    S. Camazine, Self-organization in Biological Systems (Princeton University Press, 2003)Google Scholar
  2. 2.
    N.J. Mehdiabadi, C.N. Jack, T.T. Farnham, T.G. Platt, S.E. Kalla, G. Shaulsky, D.C. Queller, J.E. Strassmann, Nature 442, 881 (2006)ADSCrossRefGoogle Scholar
  3. 3.
    Z. Cui, M.C. Willingham, A.M. Hicks, M.A. Alexander-Miller, T.D. Howard, G.A. Hawkins, M.S. Miller, H.M. Weir, W. Du, C.J. DeLong, Proc. Nat. Acad. Sci. 100, 6682 (2003)ADSCrossRefGoogle Scholar
  4. 4.
    W.C. Allee (Chicago: The University of Chicago Press, 1931)Google Scholar
  5. 5.
    T.S. Savage, Trans. Royal Entomol. Soc. London 5, 1 (1847), ISSN 1365-2311CrossRefGoogle Scholar
  6. 6.
    C. Anderson, N.R. Franks, Adv. Study Behav. 33, 1 (2003), ISSN 0065- 3454CrossRefGoogle Scholar
  7. 7.
    C. Anderson, G. Theraulaz, J.L. Deneubourg, Insectes Sociaux 49, 99 (2002), ISSN 0020-1812CrossRefGoogle Scholar
  8. 8.
    W.R. Ashby, J. Gen. Psychol. 37, 125 (1947)CrossRefGoogle Scholar
  9. 9.
    E. Bonabeau, G. Theraulaz, J.L. Deneubourg, S. Aron, S. Camazine, Trends Ecol. Evol. 12, 188 (1997), ISSN 0169-5347CrossRefGoogle Scholar
  10. 10.
    E. Bonabeau, G. Theraulaz, J.L. Deneubourg, A. Lioni, F. Libert, C. Sauwens, L. Passera, Phys. Rev. E 57, 5904 (1998)ADSCrossRefGoogle Scholar
  11. 11.
    A. Colorni, M. Dorigo, V. Maniezzo, et al., Distributed Optimization by Ant Colonies, in Proceedings of the First European Conference on Artificial Life, Vol. 142 (Paris, France, 1991), p. 134Google Scholar
  12. 12.
    S. Garnier, J. Gautrais, G. Theraulaz, Swarm Intell. 1, 3 (2007), ISSN 1935-3812CrossRefGoogle Scholar
  13. 13.
    J. Halley, D.A. Winkler, et al., Complexity 14, 10 (2008)CrossRefGoogle Scholar
  14. 14.
    B. Hölldobler, E.O. Wilson, The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies (WW Norton & Company, 2009)Google Scholar
  15. 15.
    D.J. Sumpter, Philosophical Trans. Royal Society B: Biol. Sci. 361, 5 (2006), ISSN 0962-8436CrossRefGoogle Scholar
  16. 16.
    G. Theraulaz, E. Bonabeau, C. Sauwens, J.L. Deneubourg, A. Lioni, F. Libert, L. Passera, R. Solé, Bull. Math. Biol. 63, 1079 (2001)CrossRefGoogle Scholar
  17. 17.
    S. Phonekeo, N. Mlot, D. Monaenkova, D.L. Hu, C. Tovey (in preparation) (2015)Google Scholar
  18. 18.
    J. Bibette, L.Y. Chu, E.S. Carreras, A. Royere, N. Bremond, Method for Manufacturing Capsule Series, and Related Capsule Series (2009), US Patent App. 13/131, 971Google Scholar
  19. 19.
    K. Alessandri, B.R. Sarangi, V.V. Gurchenkov, B. Sinha, T.R. Kießling, L. Fetler, F. Rico, S. Scheuring, C. Lamaze, A. Simon, et al., Proc. Nat. Acad. Sci. 110, 14843 (2013)ADSCrossRefGoogle Scholar
  20. 20.
    C.A. Higgins, J.C. Chen, J.E. Cerise, C.A. Jahoda, A.M. Christiano, Proc. Nat. Acad. Sci. 110, 19679 (2013), ISSN 0027-8424ADSCrossRefGoogle Scholar
  21. 21.
