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ScienceDirect Colour vision in marine organisms Justin Marshall1, Karen L Carleton2 and Thomas Cronin3 Colour vision in the marine environment is on average simpler than in terrestrial environments with simple or no colour vision through monochromacy or dichromacy. Monochromacy is found in marine mammals and elasmobranchs, including whales and sharks, but not some rays. Conversely, there is also a greater diversity of colour vision in the ocean than on land, examples being the polyspectral stomatopods and the many colour vision solutions found among reef fish. Recent advances in sequencing reveal more opsin (visual pigment) types than functionally useful at any one time. This diversity arises through opsin duplication and conversion. Such mechanisms allow pick-and-mix adaptation that tunes colour vision on a variety of very short non-evolutionary timescales. At least some of the diversity in marine colour vision is best explained as unconventional colour vision or as neutral drift. Addresses 1 Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4070, Australia 2 Department of Biology, University of Maryland, College Park, MD 20742, USA 3 Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, MD 21250, USA Corresponding author: Marshall, Justin ([email protected])
Current Opinion in Neurobiology 2015, 34:86–94 This review comes from a themed issue on Molecular biology of sensation Edited by David Julius and John Carlson
http://dx.doi.org/10.1016/j.conb.2015.02.002 0959-4388/# 2015 Elsevier Ltd. All rights reserved.
Introduction Colour vision in the marine environment operates between two extremes. For some organisms, it is less developed, with animals able to survive as colour-blind monochromats or at most dichromats. A few possess three or four spectral channels, potentially but not always, allowing them to venture into trichromacy or tetrachromacy, depending on how information is combined subretinally. However, the ocean also boasts animals with complex colour vision such as the stomatopod crustaceans with up to twelve spectral channels. Several drivers contribute to this complexity including the light environment, phylogeny and behaviour relative to colour. Current Opinion in Neurobiology 2015, 34:86–94
In this brief review we examine some of the recent advances in our understanding of colour vision in the ocean across both invertebrates and vertebrates and place this in context of previous hypotheses. Because the ocean is hard to work within and because its contrasting niches may deliver highly speciose animal assemblages, there are still many knowledge gaps. Some of our discussion extends from what we know about colour vision systems in freshwater fish as few marine species are well described.
Spectral sensitivities and colour vision Nearly always, a sense of colour requires the comparison of excitations between photoreceptor cells with different spectral sensitivities. At its simplest two such cells, each containing visual pigments with peak sensitivity in different spectral regions, will detect the same colour signal differently, so relative excitation ratios can be compared to form a dichromatic colour-vision system. Visual pigments are constructed from an opsin protein with centrally bound chromophore, often 11-cis retinal [1]. Their peak sensitivity, or l-max, depends both on variability in specific opsin amino acids and on the particular chromophore used [2]. Because both visual pigment absorption spectra and object reflection spectra are broad, within the 300– 750 nm range of light over which visual pigments operate, three or four visual pigments are usually sufficient [3,4] (Figure 1). Marine animals generally have two visual pigments and so are dichromats for reasons examined in the next section. Some, such as the cephalopods, many crustaceans and other invertebrates, remain colour-blind monochromats [5,6]. Surface-dwelling fish are capable of trichromacy or even tetrachromatic colour vision, and stomatopod crustaceans have evolved twelve spectral sensitivities, apparently processing spectral information in a unique way. Like their terrestrial counterparts, nocturnal and crepuscular marine animals generally forgo colour vision altogether, evolving a single spectral sensitivity for optimal light absorption [2,7]. While some nocturnal animals possess colour vision on land, in the ocean it is more common for the opposite to be true. Many diurnal animals, including the cephalopods and many crustaceans, have elaborated polarisation vision more than colour. Their single spectral sensitivity peaks around 500 nm, an optimum for polarisation vision for several reasons outside the scope of this review [8,9]. In order to absorb as much light as possible, the matching of photoreceptor sensitivity to bioluminescent emissions www.sciencedirect.com
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Figure 1
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Comparative colour vision complexity. Black rectangles marks peak spectral sensitivities relative to the spectrum below (in nanometers (nm), UV 300–400 nm and human visible 400–700 nm). Stomatopods have 12 colour channels, humans three (trichromacy), some reef fish are also trichromats but sample shorter wavelengths than humans and are very variable (Figure 3), crustaceans such as some crabs shrimp or species are dichromats or, like the cephalopods are colour blind with a single spectral sensitivity around 500 nm.
[10] or residual daylight from the surface has driven many vertebrate and invertebrate marine species to focus sensitivity between 450 and 500 nm [4,7]. The early visual ecology literature developed the ‘sensitivity hypothesis’ to explain this adaptation [7,11]. The exact match depends on the local environment, as estuarine or marine water peak transmission varies from green to blue, and to an extent on diurnal activity periods. Therefore, species in either habitat will possess spectral sensitivities that generally sample within the envelope of available light provided by spatial and temporal variations [7,12].
Evaluating colour vision type and evolution
Why is dichromacy common in many marine animals?
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Based on our relatively scant knowledge of marine animal colour vision, dichromacy emerges as the oceanic favourite. This perhaps derives from what is thought to be the basal colour sense in all animals, an ultraviolet (UV) and a green (or a mid-wavelength) sensitivity, used to differentiate UV-rich sky or open space [4] from substrate, which reflects UV poorly. This solution is still found in several invertebrates [13] including many crustaceans [5]. It has also been postulated that two-channel colour vision evolved in the shallow Cambrian oceans in order to remove luminance flicker via the differential subtractive input that two spectral sensitivities allows [4,14]. Finally, since the available spectrum of light narrows with increasing depth or viewing distance, a pair of spectral channels may provide all the information needed (Figure 2). John Lythgoe and others developed the ‘offset hypothesis’, a slight variation on this, suggesting that two sensitivities are ideal under water. One is matched to the background, and one is offset to discriminate objects against that background [4,7]. The blue and green sensitivities of many oceanic predators (fish or marine mammals) support this hypothesis [15,16,17].
A good starting point for determining the performance and limits of colour vision is to measure spectral sensitivities. Such information can be determined by absorption microspectrophotometry (MSP) of dissociated photoreceptors (rods and cones in vertebrates, rhabdoms or rhabdomeres in invertebrates [17–19] or spectral absorption measurements from expressed visual pigments [20]. The sensitivities either method delivers should be viewed as a first estimate however. MSP, unless
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l-Max positions of cones and rods in 14 species of snapper (Lutjanus) species from green coastal through clearer blue outer ocean waters are compared. Rod sensitivities — vertical bars, single cones — filled circles, double cones — semicircles. Vertical lines plot the zones of greatest sensitivity for each water type for visual pigments within at least 90% of optimum. Note how double cones fall within this range.Adapted from [4,12]. Current Opinion in Neurobiology 2015, 34:86–94
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performed systematically, often misses photoreceptor classes, while opsin expression almost invariably overestimates what the animal actually uses for colour vision. In a systematic MSP examination of 39 species of Hawaiian reef fish, Losey and co-workers determined that dichromatic or trichromatic colour vision apparently dominate in this ecosystem [19]. Analyses of these results [21,22] used the considerable overlap of double and single cone sensitivities in some species (Figure 3) to suggest that, as in birds [7], double cones may function as a luminance channel and that only the single cones participate in colour vision (for definitions of cone types, see [23]). This hypothesis is supported by the fact that among several marine fish, double cone sensitivities match light availability in the varying habitats occupied [7,12,22]. More recent behavioural observations, however, demonstrate that in one species of triggerfish, Rhinecanthus aculeatus, double cone members are certainly used separately in the construction of a trichromatic colour sense with the other single cone present [24]. It seems likely, therefore, that double cone function is variable, possibly
including polarisation vision [8,25] but cross-species behavioural evidence is lacking. It is not always clear from a spectral sensitivity count alone, which receptor channels combine beneath the retina and coordinate colour-relevant behaviours. Electrophysiological recording from photoreceptors, interneurons, or brain areas associated with colour vision often detects opponent processing [26]. Barry and Hawryshyn recorded extracellularly from retinal ganglion cells and optic tectum in the Hawaiian wrasse, Thalassoma duperrey, and found at least two cone mechanisms that appear well suited to their colour tasks [27]. Gruber and colleagues (1975) [28] and Bedore et al. [29] used electroretinogram (ERG) recordings to demonstrate multiple spectral sensitivity classes in rays. Recordings in invertebrates are mostly limited to early work, confirming mono or dichromacy in crabs and other crustaceans (for review [5]). More recently they have been used to determine the sensitivities of stomatopod photoreceptors [30,31,32], confirming the general pattern of results from MSP [18,31] but also identifying an extensive population of
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The spectral sensitivities of four species of reef fish from the same photic microhabitat. Normalized sensitivities include filtering by ocular media, in non-UV sensitive species often close to 400 nm. Note the diversity of peak positions, spectral sensitivity number and mix of single and double cones. Rods, black, single cones, red and double cones, blue curves.Adapted from [4,22]. Current Opinion in Neurobiology 2015, 34:86–94
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UV-sensitive photoreceptors (Figure 1 [30]). An interesting recent study of the ocular media filtering mechanisms stomatopods use to construct their UV sensitivities revealed a rare instance of an animal multiplying spectral channels using variable cut-off filtering and a single visual pigment [33]. Ultimately it is the behaviour of the animal relative to colour that allows us to state what type of colour vision it has. Reaction to colour varies from simple phototaxis, moving to or away from coloured areas as shown in beach amphipods [34], through wavelength-specific behaviours, to complex colour association and categorisation tasks (see [35,36] for useful summaries). Behavioural evidence in elasmobranch rays is consistent with the earlier electrophysiology [28,29], identifying likely trichromacy in the giant shovel-nosed ray Glaucostegus typus [37]. Aside from the triggerfish studies already mentioned [24], the reef damselfish, Pomacentrus ambionensis, is known to use colour choice in operant conditioning and may extend this to more complex tasks in the UV including individual facial recognition [38,39]. As indicated both by opsin types [40] and ocular media transmission [41], damselfish and other small fish on the reef [42] could use UV as a private short-distance communication channel, as larger predatory fish lack UV sensitivity [41]. Colour-vision models and field observation reveal that ‘cleaner blue’ is used as a colour code by several cleaner fish and crustaceans [43]. In addition, such modelling shows that fish with UV sensitivity are at a great advantage, not just with UV spectra or UV silhouetted prey becoming more visible [39,41] but due to boosted colour discrimination across colour space [16]. Marine invertebrates with behavioural evidence for colour vision include the fiddler crabs [44] and blue crab [45]. Crab colour sense is most likely based both on twochannel UV/violet — green retinal sensitivities and on achromatic cues [46]. Molecular evidence for more than two spectral sensitivities does exist in fiddler crabs [47]; however, it is not clear to what extent this reflects seasonal or other environmental tuning as opposed to an extension of dichromacy. Stomatopods have been known for some time to possess true colour vision in colour versus grey-card tests [48], hardly a surprise given their diverse spectral sensitivities and colourful lifestyle [49]. Early speculation pointed towards a series of dichromatic mechanisms, based on anatomy and subretinal neural connections. However more recent results indicate a far more interesting system of processing. Thoen et al. [32] demonstrate that stomatopods discriminate wavelengths up to ten times less well than other animals, such as humans, honey bees and goldfish. Theoretically, if their colour sense were based on photoreceptor comparisons, mantis shrimp hue discrimination should be extremely fine, so these results www.sciencedirect.com
indicate a different approach to processing of their twelve channel input. Our current hypothesis is that the relative spectral excitations of these twelve bins are read off as a serial linear excitation pattern. Such an unconventional way to conduct colour vision requires specific subretinal wiring, currently under investigation. Comfortingly it does explain away the worry of dodecachromatic colour vision [50].
