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The Colourful World of the Mantis Shrimp the Colour-Vision System of These Crustaceans Includes Four Types of UV Photoreceptor

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The Colourful World of the Mantis Shrimp the Colour-Vision System of These Crustaceans Includes Four Types of UV Photoreceptor brief communications The colourful world of the mantis shrimp The colour-vision system of these crustaceans includes four types of UV photoreceptor. umans cannot see ultraviolet light, Figure 1 R8 photoreceptors but many arthropods and vertebrates in the midband of the stom- Hcan because they have a single photo- atopod eye have multiple UV receptor with a peak sensitivity to light at sensitivities a, Stomatopod wavelengths of around 350 nanometres (ref. eye showing the clearly 1). Here we use electrophysiological meth- defined midband, rows 1 to ods to investigate the vision of the mantis 6 (dorsal to ventral)4,5. The shrimp, Neogonodactylus oerstedii. We find top four rows are concerned that this marine crustacean has at least four with colour information, and types of photoreceptor for ultraviolet light the remaining two are spe- that are located in cells of the eye known as cialized for polarization2,5. b, R8 cells. These photoreceptors are maxi- Diagram of the photorecep- mally sensitive to light of wavelengths 315, tors in the six midband rows 330, 340 and 380 nm. Together with previ- and the peripheral retinae. ous evidence2, this finding indicates that the R8 cells are coloured. Chro- remarkable colour-vision system in these matic channels from 400 to stomatopod crustaceans may be unique, as 700 nm are contained in a befits their habitat of kaleidoscopically population of cells called R1 colourful tropical coral reefs. to R7 (ref. 4). VH and DH are Many stomatopods inhabit the top few representatives of the dorsal metres of water, which are bathed in light of and ventral hemisphere ultraviolet-A wavelengths3. In this spectrally regions in the peripheral varied environment, they have evolved retina. c, Ultraviolet spectral extremely complex retinae within their sensitivities of R8 cells. Per, apposition compound eyes2,4–6. The top peripheral retina (DH or VH). four rows of the midband (Fig. 1a) contain eight spectral sensitivities from wavelengths periphery. Two of these sensitivities are rel- have not yet been characterized, as they are of 400 to 700 nm, each based on a different atively broad and two are very narrow, but hard to find or record from. visual pigment2. Oversampling within the they are all too narrow to be the result of The evenly spaced ultraviolet photo- spectrum is avoided by elegant filtering visual-pigment absorption alone7. Filtering receptors in the eye of N. oerstedii indicate mechanisms that narrow these sensitivities2,6. mechanisms like those in the rest of the eye that stomatopods have extended the high- The R8 cells of stomatopods, like the are almost certainly the reason for this spec- frequency sampling system of the range 400 cells R1 to R7 (see Fig. 1), have an extreme tral tuning2,6, with the filter being situated to 700 nm into the ultraviolet to form a sin- proliferation of spectral sensitivities. Three in the dioptric apparatus or within the gle colour-vision system that is sensitive of the four ultraviolet spectral sensitivities microvilli of the R8 photoreceptors8,9. Mid- from 300 to 700 nm. are found in the midband, and one is in the band row 2 or row 3 R8 spectral sensitivities The narrowed sensitivities of all four cells can be modelled using existing visual- pigment nomograms7 and a series of Row 4 - 315 peak (n=4) - 300 VP, Filter - 305 cutoff Periphery - 330 peak (n=9) - 328 VP, Filter - 305 cutoff corneal ultraviolet cut-off filters10 (Fig. 2). It 1.0 1.0 is not possible to generate the spectral sen- sitivities observed by differential filtering of 0.5 0.5 the same visual pigment. Therefore, in Sensitivity common with the longer-wavelength sensi- 0.0 0.0 tivities in the R1 to R7 portion of the eye, 300 350 400 450 300 350 400 450 ultraviolet spectral sensitivities of the R8 cells seem to be generated from a popula- Row 5&6 - 340 peak (n=5) - 320 VP, Filter - 335 cutoff Row 1 - 380 peak (n=7) - 370 VP, Shallow filter - 375nm cutoff tion of different visual pigments10. 