    K.E. Toyoshima, K. Asakawa, N. Ishibashi, H. Toki, M. Ogawa, T. Hasegawa, T. Irié, T. Tachikawa, A. Sato, A. Takeda, et al., Nat. Comm. 3, 784 (2012)ADSCrossRefGoogle Scholar
  22. 22.
    Y. Cao, J.P. Vacanti, K.T. Paige, J. Upton, C.A. Vacanti, Plastic Reconstructive Surgery 100, 297 (1997), ISSN 0032-1052CrossRefGoogle Scholar
  23. 23.
    M.A. Lancaster, M. Renner, C.A. Martin, D. Wenzel, L.S. Bicknell, M.E. Hurles, T. Homfray, J.M. Penninger, A.P. Jackson, J.A. Knoblich, Nature 501, 373 (2013), ISSN 0028-0836ADSCrossRefGoogle Scholar
  24. 24.
    C. van der Weele, in Encyclopedia of Food and Agricultural Ethics (Springer, 2014), p. 1219Google Scholar
  25. 25.
    L.J. Dunham, H.L. Stewart, J. National Cancer Inst. 13, 1299 (1953), ISSN 0027-8874Google Scholar
  26. 26.
    B. Boyer, S. Dufour, J.P. Thiery, Exper. Cell Res. 201, 347 (1992), ISSN 0014-4827CrossRefGoogle Scholar
  27. 27.
    D. Pimentel, R. Zuniga, D. Morrison, Ecological Econom. 52, 273 (2005), ISSN 0921-8009CrossRefGoogle Scholar
  28. 28.
    W.P. MacKay, S. Majdi, J. Irving, S.B. Vinson, C. Messer, Jo. Kansas Entomol. Soc., p. 39 (1992), ISSN 0022-8567Google Scholar
  29. 29.
    M. Yim, W.M. Shen, B. Salemi, D. Rus, M. Moll, H. Lipson, E. Klavins, G.S. Chirikjian, Robotics & Automation Mag., IEEE 14, 43 (2007), ISSN 1070-9932CrossRefGoogle Scholar
  30. 30.
    G. Beni, J. Wang, in Robots and Biological Systems: Towards a New Bionics? (Springer, 1993), p. 703Google Scholar
  31. 31.
    Y.U. Cao, A.S. Fukunaga, A. Kahng, Autonomous Robots 4, 7 (1997), ISSN 0929-5593CrossRefGoogle Scholar
  32. 32.
    M. Dorigo, V. Trianni, E. Ahin, R. Gro, T.H. Labella, G. Baldassarre, S. Nolfi, J.L. Deneubourg, F. Mondada, D. Floreano, Autonomous Robots 17, 223 (2004), ISSN 0929-5593CrossRefGoogle Scholar
  33. 33.
    R. Groß, M. Bonani, F. Mondada, M. Dorigo, Robotics, IEEE Trans. 22, 1115 (2006)Google Scholar
  34. 34.
    M. Rubenstein, A. Cornejo, R. Nagpal, Science 345, 795 (2014), ISSN 0036-8075ADSCrossRefGoogle Scholar
  35. 35.
    B. Hölldobler, E.O. Wilson, The Ants (Harvard University Press, 1990)Google Scholar
  36. 36.
    R. Pfeifer, M. Lungarella, F. Iida, Science 318(5853), 1088 (2007), ISSN 0036-8075ADSCrossRefGoogle Scholar
  37. 37.
    W.R. Tschinkel, The Fire Ants (Harvard University Press, 2006), ISBN 0674022076Google Scholar
  38. 38.
    W.K. Purves, G.H. Orians, D. Sadava, H.C. Heller, Life: The Science of Biology: Volume III: Plants and Animals, Vol. 3 (Macmillan, 2003), ISBN 0716758105Google Scholar
  39. 39.
    M. Godin, F.F. Delgado, S. Son, W.H. Grover, A.K. Bryan, A. Tzur, P. Jorgensen, K. Payer, A.D. Grossman, M.W. Kirschner, Nat. Meth. 7, 387 (2010), ISSN 1548-7091CrossRefGoogle Scholar
  40. 40.