Too many opsins? It is increasingly common to estimate spectral sensitivities through examining opsin expression. Many insects are molecularly trichromatic, with a UV, blue and green (or LWS for Long Wave Sensitive) classes of opsins. Of marine invertebrates, so far only stomatopods and possibly fiddler crabs reveal more than two spectral classes [13,47,51]. Early in vertebrate evolution, at least as early as lampreys, five classes of opsin arose [20,52]. These are the RH1 class found in rods and four cone opsin classes: SWS1 — very short (often UV) sensitive, SWS2 — short wavelength (often blue) sensitive, RH2 — a medium wavelength, green-sensitive rod-like opsin, and LWS — long wavelength (up to red) sensitive class [2]. It is surprising how often gene duplications, deletions and substitutions multiply and change opsins. For example, among the visually unexciting ostracods, Oakley and colleagues identify eight opsin types [53] while in stomatopods, Porter and colleagues find over thirty opsins in some species [51]. In fish, it is not uncommon to find seven to ten or more opsins expressed at a functional level [2,54]. Serial duplications, deletions, gene conversions and other transformations allow great plasticity, especially when coupled to subsequent differential gene expression and modification [55,56]. For example, in a recent survey of percomorph fish species, a new class of SWS2 gene was described [57]. Other recent studies find RH2 gene loss in pufferfish [58] and loss of SWS1 and LWS in marine mammals [15]. Having this variation available may contribute to rapid speciation in fish [2]. Hofmann et al. showed that in damselfish, varying light environment has shaped opsin diversity, particularly in the SWS and LWS classes [40]. Important to note is that not all opsins are necessarily functional at any one time, and how and when each subclass is used throughout life is poorly understood. A number of factors including the following require careful consideration. (a) Co-expression of different visual pigments in the same photoreceptor is now recognised in both invertebrates [51] and vertebrates [59]. In some examples this widens the overall spectral response of the cell; however, it may sometimes reflect a photoreceptor transitory phase. Current Opinion in Neurobiology 2015, 34:86–94
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(b) Spectral sensitivities may change during the life of an animal on a developmental, seasonal, sexual, or other basis (see e below). This may be achieved through opsin expression differences and/or a change in chromophore from A1 to A2, a transformation that extends sensitivities to longer wavelengths [7]. Almost all marine fish, including tuna [56] or bream [60] go through a larval stage, and where examined these often have a different opsin quota to the adult. Functionally this may reflect a change in foraging mode and/or light environment. (c) Retinal functional subdivision is common in invertebrates with compound eyes but is also found in fish, with different areas expressing different opsins [59,61]. Although examples of this are currently limited to freshwater, it is also likely in marine
species as their retinas often mirror the vertical change in photic environment underwater. Higher sensitivity double cones are dense in the dorsal retina, which looks into dim deeper water, while more single cones for colour specific tasks are present in the ventral and medial retina [62]. In this way, retinal sensitivities vary across the retina to match the spatially varying light environment. This above any other reason may explain the supernumerary spectral sensitivity diversity seen in fish. (d) Short-term spectral sensitivity plasticity is known in both fish and invertebrates, a surprise given our assumption that an animal’s colour sense was fixed for life or at least long-term life periods. Diurnal opsin expression changes have been recorded in freshwater cichlids and killifish [63,64]. Sensitivities also change
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Fine colour pattern combinations through resolution breakdown in Thalassoma lunare (moon wrasse, a, c, e) and Pygoplites diacanthus (angelfish, b, d, f). Fish colours (a,b) measured using reflectance spectrophotometry (c,d) where curves are colour-coded to fish colours in a and b, combine over a few metres underwater, especially to the relatively poor-resolution eyes of fish. Combined curves plotted in red in e and f. The complex colours of wrasse and parrotfish, combine to give a good match to background blue spacelight, at least for the spectrum up to 600 nm, which encompasses most of the blue-shifted sensitivities known in reef fish. Yellow and blue, frequent in reef fish colouration for a variety of reasons combine to a uniform grey spectral reflection, good camouflage in several contexts and in marked contrast to the highly conspicuous colour combination close up.Adapted from [67]. Current Opinion in Neurobiology 2015, 34:86–94
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with the spectral content of light available, correlating to different settlement depths as larvae take up their adult habitat [65]. (e) Unconventional colour vision, such as that seen in stomatopods (or on land in butterflies [50]) may result in a large number of opsin types, aimed not at allowing finer colour chromatic evaluation, but either to deliver to stomatopods the required spectral coverage that their spectral-pattern recognition system requires or to add sensitivities for specific colour tasks. This latter wavelengthspecific colour vision, with or without accompanying retinal subdivision, is worth more attention in the ocean.
Colours, colour vision and spectral sensitivity spacing The colours and colour vision systems around coral reefs have received recent attention [16,21,22,43,66,67]. These studies re-confirm many of the original visual ecological observations of Lythgoe and colleagues, such as the use of yellow and blue in marine waters for efficient signal transmission [7]. The relatively poor spatial acuity of fish vision is also important in colour communication, as many of the fine colour patterns of reef fish, for example, while conspicuous close up, add together through resolution breakdown to give grey or match to blue background space-light at a distance [67] (Figure 4). The blue-shifted spectral sensitivities of reef fish also deliver another camouflage surprise, as yellow (a common colour on the reef) is in fact well matched to an average coral colour up to around 600 nm [67]. Yellow fish seem conspicuous to us, as our primate colour vision is particularly concerned with ripening fruit and leaves in this spectral region. As with colour mixing, yellow may be both conspicuous and camouflaged as required on the reef, as it contrasts well to a blue water background but matches the yellow/green corals [16,67]. Characterisation of reef fish colour vision has revealed a greater diversity than might be expected (Figure 3) [4,19,22]. Fish from very similar light micro-habitats possess widely differing spectral sensitivity placement, and while it is easy to state that this must somehow be related to their species-specific colour task needs, these are not obvious. Modelling of a number of colour tasks with different spectral sensitivity combinations suggests that the exact placement of the colour channels may vary without greatly affecting performance [4,16]. This is also seen in the variability of spectral sensitivities in 40 species of flower-visiting hymenopterans [4]. The idea of neutral drift in the evolution of spectral sensitivity tuning may be uncomfortable but is worth considering until well defined behaviour to colour task connections are found. www.sciencedirect.com
Fluorescence of stomatopods and fish (among other animals including jumping spiders and birds) has been implicated as a means of boosting colour communication [68,69]. The fluorescent emission of stomatopods increases the underlying colour signal by 15%, enough to be seen; however, behavioural evidence of the significance of the fluorescent component is lacking. Triplefins, wrasse, and now more than 180 other species of marine fish [70] are known to fluoresce and may do so at specific depths where the longer wavelengths (yellowred) of these blue-water-excited emissions are prominent. Despite several attempts [71], behavioural evidence for fluorescent function in fish remains unconvincing, as it fails to differentiate other colour pattern elements. Many pigments in nature fluoresce, and it remains possible that fluorescence in fish serves no visual function.
Conclusions and future perspectives There is great diversity in opsin complements amongst marine animals suggesting excellent colour vision capabilities. However, before assuming animals with multiple opsins are attempting higher levels of spectral discrimination, two other explanations must be considered. Firstly, large opsin numbers are clearly a dynamic way to tune colour vision to the needs of animal on a variety of evolutionary or within-lifetime timescales [57]. Additionally, multiple spectral sensitivities may also reflect unconventional processing and/or a colour sense that is functionally subdivided across the retina. At present, there is a great need for behavioural observation to back up hypotheses and ideas gleaned from more immediate methods, and this necessarily includes in situ observation of how colour is used. The ocean is not an easy place to work, but there is clearly a great diversity of colour vision systems within it that make it worth the effort, and our greater knowledge of freshwater systems provides tantalising glimpses of discoveries-in-waiting. We also suggest that the top-down approach of phylogeny, evolution and molecular genetics needs a more effective dialogue with the functional, anatomical or neurobiological side of colour vision as identified in the recent review of Kemp et al. [72].
