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Review
Polarisation signals: a new currency for communication
N. Justin Marshall, Samuel B. Powell, Thomas W. Cronin, Roy L. Caldwell, Sonke Johnsen, Viktor Gruev, T.-H. Short Chiou, Nicholas W. Roberts, Martin J. How
Journal of Experimental Biology 2019 222: jeb134213 doi: 10.1242/jeb.134213 Published 7 February 2019
N. Justin Marshall
1Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, 4072, Australia
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  • For correspondence: Justin.marshall@uq.edu.au
Samuel B. Powell
1Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, 4072, Australia
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Thomas W. Cronin
2Department of Biological Sciences, University of Maryland Baltimore County, MD 21250, USA
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Roy L. Caldwell
3University of California Berkeley, Department of Integrative Biology, Berkeley, CA 94720-3140, USA
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Sonke Johnsen
4Department of Biology, Duke University, Durham, NC 27708-0338, USA
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Viktor Gruev
5Electrical and Computer Engineering, University of Illinois, Urbana, IL 61801, USA
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T.-H. Short Chiou
6Department of Life Sciences, National Cheng-Kung University, Tainan City 701, Taiwan
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Nicholas W. Roberts
7School of Biological Sciences, University of Bristol, Tyndall Avenue, Bristol BS8 1TQ, UK
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Martin J. How
7School of Biological Sciences, University of Bristol, Tyndall Avenue, Bristol BS8 1TQ, UK
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  • Fig. 1.
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    Fig. 1.

    Polarised light in the environment. (A) Polarisation camera images of a terrestrial scene, a waxy-leafed bush with a small cut-out polaroid fish-shape on one leaf (arrow). Left: intensity (black and white image). Centre: degree (%) polarisation, scale 0–100%, blue to white with deep-red at ∼45%, the limit of most natural polarised signals. Right: angle or e-vector direction, the circular key shows, for example, orange/red as horizontal and cyan as vertical (camera details in Gruev et al., 2010 and Johnsen et al., 2016). Note the potential polarocryptic camouflage of ‘fish’ under these circumstances. (B) The same cut-out polaroid fish in a shaded-grass background with a low degree of polarisation, showing the potential for polarisation contrast and signalling. (C) Left: diagrammatic representation of the horizontal band of polarisation underwater at midday with the sun above, and the tilt of polarisation at low sun angles (modified from Hawryshyn, 1992). Centre and right: a typical reef scene at mid–late afternoon, approximately corresponding to the tilted angle in the left-most panel (scales as in A). Note the low degree of polarisation of reef substrate and high degree of background water. (D) A mud flat environment with a fiddler crab with a dry and contrasting claw. Scales and images are similar to those in A, but the left image is in normal colour. Note slightly different colour scale in middle panel so the background mudflat is ∼45%.

  • Fig. 2.
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    Fig. 2.

    Polarisation photoreceptors in a variety of species. (A) Fiddler crab (Uca polita; photo courtesy of Jochen Zeil) and diagrammatic 3D structure of a typical crustacean rhabdom showing interdigitating orthogonal microvilli (Centre–after Stowe, 1983) seen in transmission electron micrograph (TEM) in longitudinal section (right). Scale bar here and in TEMs below: 0.2 µm. Red arrows here and below denote bidirectional angle sensitivity. (B) Squid Loligo paelei along with a 3D diagrammatic representation of abutting orthogonal microvilli in its photoreceptors (middle; after Moody and Parriss, 1961) and the retina mounted flat with local photoreceptor angles superimposed to show V- and H-orientation relative to the eye view of the environment (right) (Talbot and Marshall, 2011). (C) Swallowtail butterfly Papilio xuthus (photo and TEM courtesy of Kentaro Arikawa), 2D diagrammatic representation of ventral retina proximal photoreceptor in transverse section (centre) and TEM of microvilli (right). (D) Details of circular polarisation sensitivity in stomatopod retina showing the eye and mid-band region, a diagram of longitudinal section of the retina through mid-band from the area indicated by the line on photograph of the eye, the position of the specialised R8 photoreceptors in mid-band rows 5 and 6, TEM of the unidirectional microvilli of this photoreceptor (top right) and arrows to a diagrammatic representation of its quarter-wave retardation optical ability, converting circularly polarised light to linearly polarised light that is absorbed by photoreceptors below (Chiou et al., 2008b). The graph shows the remarkable spectral flatness resulting from this retardance (Roberts et al., 2009).