    P. DiMilla, K. Barbee, D. Lauffenburger, Biophys. J. 60, 15 (1991)CrossRefGoogle Scholar
  41. 41.
    N. Mlot, C. Tovey, D.L. Hu, Proc. Nat. Acad. Sci. 108, 7669 (2011), ISSN 0027-8424ADSCrossRefGoogle Scholar
  42. 42.
    N. Mlot, C. Tovey, D.L. Hu, Comm. Integr. Biol. 5(6), 590 (2012)CrossRefGoogle Scholar
  43. 43.
    G. Beaune, T.V. Stirbat, N. Khalifat, O. Cochet-Escartin, S. Garcia, V.V. Gurchenkov, M.P. Murrell, S. Dufour, D. Cuvelier, F. Brochard-Wyart, Proc. Nat. Acad. Sci. 111, 8055 (2014)ADSCrossRefGoogle Scholar
  44. 44.
    M.L. Heuzé, O. Collin, E. Terriac, A.M. Lennon-Duménil, M. Piel, in Cell Migration (Springer, 2011), p. 415Google Scholar
  45. 45.
    W. Federle, M. Riehle, A.S. Curtis, R.J. Full, Integrative Comparative Biol. 42, 1100 (2002), ISSN 1540-7063CrossRefGoogle Scholar
  46. 46.
    W. Federle, T. Endlein, Arthropod Struct. Dev. 33, 67 (2004), ISSN 1467-8039CrossRefGoogle Scholar
  47. 47.
    J.W. Bush, D.L. Hu, M. Prakash, Adv. Insect Physiol. 34, 117 (2007), ISSN 0065-2806CrossRefGoogle Scholar
  48. 48.
    S.P. Yanoviak, R. Dudley, M. Kaspari, Nature 433, 624 (2005), ISSN 0028-0836ADSCrossRefGoogle Scholar
  49. 49.
    N.R. Franks, T. Richardson, Nature 439, 153 (2006), ISSN 0028-0836ADSCrossRefGoogle Scholar
  50. 50.
    M. Möglich, U. Maschwitz, B. Hölldobler, Science 186, 1046 (1974)ADSCrossRefGoogle Scholar
  51. 51.
    I.D. Couzin, N.R. Franks, Proc. Royal Society London B: Biol. Sci. 270, 139 (2003), ISSN 0962-8452CrossRefGoogle Scholar
  52. 52.
    R. Rosengren, W. Fortelius, Insectes Sociaux 33, 306 (1986)CrossRefGoogle Scholar
  53. 53.
    T.S. Collett, P. Graham, R.A. Harris, N. Hempel-De-Ibarra, Adv. Study Behavior 36, 123 (2006), ISSN 0065-3454CrossRefGoogle Scholar
  54. 54.
    R.O. Hynes, Cell 69, 11 (1992), ISSN 0092-8674CrossRefGoogle Scholar
  55. 55.
    J. Pearson, J. Fluid Mech. 4, 489 (1958), ISSN 1469-7645ADSCrossRefGoogle Scholar
  56. 56.
    J. Solon, A. Kaya-Copur, J. Colombelli, D. Brunner, Cell 137, 1331 (2009), ISSN 0092-8674CrossRefGoogle Scholar
  57. 57.
    N.J. Armstrong, K.J. Painter, J.A. Sherratt, Bull. Math. Biol. 71, 1 (2009)MathSciNetCrossRefGoogle Scholar
  58. 58.
    M. Singh, C. Berkland, M.S. Detamore, Tissue Eng. Part B: Rev. 14, 341 (2008)CrossRefGoogle Scholar
  59. 59.
    F.G. Giancotti, E. Ruoslahti, Science 285, 1028 (1999)CrossRefGoogle Scholar
  60. 60.
    Y.S. Chu, W.A. Thomas, O. Eder, F. Pincet, E. Perez, J.P. Thiery, S. Dufour, J. Cell Biol. 167, 1183 (2004)CrossRefGoogle Scholar
  61. 61.
    S. Phonekeo, T. Dave, D.L. Hu, Soft Matter 12, 4214 (2016)ADSCrossRefGoogle Scholar
  62. 62.