Conflicts of interest Nothing declared.
Acknowledgements The opinion expressed here are very clearly a distillation of many years work, not just from ourselves, but from many exceptional and enlightened colleagues. These include John Lythgoe, Horace Barlow, Bill McFarland, Ellis Loew, Craig Hawryshyn, Tom Kocher, Roy Caldwell, George Losey, Misha Vorobyev and Daniel Osorio. We apologise for necessarily citing secondary references that also summarise their seminal work.
JM is supported by funding from the Australian Research Council, the Asian Office of Aerospace Research and Development and the Airforce Office of Current Opinion in Neurobiology 2015, 34:86–94
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Scientific Research (AFOSR). TC through the National Science Foundation (NSF) and AFOSR. KC through NSF.
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1.
Wald G: The molecular basis of visual excitation. Nature 1968, 219:800-807.
2.
Hunt DM, Hankins MW, Collin SP, Marshall NJ (Eds): Evolution of Visual and Non-visual Pigments. Springer; 2014.
This recent review captures the latest research on visual pigments, within photoreceptors and elsewhere, across both invertebrates and vertebrates. Data from several streams including electrophysiological, behavioural and molecular biology are included with highlights being the recent advances in opsin expression and visual pigment function. 3.
Barlow HB: What causes trichromacy? A theoretical analysis using comb-filtered spectra. Vis Res 1982, 22:635-643.
4. Cronin TW, Johnsen S, Marshall NT, Warrant EJ: Visual Ecology. Princeton University Press; 2014. This is a much needed update of the 1979 volume, The Ecology of Vision, by John Lythgoe, and reviews and expands this area of visual neuroscience. The subdiscipline of visual ecology recognises the link between the design of visual systems and the environment, as well as examining behavioural and evolutionary aspects. Visual Ecology contains many chapters relevant to marine colour vision, including examinations of photic habitat and colour vision. 5.
Marshall NJ, Kent J, Cronin TW: Visual adaptations in crustaceans: spectral sensitivity in diverse habitats. In Adaptive Mechanisms in the Ecology of Vision. Edited by Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S. Springer; 1999:285-327.
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Marshall NJ, Messenger JB: Colour-blind camouflage. Nature 1996, 382:408-409.
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Lythgoe J: The Ecology of Vision. Clarendon Press; 1979.
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Horva´th G (Ed): Polarized Light and Polarization Vision in Animal Sciences. Springer; 2014.
A twenty five chapter book that comprehensively examines recent advances in polarization vision. This includes the recent notion, advanced by authors of this article, that the information content in polarisation signals from animals makes this modality equivalent to colour vision. To some extent, this explains why many marine animals, notably the invertebrates, seem to have adopted polarization over colour in the marine environment. 9.
Marshall NJ, Cronin TW: Polarisation vision. Curr Biol 2011, 21:R101-R105.
10. Widder EA: Bioluminescence in the Ocean: origins of biological, chemical, and ecological diversity. Science 2010, 328:704-708. 11. Munz FW, McFarland WN: The significance of spectral position in the rhodopsins of tropical marine fishes. Vis Res 1973, 13:1829-1874. 12. Lythgoe J, Muntz W, Partridge JC, Shand J, Williams DM: The ecology of the visual pigments of snappers (Lutjanidae) on the Great Barrier Reef. J Comp Physiol A 1994, 174:461-467. 13. Briscoe AD, Chittka L: The evolution of colour vision in insects. Annu Rev Entomol 2001, 46:471-510. 14. Maximov V: Environmental factors which may have led to the appearance of colour vision. Philos Trans R Soc Lond B 2000, 355:1239-1242. 15. Meredith RW, Gatesy J, Emerling CA, York VM, Springer MS: Rod monochromacy and the coevolution of cetacean retinal opsins. PLoS Genet 2013, 9:e1003432. Shows that cetaceans have dispensed with all cone pigments and thus maintain all-rod retinas, other marine mammals express green opsins but no cetacean is known to express a blue-sensitive cone pigment. The narrow spectral deep-water foraging habitats of many marine mammals and lack of colour in mate choice may have driven this reduction. Current Opinion in Neurobiology 2015, 34:86–94
Pinnipeds also are thought to have lost blue cones. Colour vision therefore seems unlikely or at least rudimentary in marine mammals, although there remains behavioural evidence suggesting that some dolphins and some pinnipeds do make colour choices. This may be the result of rodcone dichromatic-like subretinal processes. 16. Marshall NJ, Vorobyev M: The design of color signals and color vision in fishes. In Sensory Processing in Aquatic Environments. Edited by Collin SP, Marshall NJ. Springer; 2003:194-222. 17. Hart NS, Lisney TJ, Marshall NJ, Collin SP: Multiple cone visual pigments and the potential for trichromatic colour vision in two species of elasmobranch. J Exp Biol 2004, 207:4587-4594. 18. Cronin TW, Marshall NJ: A retina with at least ten spectral types of photoreceptors in a mantis shrimp. Nature 1989, 339:137-140. 19. Losey GS, McFarland WN, Loew ER, Zamzow JP, Nelson PA, Marshall NJ: Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments. Copeia 2003, 3:433-454. 20. Yokoyama S: Evolution of dim-light and color vision pigments. Annu Rev Genomics Hum Genet 2008, 9:259-282. 21. Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS: Visual biology of Hawaiian coral reef fishes. II. Colors of Hawaiian coral reef fish. Copeia 2003, 3:455-466. 22. Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS: Visual biology of Hawaiian coral reef fishes. III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 2003, 3:467-480. 23. Walls GL: The Vertebrate Eye and its Adaptive Radiation. The Cranbrook Press; 1942. 24. Pignatelli V, Champ C, Marshall J, Vorobyev M: Double cones are used for colour discrimination in the reef fish, Rhinecanthus aculeatus. Biol Lett 2010, 6:537-539. 25. Kelber A, Roth LSV: Nocturnal colour vision — not as rare as we might think. J Exp Biol 2006, 209:781-788. 26. Kamermans M, Kraaij DA, Spekreijse H: The cone/horizontal cell network: a possible site for color constancy. Vis Neurosci 1998, 15:787-797. 27. Barry KL, Hawryshyn CW: Spectral sensitivity of the Hawaiian saddle wrasse, Thalassoma duperrey, and implications for visually mediated behaviour on coral reefs. Environ Biol Fishes 1999, 56:429-442. 28. Gruber SH: Duplex vision in the elasmobranchs; histological, electrophysiological and psychophysical evidence. In Vision in Fishes: New Approaches in Research. Edited by Ali MA. Plenum Press; 1975:525-540. 29. Bedore C, Loew E, Frank T, Hueter R, McComb DM, Kajiura S: A physiological analysis of color vision in batoid elasmobranchs. J Comp Physiol A 2013, 199:1129-1141. Physiological approaches were used to examine colour and specifically UV vision in two species of sting ray. ERG revealed multiple sensitivity peaks, including in the UV although no UV cones were identified. MSP showed two or three cone visual types, consolidating the previous work of Hart and colleagues [17] and the behavioural evidence of Van-Eyk et al. [37] showing likely trichromatic colour vision in shovel nosed rays. 30. Marshall NJ, Oberwinkler J: The colourful world of the mantis shrimp. Nature 1999, 401:873-874. 31. Marshall J, Cronin TW, Kleinlogel S: Stomatopod eye structure and function: a review. Arthropod Struct Dev 2007, 36:420-448. 32. Thoen HH, How MJ, Chiou T-H, Marshall NJ: A different form of color vision in mantis shrimp. Science 2014, 343:411-413. Using both intracellular electrophysiology and behaviour, the colour vision system of the stomatopod Haptosquilla trispinosa is described. Wavelength discrimination experiments are used to show that, in some ways unexpectedly, stomatopods possess discrimination levels around ten times worse than those of other animals similarly tested, including humans, butterflies, bees and goldfish. The hypothesis suggested to explain this relies on a completely new form of colour coding in which the spectrum is coded as a serially related colour pattern, rather than colours being judged from analogue comparison of two (or more) receptor output. www.sciencedirect.com
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The need to cover the spectrum with this new system therefore explains the need for full spectral coverage and twelve spectral sensitivities. The neural connection requirements underlying this are currently under investigation. 33. Bok MJ, Porter ML, Place AR, Cronin TW: Biological sunscreens tune polychromatic ultraviolet vision in mantis shrimp. Curr Biol 2014, 24:1636-1642. This examination of the UV sensitivities in stomatopods revealed several new features to this unusual visual system. They include: the use of mycosporine amino acids (MAAs) within the optical elements of the eye (crystalline cones) as variable UV filters to tune spectral sensitivity; selective filtering of visual pigment using short-pass filtering (long-pass is more common); multiplication of UV sensitivities using two visual pigments and several differential UV filters. This is unusual in the animal kingdom with animals generally providing a new visual pigment for every new added spectral sensitivity. 34. Ugolini A, Vignali B, Castellini C, Lindstrom M: Zonal orientation and spectral filtering in Talitrus saltator (Amphipoda, Talitridae). J Mar Biol Assoc UK 1996, 76:377-389. 35. Kelber A, Vorobyev M, Osorio D: Animal colour vision — behavioural tests and physiological concepts. Biol Rev 2003, 78:81-118. 36. Kelber A, Osorio D: From spectral information to animal colour vision: experiments and concepts. Proc Biol Sci 2010, 277:1617-1625. 37. Van-Eyk SM, Siebeck UE, Champ CM, Marshall NJ, Hart NS: Behavioural evidence for colour vision in an elasmobranch. J Exp Biol 2011, 214:4186-4192. 38. Siebeck UE, Wallis GM, Litherland L: Colour vision in coral reef fish. J Exp Biol 2008, 211:354-360. 39. Siebeck UE, Losey GS, Marshall NJ: UV communication in Fish. In Communication in Fishes, Vol 2. Edited by Laddich F, Collin SP, Moller P, Kapoor BG. Science Publications Inc.; 2006:423-455. 40. Hofmann CM, Marshall NJ, Abdilleh K, Patel Z, Siebeck UE, Carleton KL: Opsin evolution in Damselfish: convergence, reversal, and parallel evolution across tuning sites. J Mol Evol 2012, 75:79-91. 41. Siebeck UE, Marshall NJ: Ocular media transmission of coral reef fish — can coral reef fish see ultraviolet light? Vis Res 2001, 41:133-149. 42. Losey GS, Cronin TW, Goldsmith T, Hyde D, Marshall NJ, McFarland WN: The UV visual world of fishes: a review. J Fish Biol 1999, 54:921-943. 43. Cheney KL, Grutter AS, Blomberg SP, Marshall NJ: Blue and yellow signal cleaning behavior in coral reef fishes. Curr Biol 2009, 19:1283-1287. 44. Detto T: The fiddler crab Uca mjoebergi uses colour vision in mate choice. Proc Biol Sci 2007, 274:2785-2790. 45. Baldwin J, Johnsen S: The importance of color in mate choice of the blue crab Callinectes sapidus. J Exp Biol 2009, 212:3762-3768. 46. Baldwin J, Johnsen S: The male blue crab, Callinectes sapidus, uses both chromatic and achromatic cues during mate choice. J Exp Biol 2012, 215:1184-1191. 47. Rajkumar P, Rollmann SM, Cook TA, Layne JE: Molecular evidence for color discrimination in the Atlantic sand fiddler crab, Uca pugilator. J Exp Biol 2010, 213:4240-4248. 48. Marshall NJ, Jones J, Cronin TW: Behavioural evidence for colour vision in stomatopod crustaceans. J Comp Physiol A 1996, 179:473-481.
