Aplysia Californica as a Novel Source of Material for Biohybrid Robots and Organic Machines

  • Victoria A. WebsterEmail author
  • Katherine J. Chapin
  • Emma L. Hawley
  • Jill M. Patel
  • Ozan Akkus
  • Hillel J. Chiel
  • Roger D. Quinn
Conference paper
Part of the Lecture Notes in Computer Science book series (LNCS, volume 9793)


Aplysia californica is presented as a novel source of actuator and scaffold material for biohybrid robots. Collagen isolated from the Aplysia skin has been fabricated into gels and electrocompacted scaffolds. Additionally, the I2 muscle from the Aplysia buccal mass had been isolated for use as an organic actuator. This muscle has been characterized and the maximum force was found to be 58.5 mN with a maximum muscle strain of 12 ± 3 %. Finally, a flexible 3D printed biohybrid robot has been fabricated which is powered by the I2 muscle and is capable of locomotion at 0.43 cm/min under field stimulation.


Biohybrid devices Organic actuators Biorobotics Aplysia californica 



This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. DGE-0951783 and a GAANN Fellowship (Grant No. P200A150316). This study was also funded in part by grants from the National Science Foundation (Grant No. DMR-1306665), and the National Institute of Health (Grant No. R01 AR063701). Any opinion, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.


  1. 1.
    Feinberg, A.W., Feigel, A., Shevkoplyas, S.S., Sheehy, S., Whitesides, G.M., Parker, K.K.: Muscular thin films for building actuators and powering devices. Science 80(317), 1366–1370 (2007)CrossRefGoogle Scholar
  2. 2.
    Grosberg, A., Alford, P.W., McCain, M.L., Parker, K.K.: Ensembles of engineered cardiac tissues for physiological and pharmacological study: Heart on a chip. Lab Chip 11(24), 4165 (2011)CrossRefGoogle Scholar
  3. 3.
    Vannozzi, L., Ricotti, L., Cianchetti, M., Bearzi, C., Gargioli, C., Rizzi, R., Dario, P., Menciassi, A.: Self-assembly of polydimethylsiloxane structures from 2D to 3D forbio-hybrid actuation. Bioinspir. Biomim. 10(5), 056001 (2015)CrossRefGoogle Scholar
  4. 4.
    Nagamine, K., Kawashima, T., Sekine, S., Ido, Y., Kanzaki, M., Nishizawa, M.: Spatiotemporally controlled contraction of micropatterned skeletal muscle cells on a hydrogel sheet. Lab Chip 11(3), 513–7 (2011)CrossRefGoogle Scholar
  5. 5.
    Nawroth, J.C., Lee, H., Feinberg, A.W., Ripplinger, C.M., McCain, M.L., Grosberg, A., Dabiri, J.O., Parker, K.K.: A tissue-engineered jellyfish with biomimetic propulsion. Nat. Biotechnol. 30(8), 792–797 (2012)CrossRefGoogle Scholar
  6. 6.
    Williams, B.J., Anand, S.V., Rajagopalan, J., Saif, M.T.A.: A self-propelled biohybrid swimmer at low Reynolds number. Nat. Commun. 5, 3081 (2014)Google Scholar
  7. 7.
    Xi, J., Schmidt, J.J., Montemagno, C.D.: Self-assembled microdevices driven by muscle. Nat. Mater. 4, 180–184 (2005)CrossRefGoogle Scholar
  8. 8.
    Chan, V., Park, K., Collens, M.B., Kong, H., Saif, T.A., Bashir, R.: Development of miniaturized walking biological machines. Sci. Rep. 2, 857 (2012)CrossRefGoogle Scholar
  9. 9.
    Cvetkovic, C., Raman, R., Chan, V., Williams, B.J., Tolish, M., Bajaj, P., Sakar, M.S., Asada, H.H., Taher, A., Taher A Saif, M., Bashir, R.: Three-dimensionally printed biological machines powered by skeletalmuscle. PNAS 111(28), 10125–10130 (2014)CrossRefGoogle Scholar
  10. 10.
    Kim, J., Park, J., Yang, S., Baek, J., Kim, B., Lee, S.H., Yoon, E.-S., Chun, K., Park, S.: Establishment of a fabrication method for a long-term actuated hybrid cell robot. Lab Chip 7, 1504–1508 (2007)CrossRefGoogle Scholar
  11. 11.
    Webster, V.A., Hawley, E.L., Akkus, O., Chiel, H.J., Quinn, R.D.: Fabrication of electrocompacted aligned collagen morphs for cardiomyocyte powered living machines. In: Wilson, S.P., Verschure, P.F.M.J., Mura, A., Prescott, T.J. (eds.) Living Machines 2015. LNCS, vol. 9222, pp. 429–440. Springer, Heidelberg (2015)CrossRefGoogle Scholar
  12. 12.
    Herr, H., Dennis, R.G.: A swimming robot actuated by living muscle tissue. J. Neuroeng. Rehabil. 1, 6 (2004)CrossRefGoogle Scholar
  13. 13.
    Baryshyan, A.L., Woods, W., Trimmer, B.A., Kaplan, D.L.: Isolation and maintenance-free culture of contractile myotubes from Manduca sexta embryos. PLoS One 7(2), e31598 (2012)CrossRefGoogle Scholar
  14. 14.
    Uesugi, K., Shimizu, K., Akiyama, Y., Hoshino, T., Iwabuchi, K., Morishima, K.: Contractile performance and controllability of insect muscle-powered bioactuator with different stimulation strategies for soft robotics. Soft Robot. 3(1), 13–22 (2016)CrossRefGoogle Scholar
  15. 15.
    Kandel, E.: Behavioral Biology of Aplysia: Contribution to the Comparative Study of Opistobranch Molluscs. W.H. Freeman and Company, San Francisco (1979)Google Scholar
  16. 16.
    Hurwitz, I., Neustadter, D., Morton, D.W., Chiel, H.J., Susswein, A.J.: Activity patterns of the B31/B32 pattern initiators innervating the I2 muscle of the buccal mass during normal feeding movements in Aplysia californica. J. Neurophysiol. 75(4), 1309–26 (1996)Google Scholar
  17. 17.
    Mizuta, S., Miyagi, T., Yoshinaka, R.: Characterization of the quantitatively major collagen in the mantle of oyster Crassostrea gigas. Fish. Sci. 71(1), 229–235 (2005)CrossRefGoogle Scholar
  18. 18.
    Matsumura, T.: Shape, size and amino acid composition of collagen fibril of the starfish asterias amurensisGoogle Scholar
  19. 19.
    Cheng, X.: Umut a Gurkan, Christopher J Dehen, Michael P Tate, Hugh W Hillhouse, Garth J Simpson, and Ozan Akkus.: An electrochemical fabrication process for the assembly of anisotropically oriented collagen bundles. Biomaterials 29(22), 3278–3288 (2008)CrossRefGoogle Scholar
  20. 20.
    Yu, S.N., Crago, P.E., Chiel, H.J.: Biomechanical properties and a kinetic simulation model of the smooth muscle I2 in the buccal mass of Aplysia. Biol. Cybern. 81, 505–513 (1999)CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Victoria A. Webster
    • 1
    Email author
  • Katherine J. Chapin
    • 1
  • Emma L. Hawley
    • 1
  • Jill M. Patel
    • 1
  • Ozan Akkus
    • 1
  • Hillel J. Chiel
    • 1
  • Roger D. Quinn
    • 1
  1. 1.Case Western Reserve UniversityClevelandUSA

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