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Polarisation Vision of Crustaceans

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Polarized Light and Polarization Vision in Animal Sciences

Part of the book series: Springer Series in Vision Research ((SSVR,volume 2))

Abstract

The photoreceptor design of crustaceans, often containing regular arrays of intrinsically polarisation-sensitive microvilli, has had a profound influence on the visual biology of this subphylum. The land-based arthropods (insects and arachnids) also construct photoreceptors from ordered microvilli; however while in many species polarisation sensitivity results, a general overview of these groups suggests a major difference. With notable exceptions discussed in this chapter, many crustaceans seem to have “invested” in polarisation vision more than colour vision. This may be the result of the relatively limited spectral environment found in much of the aquatic world or due to the information content in polarisation being as useful as colour. The terrestrial arthropods are generally trichromatic with specialised visual areas for polarisation-specific tasks. Crustaceans are mostly di- or monochromats and most of their visual field displays polarisation sensitivity. This chapter examines the anatomical, neurophysiological and behavioural evidence for polarisation vision in a few of the many crustacean groups. Common themes are emerging such as the possession of vertical and horizontal E-vector sensitivity. This two-channel orthogonality is carried through the neural processing of information and reflected in behavioural capability. A few groups such as the stomatopods possess both complex colour and polarisation sensitivity, and particularly in this group, the evolutionary pressures responsible are centred on unique polarisation signalling structures used in social interaction. Other functions of polarisation sensitivity in crustaceans include navigation, phototaxis and potentially increasing visual range through de-hazing in a turbid world.

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Authors and Affiliations

  1. Sensory Neurobiology Group, Queensland Brain Institute, University of Queensland, St Lucia, Brisbane, QLD, 4072, Australia

    Justin Marshall

  2. Department of Biological Sciences, University of Maryland, Baltimore County, 1000 Hilltop Circle, Baltimore, MD, 21 250, USA

    Thomas Cronin

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Correspondence to Justin Marshall .

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  1. Environmental Optics Laboratory, Dept. Biological Physics, Eötvös University, Budapest, Hungary

    Gábor Horváth

1 Electronic Supplementary Material

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Colour Version of Fig. 7.1

Rhabdom construction in crustaceans. (a) Generalised apposition compound eye, ommatidium and diagrammatic three-dimensional transverse section through rhabdomere (in part after Kirschfeld 1976; Stowe 1977 and courtesy of Mike Bok). R1–R7 cells numbered and orthogonal microvilli made by opposite rhabdomeres and resultant E-vector sensitivities (double-headed arrows) coloured yellow and blue. (b) Transmission electron micrograph detail of orthogonal microvilli in longitudinal section from stomatopod. Scale 0.2 μm (CDR 396 kb)

Colour Version of Fig. 7.2

Orientation of crustacean microvilli relative to outside world is maintained horizontal vertical. (a) Fiddler crab female Uca vomeris (Photograph, Martin How) and inset close-up of fiddler crab eye (Photograph, Jochen Zeil). Note although body is tilted, eyes remain vertical to local substrate. (b) Light micrograph transverse section through equatorial R1–R7 rhabdoms of fiddler crab with insets showing enlarged single rhabdom (left) and diagrammatic representation of single rhabdom (right) [after Alkaladi et al. (2013) and Marshall et al. (1991a)]. White arrows denote E-vector sensitivity directions and microvillar directions (CDR 136 kb)

Colour Version of Fig. 7.4

Orientation of microvilli relative to outside world in stomatopod eye with mid-band oriented horizontal. (a) Right eye of O. scyllarus showing expanded portion of ventral periphery with diagrammatic transverse sections through R8 (left) and R1–R7 (right) cell rhabdom levels. (b) Semi-thin (2 μm) transverse section through mid-band and peripheral retina in Coronis excavatrix at transition between R8 and R1–R7 cell level and diagrammatic representation of rhabdoms (right) and microvillar directions/E-vector sensitivities (double-headed arrows), in various eye regions. Only R8 cells show in dorsal and ventral periphery. Grey shaded areas: R8 cell and microvillar orthogonality in rows 1–4 reduces PS. Green shaded area: CPS cells in Odontodactylus species and LPS in e.g. Gonodactylus chiragra. Blue shaded areas: 500 nm blue/green LPS cells. Violet shaded area: UV-sensitive R8 cells. Inset: red bounded diagram is erroneous representation of three-directional rhabdomal unit previously published (Marshall 1988). VP: ventral periphery, DP: Dorsal periphery, DR1–R7: distal R1–R7 cells, PR1–R7: proximal R1–R7 cells. Scale 100 μm. (c) Extensive rotational eye movements of O. Scyllarus eye in diagrammatic form. Eyes are most often held close to 40° (CDR 166 kb)