increasingly being recognised in vertebrates also, including fish [59,61]. Stomatopod colour vision is defined as particularly unconventional with colour coding via spectral pattern recognition over the entire spectrum rather than spectral channel comparisons as found in all other colour vision types [32]. 51. Porter ML, Speiser DI, Zaharoff AK, Caldwell RL, Cronin TW, Oakley TH: The evolution of complexity in the visual systems of stomatopods: insights from transcriptomics. Integr Comp Biol 2013, 53:39-49. The research described here uses transcriptomics to examine the diversity of opsins in stomatopod crustaceans and attempts to place this in an evolutionary context. Some species express up to 33 opsins while the retina has a maximum of 16 photoreceptor types at the functional level. 52. Collin SC, Davies W, Hart NS, Hunt D: The evolution of early vertebrate photoreceptors. Philos Trans R Soc Lond B 2009, 364:2925-2940. 53. Oakley TH, Huber D: Differential expression of duplicated opsin genes in two eyetypes of ostracod crustaceans. J Mol Evol 2004, 59:239-249. 54. Carleton KL, Spady T, Streelman JT, Kidd M, McFarland W, Loew E: Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biol 2008, 6:22. 55. Hofmann C, Carleton KL: Gene duplication and differential gene expression play an important role in the diversification of visual pigments in fish. Integr Comp Biol 2009, 49:630-643. 56. Nakamura Y, Mori K, Saitoh K, Oshima K, Mekuchi M, Sugaya T, Shigenobu Y, Ojima N, Muta S, Fujiwara A et al.: Evolutionary changes of multiple visual pigment genes in the complete genome of Pacific bluefin tuna. Proc Nat Acad Sci USA 2013, 110:11061-11066. Here the tuna genome has been sequenced to show that opsin genes duplicate in tandem and also undergo gene conversion. 57. Cortesi F, Musilova´ Z, Stieb S, Hart NS, Siebeck UE, Malmstrøm M, Tørresen OK, Jentoft S, Cheney KL, Marshall NJ, Carleton KL, Salzburger W: Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes. PNAS 2015, 112:1493-1498. A comprehensive survey of 100 fish species that documents the evolutionary history of the SWS2 gene. A new gene duplication is identified along with, in some groups, losses and conversions in this violet/blue sensitive opsin class, coinciding with radiation of the highly diverse percomorphs. One species, Pseudochromis fuscus, is used to exemplify how gene differences occur within one species ontogenetically. 58. Neafsey DE, Hartl DL: Convergent loss of an anciently duplicated, functionally divergent RH2 opsin gene in the fugu and Tetraodon pufferfish lineages. Gene 2005, 350:161-171. 59. Dalton BE, Loew ER, Cronin TW, Carleton KL: Spectral tuning by opsin coexpression in retinal regions that view different parts of the visual field. Proc Biol Soc 2014, 281:1797. 60. Shand J, Davies W, Thomas N, Balmer L, Cowing J, Pointer M: The influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream Acanthopagrus butcheri. J Exp Biol 2008, 211:1495-1503. 61. Temple SE: Why different regions of the retina have different spectral sensitivities: a review of mechanisms and functional significance of intraretinal variability in spectral sensitivity in vertebrates. Vis Neurosci 2011, 28:281-293. 62. Fritsches KA, Marshall NJ, Warrant EJ: Retinal specializations in the blue marlin: eyes designed for sensitivity to low light levels. Mar Freshwater Res 2003, 54:333-341.
49. Caldwell RL, Dingle H: Stomatopods. Sci Am 1976, 234:80-89.
63. Halstenberg S, Lindgren K, Samagh S, Nadal-Vicens M, Balt S, Fernald R: Diurnal rhythm of cone opsin expression in the teleost fish Haplochromis burtoni. Vis Neurosci 2005, 22:135-141.
50. Marshall NJ, Arikawa K: Unconventional colour vision. Curr Biol 2014, 24:R1150. Unconventional colour vision is explored and defined. It is suggested that multiple colour channels, including up to nine in butterflies and 12 in stomatopods are not attempts at increasing colour space dimensionality. In the butterflies, spectral channels are added to conduct specific colour tasks or wavelength specific behaviours. Segregation of the retina also contributes to spectral sensitivity multiplication, with different photoreceptor combinations examining different regions of visual space. This is
64. Johnson AM, Stanis S, Fuller RC: Diurnal lighting patterns and habitat alter opsin expression and colour preferences in a killifish. Proc R Soc Lond B 2013:280. This paper shows opsin expression varying on a diurnal basis, following to some extent lighting levels. While this example is in freshwater fish, this is likely to occur in the marine environment also, reflecting changes in light over the 24 h period. Such changes as with [63] are quantitative amplification of expression within one opsin type rather appearance or disappearance of different types.
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65. Cronin TW, Caldwell RL, Marshall NJ: Sensory adaptation — tunable colour vision in a mantis shrimp. Nature 2001, 411:547-548.
the potentially new fluorescing compounds that it identifies. It does point out in passing that the yellow filters found in the ocular media of several fish, including many wrasse, may help enhance the fluorescent signal.
66. Marshall NJ: The visual ecology of reef fish colours. In Animal Signals: Signalling and Signal Design in Animal Communication. Edited by Espmark Y, Amundsen T, Rosenqvist G. Tapir Press; 2000:83-120.
71. Gerlach T, Sprenge D, Michiels NK: Fairy wrasses perceive and respond to their deep red fluorescent coloration. Proc R Soc Lond B 2014, 281:20140787. Part of an extended effort by Michiels and colleagues to show that fluorescence is used in visual behaviour in fish. Mate choice tests demonstrate that fish including the fluorescent component of their colours are favoured over those that have it removed by selective lighting. However behavioural arena lighting conditions are not natural and fail to differentiate the added component of the fluorescence that forms part of an underlying and otherwise obvious colour pattern.
67. Marshall NJ: Conspicuousness and camouflage with the same ‘bright’ colours. Colours for concealment and camouflage in reef fish. Philos Trans R Soc Lond B 2000, 355:1243-1248. 68. Mazel C, Cronin TW, Caldwell RL, Marshall NJ: Fluorescent enhancement of signaling in a mantis shrimp. Science 2004, 303:51. 69. Michiels N, Anthes N, Hart NS, Herler J, Meixner A, Schleifenbaum F, Schulte G, Siebeck UE, Sprenger D, Wucherer M: Red fluorescence in reef fish: a novel signalling mechanism? BMC Ecol 2008, 8:16. 70. Sparks JS, Schelly RC, Smith WL, Davis MP, Tchernov D: The covert world of fish biofluorescence: a phylogenetically widespread and phenotypically variable phenomenon. PLoS ONE 2014, 9:e83259. This extensive survey of fish fluorescence using high-intensity excitation sources notes over 180 species of fish that fluoresce. Whether this fluorescence is also visually relevant to the fish themselves under ambient illumination is not demonstrated and this work may be more interesting for
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72. Kemp DJ, Herberstein ME, Fleishman LJ, Endler JA, Bennett ATD, Dyer AG, Hart NS, Marshall NJ, Whiting MJ: An integrative framework for the appraisal of coloration in nature. Am Nat 2015. (in press). This review or synopsis examines current methods and approaches in colour communication and colour vision in animals. It provides guidance in methods without being prescriptive and identifies two different views; first is the ‘top-down’ evolutionary/behavioural ecology school and second the more mechanistic ‘bottom-up’ neurophysiological/colour quantification school. Between these sit colour vision models which, as the article explains, are being misused due to a lack of communication between the two schools. Ways to remedy this and form a more unified, and to some extent standardised, approach to understanding aspects of colour vision are suggested.