    P.C. Foster, N.J. Mlot, A. Lin, D.L. Hu, J. Exper. Biol. 217, 2089 (2014), ISSN 0022-0949CrossRefGoogle Scholar
  63. 63.
    J.H. Dirks, C.J. Clemente, W. Federle, J. Royal Society Interface p. rsif20090308 (2009), ISSN 1742-5689Google Scholar
  64. 64.
    P. Drechsler, W. Federle, J. Comparative Physiol. A 192, 1213 (2006), ISSN 0340-7594CrossRefGoogle Scholar
  65. 65.
    A. Lipp, H. Wolf, F.O. Lehmann, J. Exper. Biol. 208, 707 (2005), ISSN 0022-0949CrossRefGoogle Scholar
  66. 66.
    P.H. Puech, K. Poole, D. Knebel, D.J. Muller, Ultramicroscopy 106, 637 (2006), ISSN 0304-3991CrossRefGoogle Scholar
  67. 67.
    A. Dejean, C. Leroy, B. Corbara, O. Roux, R. Crghino, J. Orivel, R. Boulay, PLoS ONE 5, e11331 (2010), ISSN 1932-6203, 09-PONE-RA-14396R3[PII] 20593032[pmid] PLoS One, http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2892516/ ADSCrossRefGoogle Scholar
  68. 68.
    R.J. Pelham, Y.l. Wang, Proc. Nat. Acad. Scien. 94, 13661 (1997), ISSN 0027-8424ADSCrossRefGoogle Scholar
  69. 69.
    M. Tennenbaum, Z. Liu, A. Fernéandez-Nieves, D.L. Hu, Nat. Mater. 15, 54 (2016)ADSCrossRefGoogle Scholar
  70. 70.
    R.G. Wells, Hepatology 47, 1394 (2008), ISSN 1527-3350CrossRefGoogle Scholar
  71. 71.
    W. Kim, T. Gilet, J.W. Bush, Proc. Nat. Acad. Sci. 108, 16618 (2011)ADSCrossRefGoogle Scholar
  72. 72.
    R.A. Foty, C.M. Pfleger, G. Forgacs, M.S. Steinberg, Dev. 122, 1611 (1996), ISSN 0950-1991Google Scholar
  73. 73.
    G. Forgacs, R.A. Foty, Y. Shafrir, M.S. Steinberg, Biophysical J. 74, 2227 (1998), ISSN 0006-3495, http://www.sciencedirect.com/science/article/pii/S0006349598779329 ADSCrossRefGoogle Scholar
  74. 74.
    I. Martin, B. Dozin, R. Quarto, R. Cancedda, F. Beltrame, Cytometry 28, 141 (1997), ISSN 0196-4763CrossRefGoogle Scholar
  75. 75.
    M.S. Steinberg, Science 141(3579), 401 (1963), ISSN 0036-8075 (Print)ADSCrossRefGoogle Scholar
  76. 76.
    R.A. Foty, M.S. Steinberg, Inter. J. Dev. Biol. 48, 397 (2004), ISSN 0214-6282CrossRefGoogle Scholar
  77. 77.
    M.S. Steinberg, Curr. Opin. Genet. Dev. 17, 281 (2007), ISSN 0959-437XCrossRefGoogle Scholar
  78. 78.
    R.A. Foty, G. Forgacs, C.M. Pfleger, M.S. Steinberg, Phys. Rev. Lett. 72, 2298 (1994)ADSCrossRefGoogle Scholar
  79. 79.
    K. Guevorkian, M.J. Colbert, M. Durth, S. Dufour, F. Brochard-Wyart, Phys. Rev. Lett. 104, 218101 (2010)ADSCrossRefGoogle Scholar
  80. 80.
    T. Le Pennec, K.J. Måløy, A. Hansen, M. Ammi, D. Bideau, X.l. Wu, Phys. Rev. E 53, 2257 (1996)ADSCrossRefGoogle Scholar
  81. 81.
    F. Brochard, P. De Gennes, Langmuir 8, 3033 (1992), ISSN 0743-7463CrossRefGoogle Scholar
  82. 82.
