Hanlon Lab – Colorful Skin: Changeable Pigments, Reflectors & 3D Shape

The colorful and changeable skin of cephalopods is an elegant arrangement of pigments and reflectors. We are interested in their gross and fine morphology, their control and their optical output. Octopus and cuttlefish have the unique ability for “shape shifting” skin; that is, controllable papillae that can render the skin bumpy or smooth to any degree. A wide variety of techniques is used to accomplish this research: light, electron and confocal microscopy; macrophotography and videography; underwater photography; electrophysiology, neuronal staining and tracing; and spectrometry (in the lab and the field). We collaborate with artists, modelers, materials scientists and engineers to determine how cephalopods may inspire the development of novel materials such as fabrics and cosmetics.

iBioSeminar: Changeable Skin (31:00 min)

Publications on skin ultrastructure and neurobiology:

Kingston, A. C. N., Kuzirian, A. M., Hanlon, R. T., & Cronin, T. W. (2015). Visual phototransduction components in cephalopod chromatophores suggest dermal photoreception. The Journal of Experimental Biology, 218(Pt 10), 1596–602. doi: 10.1242/jeb.117945

Kripke, E., Senft, S., Mozzherin, D., & Hanlon, R. (2015). Visualizing Biological Complexity in Cephalopod Skin: A Synergy of Art and Science Technologies. Leonardo, 48(5), 486–487. doi: 10.1162/LEON_a_01124

Kingston, A. C., Wardill, T. J., Hanlon, R. T., & Cronin, T. W. (2015). An Unexpected Diversity of Photoreceptor Classes in the Longfin Squid, Doryteuthis pealeii. PLoS One, 10(9). doi: 10.1371/journal.pone.0135381

Allen, J. J., Akkaynak, D., Sugden, A. U., & Hanlon, R. T. (2015). Adaptive body patterning, three-dimensional skin morphology and camouflage measures of the slender filefish Monacanthus tuckeri on a Caribbean coral reef. Biological Journal of the Linnean Society, 116(2), 377–396. doi: 10.1111/bij.12598

Yu, C., Li, Y., Zhang, X., Huang, X., Malyarchuk, V., Wang, S., Shi, Y., Gao, L., Su, Y., Zhang, Y., Xu, H., Hanlon, R. T., Rogers, J. A. (2014). Adaptive optoelectronic camouflage systems with designs inspired by cephalopod skins. Proceedings of the National Academy of Sciences of the United States of America, 111(36), 12998–13003. doi: 10.1073/pnas.1410494111

Bell, G. R. R., Mäthger, L. M., Gao, M., Senft, S. L., Kuzirian, A. M., Kattawar, G. W., & Hanlon, R. T. (2014). Diffuse white structural coloration from multilayer reflectors in a squid. Advanced Materials, 26(25), 4352–6. doi: 10.1002/adma.201400383

Gonzalez-Bellido, P. T., Wardill, T. J., Buresch, K. C., Ulmer, K. M., & Hanlon, R. T. (2014). Expression of squid iridescence depends on environmental luminance and peripheral ganglion control. Journal of Experimental Biology, 217(Pt 6), 850–858. doi: 10.1242/jeb.091884

Allen, J. J., Bell, G. R. R., Kuzirian, A. M., Velankar, S. S., & Hanlon, R. T. (2014). Comparative Morphology of Changeable Skin Papillae in Octopus and Cuttlefish. Journal of Morphology, 275(4), 371–390. doi: 10.1002/jmor.20221

Deravi, L. F., Magyar, A. P., Sheehy, S. P., Bell, G. R. R., Mäthger, L. M., Senft, S. L., Wardill, T.J., Lane, W.S., Kuzirian, A.M., Hanlon, R.T., Hu, E.L., & Parker, K. K. (2014). The structure-function relationships of a natural nanoscale photonic device in cuttlefish chromatophores. Journal of the Royal Society, Interface / the Royal Society, 11(93), 20130942. doi: 10.1098/rsif.2013.0942

Mäthger, L. M., Senft, S. L., Gao, M., Karaveli, S., Bell, G. R. R., Zia, R., … Hanlon, R. T. (2013). Bright White Scattering from Protein Spheres in Color Changing, Flexible Cuttlefish Skin. Advanced Functional Materials, 23(32), 3980–3989. doi: 10.1002/adfm.201203705

Allen, J. J., Bell, G. R. R., Kuzirian, A. M., & Hanlon, R. T. (2013). Cuttlefish skin papilla morphology suggests a muscular hydrostatic function for rapid changeability. Journal of Morphology, 274(6), 645–56. doi: 10.1002/jmor.20121

Bell, G. R. R., Kuzirian, A. M., Senft, S. L., Mäthger, L. M., Wardill, T. J., & Hanlon, R. T. (2013). Chromatophore radial muscle fibers anchor in flexible squid skin. Invertebrate Biology, 132(2), 120–132. doi: 10.1111/ivb.12016

Kreit, E., Mäthger, L. M., Hanlon, R. T., Dennis, P. B., Naik, R. R., Forsythe, E., & Heikenfeld, J. (2013). Biological versus electronic adaptive coloration: how can one inform the other? Journal of the Royal Society, Interface / the Royal Society, 10(78), 20120601. doi: 10.1098/rsif.2012.0601

Wardill, T. J., Gonzalez-Bellido, P. T., Crook, R. J., & Hanlon, R. T. (2012). Neural control of tuneable skin iridescence in squid. Proceedings. Biological Sciences / The Royal Society, 279(1745), 4243–52. doi: 10.1098/rspb.2012.1374

Mäthger, L. M., Bell, G. R. R., Kuzirian, A. M., Allen, J. J., & Hanlon, R. T. (2012). How does the blue-ringed octopus (Hapalochlaena lunulata) flash its blue rings? The Journal of Experimental Biology, 215(Pt 21), 3752–7. doi: 10.1242/jeb.076869

Izumi, M., Sweeney, A.M., DeMartini, D., Weaver, J. C., Powers, M.L., Tao, A., Silvas, T.V., Kramer, R.M., Crookes-Goodson, W.J., Mäthger, L.M., Naik, R.R., Hanlon, R.T., & Morse, D.E., 2010. Changes in reflectin protein phosphorylation are associated with dynamic iridescence in squid. J. Royal Society Interface 7: 549-560.