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ScienceDirect Colour vision in marine organisms Justin Marshall1, Karen L Carleton2 and Thomas Cronin3 Colour vision in the marine environment is on average simpler than in terrestrial environments with simple or no colour vision through monochromacy or dichromacy. Monochromacy is found in marine mammals and elasmobranchs, including whales and sharks, but not some rays. Conversely, there is also a greater diversity of colour vision in the ocean than on land, examples being the polyspectral stomatopods and the many colour vision solutions found among reef fish. Recent advances in sequencing reveal more opsin (visual pigment) types than functionally useful at any one time. This diversity arises through opsin duplication and conversion. Such mechanisms allow pick-and-mix adaptation that tunes colour vision on a variety of very short non-evolutionary timescales. At least some of the diversity in marine colour vision is best explained as unconventional colour vision or as neutral drift. Addresses 1 Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4070, Australia 2 Department of Biology, University of Maryland, College Park, MD 20742, USA 3 Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, MD 21250, USA Corresponding author: Marshall, Justin ([email protected])
Current Opinion in Neurobiology 2015, 34:86–94 This review comes from a themed issue on Molecular biology of sensation Edited by David Julius and John Carlson
http://dx.doi.org/10.1016/j.conb.2015.02.002 0959-4388/# 2015 Elsevier Ltd. All rights reserved.
Introduction Colour vision in the marine environment operates between two extremes. For some organisms, it is less developed, with animals able to survive as colour-blind monochromats or at most dichromats. A few possess three or four spectral channels, potentially but not always, allowing them to venture into trichromacy or tetrachromacy, depending on how information is combined subretinally. However, the ocean also boasts animals with complex colour vision such as the stomatopod crustaceans with up to twelve spectral channels. Several drivers contribute to this complexity including the light environment, phylogeny and behaviour relative to colour. Current Opinion in Neurobiology 2015, 34:86–94
In this brief review we examine some of the recent advances in our understanding of colour vision in the ocean across both invertebrates and vertebrates and place this in context of previous hypotheses. Because the ocean is hard to work within and because its contrasting niches may deliver highly speciose animal assemblages, there are still many knowledge gaps. Some of our discussion extends from what we know about colour vision systems in freshwater fish as few marine species are well described.
Spectral sensitivities and colour vision Nearly always, a sense of colour requires the comparison of excitations between photoreceptor cells with different spectral sensitivities. At its simplest two such cells, each containing visual pigments with peak sensitivity in different spectral regions, will detect the same colour signal differently, so relative excitation ratios can be compared to form a dichromatic colour-vision system. Visual pigments are constructed from an opsin protein with centrally bound chromophore, often 11-cis retinal [1]. Their peak sensitivity, or l-max, depends both on variability in specific opsin amino acids and on the particular chromophore used [2]. Because both visual pigment absorption spectra and object reflection spectra are broad, within the 300– 750 nm range of light over which visual pigments operate, three or four visual pigments are usually sufficient [3,4] (Figure 1). Marine animals generally have two visual pigments and so are dichromats for reasons examined in the next section. Some, such as the cephalopods, many crustaceans and other invertebrates, remain colour-blind monochromats [5,6]. Surface-dwelling fish are capable of trichromacy or even tetrachromatic colour vision, and stomatopod crustaceans have evolved twelve spectral sensitivities, apparently processing spectral information in a unique way. Like their terrestrial counterparts, nocturnal and crepuscular marine animals generally forgo colour vision altogether, evolving a single spectral sensitivity for optimal light absorption [2,7]. While some nocturnal animals possess colour vision on land, in the ocean it is more common for the opposite to be true. Many diurnal animals, including the cephalopods and many crustaceans, have elaborated polarisation vision more than colour. Their single spectral sensitivity peaks around 500 nm, an optimum for polarisation vision for several reasons outside the scope of this review [8,9]. In order to absorb as much light as possible, the matching of photoreceptor sensitivity to bioluminescent emissions www.sciencedirect.com
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Comparative colour vision complexity. Black rectangles marks peak spectral sensitivities relative to the spectrum below (in nanometers (nm), UV 300–400 nm and human visible 400–700 nm). Stomatopods have 12 colour channels, humans three (trichromacy), some reef fish are also trichromats but sample shorter wavelengths than humans and are very variable (Figure 3), crustaceans such as some crabs shrimp or species are dichromats or, like the cephalopods are colour blind with a single spectral sensitivity around 500 nm.
[10] or residual daylight from the surface has driven many vertebrate and invertebrate marine species to focus sensitivity between 450 and 500 nm [4,7]. The early visual ecology literature developed the ‘sensitivity hypothesis’ to explain this adaptation [7,11]. The exact match depends on the local environment, as estuarine or marine water peak transmission varies from green to blue, and to an extent on diurnal activity periods. Therefore, species in either habitat will possess spectral sensitivities that generally sample within the envelope of available light provided by spatial and temporal variations [7,12].
Evaluating colour vision type and evolution
Why is dichromacy common in many marine animals?
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Based on our relatively scant knowledge of marine animal colour vision, dichromacy emerges as the oceanic favourite. This perhaps derives from what is thought to be the basal colour sense in all animals, an ultraviolet (UV) and a green (or a mid-wavelength) sensitivity, used to differentiate UV-rich sky or open space [4] from substrate, which reflects UV poorly. This solution is still found in several invertebrates [13] including many crustaceans [5]. It has also been postulated that two-channel colour vision evolved in the shallow Cambrian oceans in order to remove luminance flicker via the differential subtractive input that two spectral sensitivities allows [4,14]. Finally, since the available spectrum of light narrows with increasing depth or viewing distance, a pair of spectral channels may provide all the information needed (Figure 2). John Lythgoe and others developed the ‘offset hypothesis’, a slight variation on this, suggesting that two sensitivities are ideal under water. One is matched to the background, and one is offset to discriminate objects against that background [4,7]. The blue and green sensitivities of many oceanic predators (fish or marine mammals) support this hypothesis [15,16,17].
A good starting point for determining the performance and limits of colour vision is to measure spectral sensitivities. Such information can be determined by absorption microspectrophotometry (MSP) of dissociated photoreceptors (rods and cones in vertebrates, rhabdoms or rhabdomeres in invertebrates [17–19] or spectral absorption measurements from expressed visual pigments [20]. The sensitivities either method delivers should be viewed as a first estimate however. MSP, unless
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l-Max positions of cones and rods in 14 species of snapper (Lutjanus) species from green coastal through clearer blue outer ocean waters are compared. Rod sensitivities — vertical bars, single cones — filled circles, double cones — semicircles. Vertical lines plot the zones of greatest sensitivity for each water type for visual pigments within at least 90% of optimum. Note how double cones fall within this range.Adapted from [4,12]. Current Opinion in Neurobiology 2015, 34:86–94
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performed systematically, often misses photoreceptor classes, while opsin expression almost invariably overestimates what the animal actually uses for colour vision. In a systematic MSP examination of 39 species of Hawaiian reef fish, Losey and co-workers determined that dichromatic or trichromatic colour vision apparently dominate in this ecosystem [19]. Analyses of these results [21,22] used the considerable overlap of double and single cone sensitivities in some species (Figure 3) to suggest that, as in birds [7], double cones may function as a luminance channel and that only the single cones participate in colour vision (for definitions of cone types, see [23]). This hypothesis is supported by the fact that among several marine fish, double cone sensitivities match light availability in the varying habitats occupied [7,12,22]. More recent behavioural observations, however, demonstrate that in one species of triggerfish, Rhinecanthus aculeatus, double cone members are certainly used separately in the construction of a trichromatic colour sense with the other single cone present [24]. It seems likely, therefore, that double cone function is variable, possibly
including polarisation vision [8,25] but cross-species behavioural evidence is lacking. It is not always clear from a spectral sensitivity count alone, which receptor channels combine beneath the retina and coordinate colour-relevant behaviours. Electrophysiological recording from photoreceptors, interneurons, or brain areas associated with colour vision often detects opponent processing [26]. Barry and Hawryshyn recorded extracellularly from retinal ganglion cells and optic tectum in the Hawaiian wrasse, Thalassoma duperrey, and found at least two cone mechanisms that appear well suited to their colour tasks [27]. Gruber and colleagues (1975) [28] and Bedore et al. [29] used electroretinogram (ERG) recordings to demonstrate multiple spectral sensitivity classes in rays. Recordings in invertebrates are mostly limited to early work, confirming mono or dichromacy in crabs and other crustaceans (for review [5]). More recently they have been used to determine the sensitivities of stomatopod photoreceptors [30,31,32], confirming the general pattern of results from MSP [18,31] but also identifying an extensive population of
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The spectral sensitivities of four species of reef fish from the same photic microhabitat. Normalized sensitivities include filtering by ocular media, in non-UV sensitive species often close to 400 nm. Note the diversity of peak positions, spectral sensitivity number and mix of single and double cones. Rods, black, single cones, red and double cones, blue curves.Adapted from [4,22]. Current Opinion in Neurobiology 2015, 34:86–94
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UV-sensitive photoreceptors (Figure 1 [30]). An interesting recent study of the ocular media filtering mechanisms stomatopods use to construct their UV sensitivities revealed a rare instance of an animal multiplying spectral channels using variable cut-off filtering and a single visual pigment [33]. Ultimately it is the behaviour of the animal relative to colour that allows us to state what type of colour vision it has. Reaction to colour varies from simple phototaxis, moving to or away from coloured areas as shown in beach amphipods [34], through wavelength-specific behaviours, to complex colour association and categorisation tasks (see [35,36] for useful summaries). Behavioural evidence in elasmobranch rays is consistent with the earlier electrophysiology [28,29], identifying likely trichromacy in the giant shovel-nosed ray Glaucostegus typus [37]. Aside from the triggerfish studies already mentioned [24], the reef damselfish, Pomacentrus ambionensis, is known to use colour choice in operant conditioning and may extend this to more complex tasks in the UV including individual facial recognition [38,39]. As indicated both by opsin types [40] and ocular media transmission [41], damselfish and other small fish on the reef [42] could use UV as a private short-distance communication channel, as larger predatory fish lack UV sensitivity [41]. Colour-vision models and field observation reveal that ‘cleaner blue’ is used as a colour code by several cleaner fish and crustaceans [43]. In addition, such modelling shows that fish with UV sensitivity are at a great advantage, not just with UV spectra or UV silhouetted prey becoming more visible [39,41] but due to boosted colour discrimination across colour space [16]. Marine invertebrates with behavioural evidence for colour vision include the fiddler crabs [44] and blue crab [45]. Crab colour sense is most likely based both on twochannel UV/violet — green retinal sensitivities and on achromatic cues [46]. Molecular evidence for more than two spectral sensitivities does exist in fiddler crabs [47]; however, it is not clear to what extent this reflects seasonal or other environmental tuning as opposed to an extension of dichromacy. Stomatopods have been known for some time to possess true colour vision in colour versus grey-card tests [48], hardly a surprise given their diverse spectral sensitivities and colourful lifestyle [49]. Early speculation pointed towards a series of dichromatic mechanisms, based on anatomy and subretinal neural connections. However more recent results indicate a far more interesting system of processing. Thoen et al. [32] demonstrate that stomatopods discriminate wavelengths up to ten times less well than other animals, such as humans, honey bees and goldfish. Theoretically, if their colour sense were based on photoreceptor comparisons, mantis shrimp hue discrimination should be extremely fine, so these results www.sciencedirect.com
indicate a different approach to processing of their twelve channel input. Our current hypothesis is that the relative spectral excitations of these twelve bins are read off as a serial linear excitation pattern. Such an unconventional way to conduct colour vision requires specific subretinal wiring, currently under investigation. Comfortingly it does explain away the worry of dodecachromatic colour vision [50].