    K. Migler, H. Hervet, L. Leger, Phys. Rev. Lett. 70, 287 (1993)ADSCrossRefGoogle Scholar
  83. 83.
    F.C. Linn, J. Bone & Joint Surgery 49, 1079 (1967)Google Scholar
  84. 84.
    Z. Dai, S.N. Gorb, Science in China Series G: Phys., Mechan. Astron. 47, 99 (2004)CrossRefGoogle Scholar
  85. 85.
    N. Gravish, S.V. Franklin, D.L. Hu, D.I. Goldman, Phys. Rev. Lett. 108, 208001 (2012)ADSCrossRefGoogle Scholar
  86. 86.
    S.V. Franklin, EPL (Europhysics Letters) 106, 58004 (2014), ISSN 0295-5075ADSCrossRefGoogle Scholar
  87. 87.
    S. Douezan, K. Guevorkian, R. Naouar, S. Dufour, D. Cuvelier, F. Brochard-Wyart, Proc. Nat. Acad. Sci. 108, 7315 (2011)ADSCrossRefGoogle Scholar
  88. 88.
    S. Douezan, F. Brochard-Wyart, Eur. Phys. J. E 35, 1 (2012)CrossRefGoogle Scholar
  89. 89.
    A. John, A. Schadschneider, D. Chowdhury, K. Nishinari, Phys. Rev. Lett. 102, 108001 (2009)ADSCrossRefGoogle Scholar
  90. 90.
    S.C. Nicolis, J. Fernández, C. Pérez-Penichet, C. Noda, F. Tejera, O. Ramos, D.J. Sumpter, E. Altshuler, Phys. Rev. Lett. 110, 268104 (2013)ADSCrossRefGoogle Scholar
  91. 91.
    F. Tejera, A. Reyes, E. Altshuler, Eur. Phys. J. Special Topics 225(4), 663 (2016)Google Scholar
  92. 92.
    E. Altshuler, O. Ramos, Y. Núñez, J. Fernández, A. Batista-Leyva, C. Noda, Amer. Nat. 166, 643 (2005)CrossRefGoogle Scholar
  93. 93.
    D. Monaenkova, N. Gravish, G. Rodriguez, R. Kutner, M.A. Goodisman, D.I. Goldman, J. Exp. Biol. 218, 1295 (2015), ISSN 0022-0949CrossRefGoogle Scholar
  94. 94.
    T. Balch, Z. Khan, M. Veloso, Proceedings of the fifth International Conference on Autonomous Agents (2001), p. 521Google Scholar
  95. 95.
    Z. Khan, T. Balch, F. Dellaert, An MCMC-based Particle Filter For Tracking Multiple Interacting Targets (Springer, 2004), p. 279, ISBN 3540219811Google Scholar
  96. 96.
    C. Noda, J. Fernández, C. Pérez-Penichet, E. Altshuler, Rev. Sci. Inst. 77, 126102 (2006)ADSCrossRefGoogle Scholar
  97. 97.
    E.J. Robinson, T.O. Richardson, A.B. Sendova-Franks, O. Feinerman, N.R. Franks, Behav. Ecol. Sociobiol. 63, 627 (2009), ISSN 0340-5443CrossRefGoogle Scholar
  98. 98.
    J. Li, D. Han, Y.P. Zhao, Sci. Rep. 4 (2014)Google Scholar
  99. 99.
    J.H. Dirks, W. Federle, Soft Matter 7, 11047 (2011)ADSCrossRefGoogle Scholar

Copyright information

© EDP Sciences and Springer 2016

Authors and Affiliations

  • D.L. Hu
    • 1
    Email author
  • S. Phonekeo
    • 1
  • E. Altshuler
    • 2
  • F. Brochard-Wyart
    • 3
    • 4
  1. 1.Schools of Mechanical Engineering and Biology, Georgia Institute of TechnologyAtlantaUSA
  2. 2.Group of Complex Systems and Statistical Physics, Physics Faculty, University of HavanaLa HabanaCuba
  3. 3.UPMC Univ. Paris 06, UMR 168, Institut Curie, 26 rue d’UlmParis Cedex 05France
  4. 4.CNRS, UMR 168, Institut CurieParis Cedex 05France

Personalised recommendations