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A multilayer mechanism of omnidirectional reflection in silvery pelagic fish

Tom Jordan1, 2*, Nicholas Roberts1 and Julian Partridge1
  • 1 University of Bristol, School of Biological Sciences, United Kingdom
  • 2 Bristol Centre for Complexity Sciences, United Kingdom

Silvery reflections from pelagic fish are produced by a multilayer “stack” of birefringent guanine crystals with cytoplasm gaps. These reflecting structures provide camouflage in the near-axially symmetric underwater pelagic light field, with reflections from the sides of the fishes matching the rays from behind [1]. For optimal concealment, the reflecting structures must be able to produce spectrally broadband and omnidirectional (non-polarizing) reflectivity. Mechanisms capable of producing spectrally broadband reflectivity are well understood [2,3]. However the low polarization, near-omnidirectional reflections reported in previous experimental studies lack an optical explanation [4].

Here we report a novel multilayer mechanism of omnidirectional reflection in silvery pelagic fish. Using reflectance spectrophotometry, we detail the reflectance spectra from two species of fish, Clupea harengus and Sardina pilchardus, and we characterize the polarization dependence of those spectra as a function of angle of incidence. We further measure the birefringent properties of individual guanine crystals from both species and discover that in the reflecting argenteum there are two distinct populations of crystal morphology. From these experimental results we develop an optical model based upon anisotropic reflectivity coefficients [5], that correctly incorporates the birefringence of the guanine crystals in the multilayer structure. We establish that the neutralization of the polarization over the whole visible range and at all angles of incidence is due to both a variation in optical thickness of the layers and a mixture of orientations of the optic axis of the birefringent guanine layers.

This polarization behavior uncovered in our study is very different to existing isotropic optical models of guanine-cytoplasm multilayers, which predict full polarization at Brewster’s angle. Our study demonstrates that polarization properties can be controlled by the orientation of the crystals in the multilayer, with both a fully polarizing Brewster’s angle and an entirely polarization-neutral omnidirectional reflection possible from different orientation arrangements. These findings have important consequences for our understanding of sensory adaptations related to how animals control the reflection of polarized light, and there is wide potential for the ideas to influence current debates in vision ecology upon polarization camouflage and polarization signaling.

Acknowledgements

The authors acknowledge support from the BBSRC (grant no. BB/G022917/1), the EPSRC 334 (grant no. EP/E501214/1) and the Air Force Office of Scientific Research (grant no. FA- 335 9550-09-1-0149).

References

[1] Denton, E. J. Review Lecture: On the Organization of Reflecting Surfaces in Some Marine Animals. Philosophical Transactions of the Royal Society B: Biological Sciences 258(824), 285–313, 1970.

[2] Denton, E. J. and Land, M. F. Mechanism of reflexion in silvery layers of fish and cephalopods. Proceedings of the Royal Society of London. Series B 178(50), 43–61 1971.

[3] McKenzie, D. R., Yin, Y., and McFall, W. D., “Silvery Fish Skin as an Example of a Chaotic Reflector,” Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences 451, 579–584, 1995.

[4] Denton, E. J. and Nicol, J. Polarization of light reflected from the silvery exterior of the bleak, Alburnus alburnus. Journal of the Marine Biological Association of the United Kingdom 45(03), 705–709 (1965).

[5] Weber, M. F., Stover, C. A., Gilbert, L., Nevitt, T., and Ouderkirk, A., “Giant Birefringent Optics in Multilayer Polymer Mirrors,” Science 287, 2451–2456, 2000.

Keywords: Birefringence, Camouflage, fish, Omnidirectional, polarization, Reflector

Conference: Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.

Presentation Type: Poster (but consider for participant symposium and student poster award)

Topic: Sensory: Vision

Citation: Jordan T, Roberts N and Partridge J (2012). A multilayer mechanism of omnidirectional reflection in silvery pelagic fish. Conference Abstract: Tenth International Congress of Neuroethology. doi: 10.3389/conf.fnbeh.2012.27.00117

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Received: 25 Apr 2012; Published Online: 07 Jul 2012.

* Correspondence: Mr. Tom Jordan, University of Bristol, School of Biological Sciences, Bristol, BS8 1UG, United Kingdom, tj9717@bris.ac.uk