Too many opsins? It is increasingly common to estimate spectral sensitivities through examining opsin expression. Many insects are molecularly trichromatic, with a UV, blue and green (or LWS for Long Wave Sensitive) classes of opsins. Of marine invertebrates, so far only stomatopods and possibly fiddler crabs reveal more than two spectral classes [13,47,51]. Early in vertebrate evolution, at least as early as lampreys, five classes of opsin arose [20,52]. These are the RH1 class found in rods and four cone opsin classes: SWS1 — very short (often UV) sensitive, SWS2 — short wavelength (often blue) sensitive, RH2 — a medium wavelength, green-sensitive rod-like opsin, and LWS — long wavelength (up to red) sensitive class [2]. It is surprising how often gene duplications, deletions and substitutions multiply and change opsins. For example, among the visually unexciting ostracods, Oakley and colleagues identify eight opsin types [53] while in stomatopods, Porter and colleagues find over thirty opsins in some species [51]. In fish, it is not uncommon to find seven to ten or more opsins expressed at a functional level [2,54]. Serial duplications, deletions, gene conversions and other transformations allow great plasticity, especially when coupled to subsequent differential gene expression and modification [55,56]. For example, in a recent survey of percomorph fish species, a new class of SWS2 gene was described [57]. Other recent studies find RH2 gene loss in pufferfish [58] and loss of SWS1 and LWS in marine mammals [15]. Having this variation available may contribute to rapid speciation in fish [2]. Hofmann et al. showed that in damselfish, varying light environment has shaped opsin diversity, particularly in the SWS and LWS classes [40]. Important to note is that not all opsins are necessarily functional at any one time, and how and when each subclass is used throughout life is poorly understood. A number of factors including the following require careful consideration. (a) Co-expression of different visual pigments in the same photoreceptor is now recognised in both invertebrates [51] and vertebrates [59]. In some examples this widens the overall spectral response of the cell; however, it may sometimes reflect a photoreceptor transitory phase. Current Opinion in Neurobiology 2015, 34:86–94
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(b) Spectral sensitivities may change during the life of an animal on a developmental, seasonal, sexual, or other basis (see e below). This may be achieved through opsin expression differences and/or a change in chromophore from A1 to A2, a transformation that extends sensitivities to longer wavelengths [7]. Almost all marine fish, including tuna [56] or bream [60] go through a larval stage, and where examined these often have a different opsin quota to the adult. Functionally this may reflect a change in foraging mode and/or light environment. (c) Retinal functional subdivision is common in invertebrates with compound eyes but is also found in fish, with different areas expressing different opsins [59,61]. Although examples of this are currently limited to freshwater, it is also likely in marine
species as their retinas often mirror the vertical change in photic environment underwater. Higher sensitivity double cones are dense in the dorsal retina, which looks into dim deeper water, while more single cones for colour specific tasks are present in the ventral and medial retina [62]. In this way, retinal sensitivities vary across the retina to match the spatially varying light environment. This above any other reason may explain the supernumerary spectral sensitivity diversity seen in fish. (d) Short-term spectral sensitivity plasticity is known in both fish and invertebrates, a surprise given our assumption that an animal’s colour sense was fixed for life or at least long-term life periods. Diurnal opsin expression changes have been recorded in freshwater cichlids and killifish [63,64]. Sensitivities also change
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Fine colour pattern combinations through resolution breakdown in Thalassoma lunare (moon wrasse, a, c, e) and Pygoplites diacanthus (angelfish, b, d, f). Fish colours (a,b) measured using reflectance spectrophotometry (c,d) where curves are colour-coded to fish colours in a and b, combine over a few metres underwater, especially to the relatively poor-resolution eyes of fish. Combined curves plotted in red in e and f. The complex colours of wrasse and parrotfish, combine to give a good match to background blue spacelight, at least for the spectrum up to 600 nm, which encompasses most of the blue-shifted sensitivities known in reef fish. Yellow and blue, frequent in reef fish colouration for a variety of reasons combine to a uniform grey spectral reflection, good camouflage in several contexts and in marked contrast to the highly conspicuous colour combination close up.Adapted from [67]. Current Opinion in Neurobiology 2015, 34:86–94
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Colour vision in marine organisms Marshall, Carleton and Cronin 91
with the spectral content of light available, correlating to different settlement depths as larvae take up their adult habitat [65]. (e) Unconventional colour vision, such as that seen in stomatopods (or on land in butterflies [50]) may result in a large number of opsin types, aimed not at allowing finer colour chromatic evaluation, but either to deliver to stomatopods the required spectral coverage that their spectral-pattern recognition system requires or to add sensitivities for specific colour tasks. This latter wavelengthspecific colour vision, with or without accompanying retinal subdivision, is worth more attention in the ocean.
Colours, colour vision and spectral sensitivity spacing The colours and colour vision systems around coral reefs have received recent attention [16,21,22,43,66,67]. These studies re-confirm many of the original visual ecological observations of Lythgoe and colleagues, such as the use of yellow and blue in marine waters for efficient signal transmission [7]. The relatively poor spatial acuity of fish vision is also important in colour communication, as many of the fine colour patterns of reef fish, for example, while conspicuous close up, add together through resolution breakdown to give grey or match to blue background space-light at a distance [67] (Figure 4). The blue-shifted spectral sensitivities of reef fish also deliver another camouflage surprise, as yellow (a common colour on the reef) is in fact well matched to an average coral colour up to around 600 nm [67]. Yellow fish seem conspicuous to us, as our primate colour vision is particularly concerned with ripening fruit and leaves in this spectral region. As with colour mixing, yellow may be both conspicuous and camouflaged as required on the reef, as it contrasts well to a blue water background but matches the yellow/green corals [16,67]. Characterisation of reef fish colour vision has revealed a greater diversity than might be expected (Figure 3) [4,19,22]. Fish from very similar light micro-habitats possess widely differing spectral sensitivity placement, and while it is easy to state that this must somehow be related to their species-specific colour task needs, these are not obvious. Modelling of a number of colour tasks with different spectral sensitivity combinations suggests that the exact placement of the colour channels may vary without greatly affecting performance [4,16]. This is also seen in the variability of spectral sensitivities in 40 species of flower-visiting hymenopterans [4]. The idea of neutral drift in the evolution of spectral sensitivity tuning may be uncomfortable but is worth considering until well defined behaviour to colour task connections are found. www.sciencedirect.com
Fluorescence of stomatopods and fish (among other animals including jumping spiders and birds) has been implicated as a means of boosting colour communication [68,69]. The fluorescent emission of stomatopods increases the underlying colour signal by 15%, enough to be seen; however, behavioural evidence of the significance of the fluorescent component is lacking. Triplefins, wrasse, and now more than 180 other species of marine fish [70] are known to fluoresce and may do so at specific depths where the longer wavelengths (yellowred) of these blue-water-excited emissions are prominent. Despite several attempts [71], behavioural evidence for fluorescent function in fish remains unconvincing, as it fails to differentiate other colour pattern elements. Many pigments in nature fluoresce, and it remains possible that fluorescence in fish serves no visual function.