1.0 1.0 For colour vision, narrow-band photo- receptors have several advantages over 0.5 0.5 broad-band systems, including fine colour discrimination11 and improved colour con- Sensitivity 11,12 0.0 0.0 stancy . The main drawback is a drastic 300 350 400 450 300 350 400 450 reduction in sensitivity6, but many stom- Wavelength (nm) Wavelength (nm) atopods are found in the brightly lit waters of coral reefs and are usually diurnally Figure 2 The multiple ultraviolet sensitivities are caused by several different rhodopsins that are heavily filtered. Electrophysiological spectral active, so highly sensitive vision is not sensitivities (orange) are shown with standard errors for number of cells measured (n). A modelled spectral sensitivity (thick black line) has been required7. fitted to these. Model components are possible visual-pigment absorbances calculated from ref. 7 (thin black lines) and putative filters that nar- Stomatopods use colour in communica- row the visual-pigment absorbance (green lines). Filter spectra are chosen from a series of known ultraviolet filters (J.M. and U. Siebeck, tion13 and possess colour vision14 but it has unpublished data) with 50% cut-off points in the range 300 to 400 nm. These intracellular recordings from stomatopod photoreceptors and remained unknown whether these extend our recordings from R1–7 cells in the range 400 to 700 nm (data not shown) broadly confirm previous microspectrophotometric results2,6. into the ultraviolet as they do in birds and NATURE | VOL 401 | 28 OCTOBER 1999 | www.nature.com © 1999 Macmillan Magazines Ltd 873 brief communications fish1, although many coloured areas used by exists in row 6 and that this is theoretically consecutive time points, despite culturing stomatopods in communication contain optimal for polarized-light vision16. up to 330 million cells5, and the virus could ultraviolet components14. Most of the colour As ultraviolet-blind humans, we have not be isolated from the lymph nodes of information from natural objects can be created a barrier in the spectrum at 400 nm. either patient5. After HAART was discontin- decoded by just four types of photo-receptor For the colour or polarization vision of ued, we were able to detect plasma viraemia in the 300–700 nm range12,15, so there must stomatopods, this barrier is meaningless. within three weeks in both patients. be other reasons for the bizarre retinal Justin Marshall*, Johannes Oberwinkler† We carried out quantitative co-culture design of stomatopods, which probably uses *VTHRC, University of Queensland, assays5,10 by using highly purified resting & 12 channels for colour. There are two possi- Brisbane 4071, Australia CD4 T cells at several time points. The & ble explanations that logically extend the †Department of Neurobiophysics, pool of resting CD4 T cells carrying repli- sensitivity range of 400 to 700 nm. University of Groningen, Nijenborgh 4, cation-competent HIV emerged shortly The first possibility is that stomatopod 9747 AG, Groningen, The Netherlands after plasma viraemia was detected (Fig. 1). eyes examine colour space from 300 to 700 1. Tovee, M. J. Trends Ecol. Evol. 10, 455–460 (1995). This pool of cells increased in size by 3.8 log nm in much the same way as the ear exam- 2. Cronin, T. W. & Marshall, N. J. Nature 339, 137–140 (1989). by week 4 and by 2.0 log by week 6 in ines auditory space. The multiple, narrow- 3. Smith, R. C. & Baker, K. S. Appl. Optics 20, 177–184 (1981). patients 1 and 13 (numbered according to band spectral sampling channels, from 300 4. Marshall, N. J. Nature 333, 557–560 (1988). ref. 5), respectively, following the discontin- 5. Marshall, N. J. et al. Phil. Trans. R. Soc. Lond. B 334, 33–56 (1991). to 700 nm, may be analogous to the different 6. Cronin, T. W. et al. Vision Res. 34, 2639–2656 (1994). uation of HAART. The integrated form of auditory frequencies to which a cochlea is 7. Hart, N. S., Partridge, J. C. & Cuthill, I. C. J. Exp. Biol. 201, HIV DNA, which was not detected by Alu- tuned along its length. This may be thought 1433–1446 (1998). LTR polymerase chain reaction (Table 1) in 8. Hardie, R. C. Trends Neurosci. 9, 419–423 (1986). 6 & of as a kind of ‘digital’ colour vision. 9. Arikawa, K. et al. Vision Res. 39, 1–8 (1999). 10 resting CD4 T cells from either patient Alternatively, stomatopods may divide 10.Cronin, T. W. & Marshall, N. J. J. Comp. Physiol. A 166, during HAART, was readily detectable dur- the spectral world from 300 to 700 nm into 261–275 (1989). ing the reappearance of the virus in both 11.Neumeyer, C. in Vision and Visual Dysfunction: Evolution of the six dichromatically examined windows Eye and Visual System Vol. 2 (eds Cronly-Dillon, J. R. & patients (142 copies per million cells for (two in the ultraviolet, mediated by row 1–4 Gregory, R. L.) 284–305 (Macmillan, London, 1991). patient 1 at week 6, and 420 copies for R8 cells), each of which is subject to very 12.Osorio, D., Marshall, N. J. & Cronin, T. W. Vision Res. 37, patient 13 at week 8). fine spectral discrimination14. 3299–3309 (1997). Our results demonstrate the speed with 13.Caldwell, R. L. & Dingle, H. Sci. Am. 234, 80–89 (1976). One of the ultraviolet sensitivities is in 14.Marshall, N. J., Jones, J. P. & Cronin, T. W. J. Comp. Physiol. A which the latent HIV reservoir in the resting & row 5 of the midband, a region of the eye 179, 473–481 (1996). CD4 T-cell compartment emerges during that is probably used in polarization vision4,5.
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