Colour Version of Fig. 7.7

Aspects of circular polarisation vision in stomatopods. (a) Diagram of longitudinal section through stomatopod ommatidia including mid-band rows 1–6 and representative ommatidia from dorsal and ventral hemispheres (DH, VH) or peripheral regions. (b) Rows 5 and 6 that construct CPS in semi-thin section at transition between oval profile R8 cells and diamond profile R1–R7 cells. Scale 10 μm. (c) Diagrammatic representation of row 6 rhabdom. As circular polarised light passes through R8 cells, it is converted through 1/4 wave retardation to linearly polarised light in one of two directions, depending on CPL handedness. The R1–R7 cells of these rows are in the correct orientation to absorb this ongoing light, being set at 45° to the R8 cell’s fast axis [after Chiou et al. (2011)]. (d) Transmission electron micrograph of R8 cell in row 6 in transverse (left) and longitudinal section (right) showing unidirectional microvilli. This cell has dual function as 1/4 wave retarder and UV linear PS as shown by violet double-headed arrow (Fig. 7.11). Scale 1 μm at left, 0.2 μm at right. (e) Transmission electron micrograph of R1–R7 cells in row 6 in transverse (left) and longitudinal section (right) showing orthogonal microvilli that are sensitive to CPL in Odontodactylus species and LPL in Gonodactylus chiragra. Scale 2 μm at left, 0.2 μm at right (CDR 334 kb)

Colour Version of Fig. 7.8

Behavioural tests showing E-vector and CPL handedness discrimination in stomatopod Odontodactylus scyllarus. (a) Experimental paradigm to demonstrate linear E-vector discrimination in O. scyllarus from cube-shaped food containers with polarising filters glued to one side, top: no camera filter, mid: vertical polarising filter to show different feeding cubes and bottom with E-vector lines drawn on photograph. Stomatopods can learn to choose vertically polarised from horizontally polarised food containers. Right: stomatopod reaching inside a smashed open feeding container (after Marshall et al. 1999). (b) Details of CPL paradigm. Top: construction of feeding containers with polarising filter and 1/4 wave plate glued to end. Other end is sealed with coverslip after food is placed inside and animal must choose and break open tube with handedness of CPL trained to. Middle: Feeding containers photographed through left- and right-handed CP filters and no filter (as we see them). Bottom: Graph of choices (correct black and incorrect grey out of an array of three feeding tubes where one was correct choice) of 7 animals trained to left- or right-handed CP feeding containers. Stars indicate statistical significance [after Chiou et al. (2008)] (CDR 230 kb)

Colour Version of Fig. 7.9

Animals living in close association with horizontal reflective surfaces, such as fiddler crabs Uca sp., may experience and utilise a strong horizontally polarised large field. (a) Waving coloured and possibly polarised claw. (b) In the ventral part of the eye of Uca signata, more vertical than horizontal microvilli are found per band and may reduce glare from horizontal mud-flat habitat [after Alkaladi et al. (2013)] (CDR 172 kb)

Colour Version of Fig. 7.13

Gross morphology of chloral hydrate stained stomatopod optic neuropils showing partition of colour and polarisation. (a) The eye of a gonodactyloid stomatopod. Scale 1 mm. (b) Semi-thin section of eye in same orientation as a. (c) Transverse section at lamina cartridge level (dotted line in b showing segregation of lamina under each retinal subsection and differing cartridge morphologies. Scale 70 μm. (e) Enlargement of area boxed in b showing separate accessory lobes of ME and MI dedicated to MB. Scale 100 μm. (e, f) Section and drawing of section of proximal portion of retina and neuropils, mapping of mid-band rows and separation of polarisation information. The single accessory lobe in ME appears in two areas due to its curvature in and out of section plane. Lines show representative R8 cell axonal projections. Scale 100 μm. c: cornea, MB: mid-band retina, DH, VH: dorsal and ventral hemispheres or peripheral retina, LA: lamina, ME: medulla externa, MI: medulla interna = part of lobular complex, Ch1,Ch2: chiasmata between neuropils, Acc: Accessory lobes of ME or MI from mid-band [modified from Kleinlogel et al. (2003) and Marshall et al. (2007)] (CDR 101 kb)

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Marshall, J., Cronin, T. (2014). Polarisation Vision of Crustaceans. In: Horváth, G. (eds) Polarized Light and Polarization Vision in Animal Sciences. Springer Series in Vision Research, vol 2. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-54718-8_7

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