Conclusions and future perspectives There is great diversity in opsin complements amongst marine animals suggesting excellent colour vision capabilities. However, before assuming animals with multiple opsins are attempting higher levels of spectral discrimination, two other explanations must be considered. Firstly, large opsin numbers are clearly a dynamic way to tune colour vision to the needs of animal on a variety of evolutionary or within-lifetime timescales [57]. Additionally, multiple spectral sensitivities may also reflect unconventional processing and/or a colour sense that is functionally subdivided across the retina. At present, there is a great need for behavioural observation to back up hypotheses and ideas gleaned from more immediate methods, and this necessarily includes in situ observation of how colour is used. The ocean is not an easy place to work, but there is clearly a great diversity of colour vision systems within it that make it worth the effort, and our greater knowledge of freshwater systems provides tantalising glimpses of discoveries-in-waiting. We also suggest that the top-down approach of phylogeny, evolution and molecular genetics needs a more effective dialogue with the functional, anatomical or neurobiological side of colour vision as identified in the recent review of Kemp et al. [72].
Conflicts of interest Nothing declared.
Acknowledgements The opinion expressed here are very clearly a distillation of many years work, not just from ourselves, but from many exceptional and enlightened colleagues. These include John Lythgoe, Horace Barlow, Bill McFarland, Ellis Loew, Craig Hawryshyn, Tom Kocher, Roy Caldwell, George Losey, Misha Vorobyev and Daniel Osorio. We apologise for necessarily citing secondary references that also summarise their seminal work.
JM is supported by funding from the Australian Research Council, the Asian Office of Aerospace Research and Development and the Airforce Office of Current Opinion in Neurobiology 2015, 34:86–94
92 Molecular biology of sensation
Scientific Research (AFOSR). TC through the National Science Foundation (NSF) and AFOSR. KC through NSF.
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1.
Wald G: The molecular basis of visual excitation. Nature 1968, 219:800-807.
2.
Hunt DM, Hankins MW, Collin SP, Marshall NJ (Eds): Evolution of Visual and Non-visual Pigments. Springer; 2014.
This recent review captures the latest research on visual pigments, within photoreceptors and elsewhere, across both invertebrates and vertebrates. Data from several streams including electrophysiological, behavioural and molecular biology are included with highlights being the recent advances in opsin expression and visual pigment function. 3.
Barlow HB: What causes trichromacy? A theoretical analysis using comb-filtered spectra. Vis Res 1982, 22:635-643.
4. Cronin TW, Johnsen S, Marshall NT, Warrant EJ: Visual Ecology. Princeton University Press; 2014. This is a much needed update of the 1979 volume, The Ecology of Vision, by John Lythgoe, and reviews and expands this area of visual neuroscience. The subdiscipline of visual ecology recognises the link between the design of visual systems and the environment, as well as examining behavioural and evolutionary aspects. Visual Ecology contains many chapters relevant to marine colour vision, including examinations of photic habitat and colour vision. 5.
Marshall NJ, Kent J, Cronin TW: Visual adaptations in crustaceans: spectral sensitivity in diverse habitats. In Adaptive Mechanisms in the Ecology of Vision. Edited by Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S. Springer; 1999:285-327.
6.
Marshall NJ, Messenger JB: Colour-blind camouflage. Nature 1996, 382:408-409.
7.
Lythgoe J: The Ecology of Vision. Clarendon Press; 1979.
8.
Horva´th G (Ed): Polarized Light and Polarization Vision in Animal Sciences. Springer; 2014.
A twenty five chapter book that comprehensively examines recent advances in polarization vision. This includes the recent notion, advanced by authors of this article, that the information content in polarisation signals from animals makes this modality equivalent to colour vision. To some extent, this explains why many marine animals, notably the invertebrates, seem to have adopted polarization over colour in the marine environment. 9.
Marshall NJ, Cronin TW: Polarisation vision. Curr Biol 2011, 21:R101-R105.
10. Widder EA: Bioluminescence in the Ocean: origins of biological, chemical, and ecological diversity. Science 2010, 328:704-708. 11. Munz FW, McFarland WN: The significance of spectral position in the rhodopsins of tropical marine fishes. Vis Res 1973, 13:1829-1874. 12. Lythgoe J, Muntz W, Partridge JC, Shand J, Williams DM: The ecology of the visual pigments of snappers (Lutjanidae) on the Great Barrier Reef. J Comp Physiol A 1994, 174:461-467. 13. Briscoe AD, Chittka L: The evolution of colour vision in insects. Annu Rev Entomol 2001, 46:471-510. 14. Maximov V: Environmental factors which may have led to the appearance of colour vision. Philos Trans R Soc Lond B 2000, 355:1239-1242. 15. Meredith RW, Gatesy J, Emerling CA, York VM, Springer MS: Rod monochromacy and the coevolution of cetacean retinal opsins. PLoS Genet 2013, 9:e1003432. Shows that cetaceans have dispensed with all cone pigments and thus maintain all-rod retinas, other marine mammals express green opsins but no cetacean is known to express a blue-sensitive cone pigment. The narrow spectral deep-water foraging habitats of many marine mammals and lack of colour in mate choice may have driven this reduction. Current Opinion in Neurobiology 2015, 34:86–94
Pinnipeds also are thought to have lost blue cones. Colour vision therefore seems unlikely or at least rudimentary in marine mammals, although there remains behavioural evidence suggesting that some dolphins and some pinnipeds do make colour choices. This may be the result of rodcone dichromatic-like subretinal processes. 16. Marshall NJ, Vorobyev M: The design of color signals and color vision in fishes. In Sensory Processing in Aquatic Environments. Edited by Collin SP, Marshall NJ. Springer; 2003:194-222. 17. Hart NS, Lisney TJ, Marshall NJ, Collin SP: Multiple cone visual pigments and the potential for trichromatic colour vision in two species of elasmobranch. J Exp Biol 2004, 207:4587-4594. 18. Cronin TW, Marshall NJ: A retina with at least ten spectral types of photoreceptors in a mantis shrimp. Nature 1989, 339:137-140. 19. Losey GS, McFarland WN, Loew ER, Zamzow JP, Nelson PA, Marshall NJ: Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments. Copeia 2003, 3:433-454. 20. Yokoyama S: Evolution of dim-light and color vision pigments. Annu Rev Genomics Hum Genet 2008, 9:259-282. 21. Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS: Visual biology of Hawaiian coral reef fishes. II. Colors of Hawaiian coral reef fish. Copeia 2003, 3:455-466. 22. Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS: Visual biology of Hawaiian coral reef fishes. III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 2003, 3:467-480. 23. Walls GL: The Vertebrate Eye and its Adaptive Radiation. The Cranbrook Press; 1942. 24. Pignatelli V, Champ C, Marshall J, Vorobyev M: Double cones are used for colour discrimination in the reef fish, Rhinecanthus aculeatus. Biol Lett 2010, 6:537-539. 25. Kelber A, Roth LSV: Nocturnal colour vision — not as rare as we might think. J Exp Biol 2006, 209:781-788. 26. Kamermans M, Kraaij DA, Spekreijse H: The cone/horizontal cell network: a possible site for color constancy. Vis Neurosci 1998, 15:787-797. 27. Barry KL, Hawryshyn CW: Spectral sensitivity of the Hawaiian saddle wrasse, Thalassoma duperrey, and implications for visually mediated behaviour on coral reefs. Environ Biol Fishes 1999, 56:429-442. 28. Gruber SH: Duplex vision in the elasmobranchs; histological, electrophysiological and psychophysical evidence. In Vision in Fishes: New Approaches in Research. Edited by Ali MA. Plenum Press; 1975:525-540. 29. Bedore C, Loew E, Frank T, Hueter R, McComb DM, Kajiura S: A physiological analysis of color vision in batoid elasmobranchs. J Comp Physiol A 2013, 199:1129-1141. Physiological approaches were used to examine colour and specifically UV vision in two species of sting ray. ERG revealed multiple sensitivity peaks, including in the UV although no UV cones were identified. MSP showed two or three cone visual types, consolidating the previous work of Hart and colleagues [17] and the behavioural evidence of Van-Eyk et al. [37] showing likely trichromatic colour vision in shovel nosed rays. 30. Marshall NJ, Oberwinkler J: The colourful world of the mantis shrimp. Nature 1999, 401:873-874. 31. Marshall J, Cronin TW, Kleinlogel S: Stomatopod eye structure and function: a review. Arthropod Struct Dev 2007, 36:420-448. 32. Thoen HH, How MJ, Chiou T-H, Marshall NJ: A different form of color vision in mantis shrimp. Science 2014, 343:411-413. Using both intracellular electrophysiology and behaviour, the colour vision system of the stomatopod Haptosquilla trispinosa is described. Wavelength discrimination experiments are used to show that, in some ways unexpectedly, stomatopods possess discrimination levels around ten times worse than those of other animals similarly tested, including humans, butterflies, bees and goldfish. The hypothesis suggested to explain this relies on a completely new form of colour coding in which the spectrum is coded as a serially related colour pattern, rather than colours being judged from analogue comparison of two (or more) receptor output. www.sciencedirect.com
Colour vision in marine organisms Marshall, Carleton and Cronin 93
The need to cover the spectrum with this new system therefore explains the need for full spectral coverage and twelve spectral sensitivities. The neural connection requirements underlying this are currently under investigation. 33. Bok MJ, Porter ML, Place AR, Cronin TW: Biological sunscreens tune polychromatic ultraviolet vision in mantis shrimp. Curr Biol 2014, 24:1636-1642. This examination of the UV sensitivities in stomatopods revealed several new features to this unusual visual system. They include: the use of mycosporine amino acids (MAAs) within the optical elements of the eye (crystalline cones) as variable UV filters to tune spectral sensitivity; selective filtering of visual pigment using short-pass filtering (long-pass is more common); multiplication of UV sensitivities using two visual pigments and several differential UV filters. This is unusual in the animal kingdom with animals generally providing a new visual pigment for every new added spectral sensitivity. 34. Ugolini A, Vignali B, Castellini C, Lindstrom M: Zonal orientation and spectral filtering in Talitrus saltator (Amphipoda, Talitridae). J Mar Biol Assoc UK 1996, 76:377-389. 35. Kelber A, Vorobyev M, Osorio D: Animal colour vision — behavioural tests and physiological concepts. Biol Rev 2003, 78:81-118. 36. Kelber A, Osorio D: From spectral information to animal colour vision: experiments and concepts. Proc Biol Sci 2010, 277:1617-1625. 37. Van-Eyk SM, Siebeck UE, Champ CM, Marshall NJ, Hart NS: Behavioural evidence for colour vision in an elasmobranch. J Exp Biol 2011, 214:4186-4192. 38. Siebeck UE, Wallis GM, Litherland L: Colour vision in coral reef fish. J Exp Biol 2008, 211:354-360. 39. Siebeck UE, Losey GS, Marshall NJ: UV communication in Fish. In Communication in Fishes, Vol 2. Edited by Laddich F, Collin SP, Moller P, Kapoor BG. Science Publications Inc.; 2006:423-455. 40. Hofmann CM, Marshall NJ, Abdilleh K, Patel Z, Siebeck UE, Carleton KL: Opsin evolution in Damselfish: convergence, reversal, and parallel evolution across tuning sites. J Mol Evol 2012, 75:79-91. 41. Siebeck UE, Marshall NJ: Ocular media transmission of coral reef fish — can coral reef fish see ultraviolet light? Vis Res 2001, 41:133-149. 42. Losey GS, Cronin TW, Goldsmith T, Hyde D, Marshall NJ, McFarland WN: The UV visual world of fishes: a review. J Fish Biol 1999, 54:921-943. 43. Cheney KL, Grutter AS, Blomberg SP, Marshall NJ: Blue and yellow signal cleaning behavior in coral reef fishes. Curr Biol 2009, 19:1283-1287. 44. Detto T: The fiddler crab Uca mjoebergi uses colour vision in mate choice. Proc Biol Sci 2007, 274:2785-2790. 45. Baldwin J, Johnsen S: The importance of color in mate choice of the blue crab Callinectes sapidus. J Exp Biol 2009, 212:3762-3768. 46. Baldwin J, Johnsen S: The male blue crab, Callinectes sapidus, uses both chromatic and achromatic cues during mate choice. J Exp Biol 2012, 215:1184-1191. 47. Rajkumar P, Rollmann SM, Cook TA, Layne JE: Molecular evidence for color discrimination in the Atlantic sand fiddler crab, Uca pugilator. J Exp Biol 2010, 213:4240-4248. 48. Marshall NJ, Jones J, Cronin TW: Behavioural evidence for colour vision in stomatopod crustaceans. J Comp Physiol A 1996, 179:473-481.
