Colour vision in stomatopod crustaceans

Abstract

The stomatopod crustaceans, or mantis shrimps, are colourful marine invertebrate predators. Their unusual compound eyes have dorsal and ventral regions resembling typical crustacean apposition designs separated by a unique region called the midband that consists of from two to six parallel rows of ommatidia. In species with six-row midbands, the dorsal four rows are themselves uniquely specialized for colour analysis. Rhabdoms of ommatidia in these rows are longitudinally divided into three distinct regions: an apical ultraviolet (UV) receptor, a shorter-wavelength middle tier receptor and a longer-wavelength proximal tier receptor. Each of the total of 12 photoreceptors has a different spectral sensitivity, potentially contributing to a colour-vision system with 12 channels. Mantis shrimps can discriminate both human-visible and UV colours, but with limited precision compared to other colour-vision systems. Here, we review the structure and function of stomatopod colour vision, examining the types of receptors present in a species, the spectral tuning of photoreceptors both within and across species, the neural analysis of colour and the genetics underlying the multiple visual pigments used for colour vision. Even today, after many decades of research into the colour vision of stomatopods, much of its operation and its use in nature remain a mystery. This article is part of the theme issue 'Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods'.

Keywords: colour vision; filtering; stomatopod; ultraviolet vision; visual ecology; visual genetics.

Figure 1.

(a) A typical Caribbean reef stomatopod, Neogonodactylus oerstedii. (b) A close-up view of one of its compound eyes, showing the dorsal hemisphere (DH) and ventral hemsphere (VH), which together make up the peripheral ommatidia of the eye, and the six-row midband (MB). (c) A schematic diagram to show the organization of each ommatidium in the hemispheres and the midband. Midband rows are numbered 1 to 6, from dorsal to ventral. The colour-vision region of the eye is thought to be contained in the tiered Rows 1 to 4. The retinular cells are coloured to show the spectral region absorbed by the visual pigment they contain (UV-sensitive cells are coloured grey or black). CC: crystalline cone; Co: cornea. (d) Absorbance spectra of all 12 visual pigments in this eye as measured by microspectrophotometry (MSP). Visual pigment spectra are coloured to approximately match the spectral range absorbed by each pigment (the same colours show where they are expressed in (c) [6]); norm. abs., normalized absorbance.

Figure 2.

(a) Sensitivities of the colour-sensitive photoreceptors in the dorsal four rows of the midband of N. oerstedii compound eyes, obtained from intracellular recordings [–28]. The retinal region where each sensitivity was measured is indicated by the corresponding colour in the diagram to the right. Note that the spectral sensitivity of the R8 cell in Row 3 is not yet known; it is marked black because it contains the short UV (334 nm) visual pigment. (b) Absorbance spectra of photostable filter pigments (carotenoproteins and mycosporine-like amino acids (MAAs)) in the retina of N. oerstedii. The curves are coloured to match the appearance of the filter to the human eye (UV filters, which are invisible to a human, are indicated in greyscale) and filter locations are revealed by corresponding colours or grey levels in the diagram to the right.

Figure 3.

Peak sensitivities in colour photoreceptors of 12 stomatopod species from various habitats. Each group of points represents the sensitivity maxima of the 12 retinas in the retinal region indicated at the bottom of the figure, coloured to match the approximate spectral peak of receptors in that retinal region. Point types vary by primary habitat of the species: intertidal, open circles; shallow subtidal (less than 5 m), hatched circles; species found in a range of depths from shallow to deep, half-filled circles; deep water (greater than 5 m), fully filled circles. (After [30].) M, middle tier; P, proximal tier.

Figure 4.

Tissue expression patterns of colour opsins in N. oerstedii revealed by in situ hybridization. Expressions are grouped into opsin types: SWS, short-wavelength and UV sensitive; MWS, middle-wavelength sensitive; LWS, long-wavelength sensitive. A schematic showing the dorsal four rows of the midband is placed above each expression panel; see description in figure 1 caption. In this schematic, the expression location of the associated opsin is indicated by the coloured region. Colours suggest the approximate part of the spectrum for which that retinal region is responsible; black indicates UV. See §7 for details [6].