  • Fig. 3.
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    Fig. 3.

    Linear polarisation signals in cephalopods. (A) Sepia latimanus, the broad-club cuttlefish. (B) Polarisation video images (as detailed in Fig. 1) showing highly polarised arm-stripe signals in the centre (% polarisation) panel. (C) Details of arm-stripe reflector in cephalopods, reflectance (top graph) and % polarisation (bottom graph) measured at several angles of tilt. The similar % or degree of polarisation at all angles of measurement clearly shows the independence of this signal to angles of view also. The thick green curve shows the spectral sensitivity of cuttlefish, showing a good match to maximum polarisation efficiency at ∼500 nm. TEM of arm-stripe iridophores showing localised random reflection direction allowing the angle independence of % polarisation (Chiou et al., 2007). Scale bar: 7.5 µm.

  • Fig. 4.
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    Fig. 4.

    Linear polarisation signals in stomatopods. (A) Odontodactylus scyllarus (photo courtesy of Roy Caldwell) showing polarising antennal scales (B) photographed through H and V linear polarising filters denoted by white arrows. Maximal % polarisation is reached at a ∼45 deg tilt angle of the scale (far right pair and appearing dark red to the vertical analyser) and is measured in related species in C (blue line). Green line shows that linear polarisation receptor spectral sensitivity is matched to polarisation reflection spectral efficiency in many stomatopods, as in cuttlefish (Fig. 3C), with peak sensitivity close to 500 nm (Chiou et al., 2012). (D) Haptosquilla trispinosa polarisation images (scales as in Fig. 1) showing highly H-polarised segments of maxillipeds corresponding to blue areas in E (photo courtesy of Roy Caldwell) and F (inset). (F) TEM of the elongated vesicular structure of the blue polarised maxillipeds of H. trispinosa: an anisotropic, dichroic, scattering nanostructure (Jordan et al., 2016). Scale bar: 0.5 µm.

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    Fig. 5.

    Functional and probable non-functional linear polarisation signals. (A) Heliconius cydno, a nymphalid butterfly, in colour and % polarisation image (right, scale similar to Fig. 1). (B) Preferential mate choice frequency of males given females to interact with under normal polarising conditions and with a de-polarising filter placed over the wings (Sweeney et al., 2003). Bars indicate s.e.m. (C) The butterfly Curetis acuta with wings closed is thought to achieve polarisation and colour camouflage among leaves in shade by reflecting both to match the background, probably in a similar manner to that shown in Fig. 1A. (D) The toby pufferfish (Canthigaster papua), in common with many marine and freshwater fish, displays iridescent coloured markings that are also polarising. This includes the iridescent cornea and blue areas that, while having colour and eye-shade function (Lythgoe and Shand, 1982), are most likely non-functional polarisation signals that are not visible to this and other fish that lack polarisation vision.

  • Fig. 6.
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    Fig. 6.

    Circular polarisation signals in stomatopods. Odontodactylus cultrifer has both linear and polarising reflections. (A) Linear reflections from abdominal and thoracic areas shown by photographing through linear H- and V-polarising filters (denoted by arrows). Note that the telson keel area does not alter reflectance (boxed area). (B) Keel from the boxed area in A shown in detail and photographed through left- and right-handed circular polarising filters. The colour change indicates circular polarising activity. (C) Section of keel showing a red-orange layer, which is presumed to be an astaxanthin linear reflector (Chiou et al., 2012), and a clear layer, which is presumed to be a quarter-wave retarder with its fast axis at 45 deg to the linear reflector underneath, resulting in circular reflection. Note that circular polarisation is not from a chiral structure as known in beetles (Vukusic and Sambles, 2004). (D) A diagram showing the currently assumed structure of the keel-reflector, in cross section (centre), that allows left-handed reflection from one side and right-handed reflection from the other.