Mäthger, L.M., Denton, E.J., Marshall, J., & Hanlon, R.T. 2009. Mechanisms and behavioral functions of structural coloration in cephalopods. Journal of the Royal Society Interface 6: S149-S164.

Mäthger, L.M., Shashar, N., & Hanlon, R.T. 2009. Do cephalopods communicate using polarized light reflections from their skin? Journal of Experimental Biology 212: 2133-2140. (Featured Commentary)

Allen, J.J., Mäthger, L.M., Barbosa, A., & Hanlon, R.T. 2009. Cuttlefish use visual cues to control 3-dimensional skin papillae for camouflage. Journal of Comparative Physiology A 195: 547-555.

Miserez, A., Weaver, J.C., Pedersen, P.B., Schneeberk, T., Hanlon, R.T., Kisailus, D., & Birkedal, H. 2008. Microstructural and biochemical characterization of the nano-porous sucker rings from Dosidicus gigas. Advanced Materials 20: 1-6.

Mäthger, L.M., Denton, E.J., Marshall, J., & Hanlon, R.T. 2008. Mechanisms and behavioral functions of structural coloration in cephalopods. Journal of the Royal Society Interface 6: S149-S164.

Sutherland, R.L., Mäthger, L.M., Hanlon, R.T., Urbas, A.M., & Stone, M.O. 2008. Cephalopod coloration model. I. Squid chromatophores and iridophores. Journal of the Optical Society of America, 25 (3): 588-599.

Sutherland, R.L., Mäthger, L M., Hanlon, R.T., Urbas, A.M., & Stone, M.O. 2008. Cephalopod coloration model. II. Multiple layer skin effects. Journal of the Optical Society of America, 25 (8): 2044-2054.

Chiou, T.H., Hanlon, R.T., Mäthger, L.M., & Cronin, T.W. 2007. Spectral and spatial properties of the polarized light reflections on the arms of squid (Loligo pealeii) and cuttlefish (Sepia officinalis L.). Journal of Experimental Biology. 210: 3624-3635.

Mäthger, L.M., & Hanlon, R.T. 2007. Malleable skin coloration in cephalopods: selective reflectance, transmission and absorbance of light by chromatophores and iridophores. Cell and Tissue Research 329: 179-186.

Mäthger, L.M., Barbosa, A., Miner, S., & Hanlon, R.T. 2006. Color blindness and contrast perception in cuttlefish (Sepia officinalis). Vision Research 46: 1746-1753.

Saidel, W.M., Shashar, N., Schmolesky, M.T., & Hanlon, R.T. 2005. Discriminative responses of squid (Loligo pealeii) photoreceptors to polarized light. Comparative Biochemistry & Physiology A: 142/3: 340-346.

Shashar, N., Borst, D.T., Ament, S.A., Saidel, W.M., Smolowitz, R.M., & Hanlon, R.T. 2001. Polarization reflecting iridophores in the arms of the squid Loligo pealeii. Biol. Bull. 201:267-268.

Hanlon, R.T., Cooper, K.M., Budelmann, B.U., & Pappas, T.C. 1990. Physiological color change in squid iridophores I. Behavior, morphology and pharmacology in Lolliguncula brevis. Cell Tissue Res. 259(1): 3-14.

Cooper, K.M., Hanlon, R.T., & Budelmann, B.U. 1990. Physiological color change in squid iridophores II. Ultrastructural mechanisms in Lolliguncula brevis. Cell Tissue Res. 259(1): 15-24.

Novicki, A., Budelmann, B.U., & Hanlon, R.T. 1990. Brain pathways of the chromatophore system in the squid Lolliguncula brevis. Brain Res. 519(1- 2): 315-323.

Cooper, K.M., & Hanlon, R.T. 1986. Correlation of iridescence with changes in iridophore platelet ultrastructure in the squid Lolliguncula brevis. J. exp. Biol. 121: 451-455.

Dubas, F., Hanlon, R.T., Ferguson, G.P., & Pinsker, H.M. 1986. Localization and stimulation of chromatophore motoneurones in the brain of the squid, Lolliguncula brevis. J. exp. Biol. 121: 1-25.

Dubas, F., Leonard, R.B., & Hanlon, R.T. 1986. Chromatophore motoneurons in the brain of the squid, Lolliguncula brevis: An HRP study. Brain Res. 374(1): 21-29.

Florey, E., Dubas, F., & Hanlon, R.T. 1985. Evidence for L-glutamate as a transmitter substance of motoneurons innervating squid chromatophore muscles. Comp. Biochem. Physiol. C. 82(2): 259-268.

Hanlon, R.T. 1982. The functional organization of chromatophores and iridescent cells in the body patterning of Loligo plei (Cephalopoda: Myopsida). Malacologia 23(1): 89-119.