  • Fig. 7.
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    Fig. 7.

    Behavioural assessment of polarisation vision in the lab. (A) A fiddler crab on a floating ball treadmill and a polar-graph of the escape reaction (histogram showing the number of runs and their direction) to looming stimuli presented to the crab from a computer monitor that shows polarisation contrast only. Animals without polarisation vision see no image on the screen (Pignatelli et al., 2011; How et al., 2012). (B) The same experiment for cuttlefish; again, the looming stimulus is only visible to polarisation-sensitive animals. (C) The cuttlefish reacts to the loom shown by skin-pattern change (split-screen image of pattern before and after loom, top and bottom, respectively). (D) Graph showing high sensitivity of cuttlefish to polarisation angle difference of the stimulus down to 1.5 deg (Temple et al., 2012). Bars show s.e.m. (E) Feeding containers with linear polarising filters (top) that are invisible until photographed through a V-polarising filter (bottom). The white lines were drawn after to show the angle orientation of the filters. (F) A stomatopod handling a feeding container in a choice test where both linear polarisation e-vector angle (as in E) and circular polarisation handedness can be discriminated. (G) Results for animals trained to left- and right-handed reflecting feeding containers, as indicated by L or R. Asterisks indicate statistical significance based on a Fisher’s exact test (Marshall et al., 1999a; Chiou et al., 2008b).

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    Fig. 8.

    Midwater camouflage and lack of polarocrypsis. (A) A diver among superbly camouflaged silvery big-eye trevally, Caranx sexfasciatus. The fish are also imaged using a polarising camera below (see Fig. 1 legend for explanation of scales). In intensity and colour, the reflective camouflage mechanism functions well, but it breaks down in % polarisation (Johnsen et al., 2016). (B) Ratio of % polarisation of fish and background water in 8 species of silvery fish (Johnsen et al., 2016 and see Fig. S1) showing that silvery fish do not return polarised reflections (Brady et al., 2013, 2015), as also predicted theoretically (Jordan et al., 2012). Animals with polarisation vision would therefore break this form of camouflage, suggesting that polarocrypsis, in this context, does not work. Key: red, Caranx sexfasciatus; black, Sphyraena qenie; blue, Pseudocaranx dentex; bright green, Trachinotus blochii; dark green, Caranx melampygus; yellow, Gnathanodon speciosus; grey, Pterocaesio marri; orange, Fistularia commersonii.

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  • Signalling
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Review
Polarisation signals: a new currency for communication
N. Justin Marshall, Samuel B. Powell, Thomas W. Cronin, Roy L. Caldwell, Sonke Johnsen, Viktor Gruev, T.-H. Short Chiou, Nicholas W. Roberts, Martin J. How
Journal of Experimental Biology 2019 222: jeb134213 doi: 10.1242/jeb.134213 Published 7 February 2019
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Review
Polarisation signals: a new currency for communication
N. Justin Marshall, Samuel B. Powell, Thomas W. Cronin, Roy L. Caldwell, Sonke Johnsen, Viktor Gruev, T.-H. Short Chiou, Nicholas W. Roberts, Martin J. How
Journal of Experimental Biology 2019 222: jeb134213 doi: 10.1242/jeb.134213 Published 7 February 2019

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  • Top
  • Article
    • ABSTRACT
    • Introduction
    • Polarised light
    • Polarisation vision
    • Polarisation in aquatic environments
    • Polarising signals and polarisation information
    • Polarised food
    • Mate choice, habitat choice, polarisation and colour
    • Signal orientation, confounding parameters and polarisation contrast
    • Polarisation camouflage
    • Circular polarisation and the case for covert communication
    • A guide to studying polarisation signalling
    • Conclusions
    • FOOTNOTES
    • References
  • Figures & tables
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