increasingly being recognised in vertebrates also, including fish [59,61]. Stomatopod colour vision is defined as particularly unconventional with colour coding via spectral pattern recognition over the entire spectrum rather than spectral channel comparisons as found in all other colour vision types [32]. 51. Porter ML, Speiser DI, Zaharoff AK, Caldwell RL, Cronin TW, Oakley TH: The evolution of complexity in the visual systems of stomatopods: insights from transcriptomics. Integr Comp Biol 2013, 53:39-49. The research described here uses transcriptomics to examine the diversity of opsins in stomatopod crustaceans and attempts to place this in an evolutionary context. Some species express up to 33 opsins while the retina has a maximum of 16 photoreceptor types at the functional level. 52. Collin SC, Davies W, Hart NS, Hunt D: The evolution of early vertebrate photoreceptors. Philos Trans R Soc Lond B 2009, 364:2925-2940. 53. Oakley TH, Huber D: Differential expression of duplicated opsin genes in two eyetypes of ostracod crustaceans. J Mol Evol 2004, 59:239-249. 54. Carleton KL, Spady T, Streelman JT, Kidd M, McFarland W, Loew E: Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biol 2008, 6:22. 55. Hofmann C, Carleton KL: Gene duplication and differential gene expression play an important role in the diversification of visual pigments in fish. Integr Comp Biol 2009, 49:630-643. 56. Nakamura Y, Mori K, Saitoh K, Oshima K, Mekuchi M, Sugaya T, Shigenobu Y, Ojima N, Muta S, Fujiwara A et al.: Evolutionary changes of multiple visual pigment genes in the complete genome of Pacific bluefin tuna. Proc Nat Acad Sci USA 2013, 110:11061-11066. Here the tuna genome has been sequenced to show that opsin genes duplicate in tandem and also undergo gene conversion. 57. Cortesi F, Musilova´ Z, Stieb S, Hart NS, Siebeck UE, Malmstrøm M, Tørresen OK, Jentoft S, Cheney KL, Marshall NJ, Carleton KL, Salzburger W: Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes. PNAS 2015, 112:1493-1498. A comprehensive survey of 100 fish species that documents the evolutionary history of the SWS2 gene. A new gene duplication is identified along with, in some groups, losses and conversions in this violet/blue sensitive opsin class, coinciding with radiation of the highly diverse percomorphs. One species, Pseudochromis fuscus, is used to exemplify how gene differences occur within one species ontogenetically. 58. Neafsey DE, Hartl DL: Convergent loss of an anciently duplicated, functionally divergent RH2 opsin gene in the fugu and Tetraodon pufferfish lineages. Gene 2005, 350:161-171. 59. Dalton BE, Loew ER, Cronin TW, Carleton KL: Spectral tuning by opsin coexpression in retinal regions that view different parts of the visual field. Proc Biol Soc 2014, 281:1797. 60. Shand J, Davies W, Thomas N, Balmer L, Cowing J, Pointer M: The influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream Acanthopagrus butcheri. J Exp Biol 2008, 211:1495-1503. 61. Temple SE: Why different regions of the retina have different spectral sensitivities: a review of mechanisms and functional significance of intraretinal variability in spectral sensitivity in vertebrates. Vis Neurosci 2011, 28:281-293. 62. Fritsches KA, Marshall NJ, Warrant EJ: Retinal specializations in the blue marlin: eyes designed for sensitivity to low light levels. Mar Freshwater Res 2003, 54:333-341.
49. Caldwell RL, Dingle H: Stomatopods. Sci Am 1976, 234:80-89.
63. Halstenberg S, Lindgren K, Samagh S, Nadal-Vicens M, Balt S, Fernald R: Diurnal rhythm of cone opsin expression in the teleost fish Haplochromis burtoni. Vis Neurosci 2005, 22:135-141.
50. Marshall NJ, Arikawa K: Unconventional colour vision. Curr Biol 2014, 24:R1150. Unconventional colour vision is explored and defined. It is suggested that multiple colour channels, including up to nine in butterflies and 12 in stomatopods are not attempts at increasing colour space dimensionality. In the butterflies, spectral channels are added to conduct specific colour tasks or wavelength specific behaviours. Segregation of the retina also contributes to spectral sensitivity multiplication, with different photoreceptor combinations examining different regions of visual space. This is
64. Johnson AM, Stanis S, Fuller RC: Diurnal lighting patterns and habitat alter opsin expression and colour preferences in a killifish. Proc R Soc Lond B 2013:280. This paper shows opsin expression varying on a diurnal basis, following to some extent lighting levels. While this example is in freshwater fish, this is likely to occur in the marine environment also, reflecting changes in light over the 24 h period. Such changes as with [63] are quantitative amplification of expression within one opsin type rather appearance or disappearance of different types.
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65. Cronin TW, Caldwell RL, Marshall NJ: Sensory adaptation — tunable colour vision in a mantis shrimp. Nature 2001, 411:547-548.
the potentially new fluorescing compounds that it identifies. It does point out in passing that the yellow filters found in the ocular media of several fish, including many wrasse, may help enhance the fluorescent signal.
66. Marshall NJ: The visual ecology of reef fish colours. In Animal Signals: Signalling and Signal Design in Animal Communication. Edited by Espmark Y, Amundsen T, Rosenqvist G. Tapir Press; 2000:83-120.
71. Gerlach T, Sprenge D, Michiels NK: Fairy wrasses perceive and respond to their deep red fluorescent coloration. Proc R Soc Lond B 2014, 281:20140787. Part of an extended effort by Michiels and colleagues to show that fluorescence is used in visual behaviour in fish. Mate choice tests demonstrate that fish including the fluorescent component of their colours are favoured over those that have it removed by selective lighting. However behavioural arena lighting conditions are not natural and fail to differentiate the added component of the fluorescence that forms part of an underlying and otherwise obvious colour pattern.
67. Marshall NJ: Conspicuousness and camouflage with the same ‘bright’ colours. Colours for concealment and camouflage in reef fish. Philos Trans R Soc Lond B 2000, 355:1243-1248. 68. Mazel C, Cronin TW, Caldwell RL, Marshall NJ: Fluorescent enhancement of signaling in a mantis shrimp. Science 2004, 303:51. 69. Michiels N, Anthes N, Hart NS, Herler J, Meixner A, Schleifenbaum F, Schulte G, Siebeck UE, Sprenger D, Wucherer M: Red fluorescence in reef fish: a novel signalling mechanism? BMC Ecol 2008, 8:16. 70. Sparks JS, Schelly RC, Smith WL, Davis MP, Tchernov D: The covert world of fish biofluorescence: a phylogenetically widespread and phenotypically variable phenomenon. PLoS ONE 2014, 9:e83259. This extensive survey of fish fluorescence using high-intensity excitation sources notes over 180 species of fish that fluoresce. Whether this fluorescence is also visually relevant to the fish themselves under ambient illumination is not demonstrated and this work may be more interesting for
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72. Kemp DJ, Herberstein ME, Fleishman LJ, Endler JA, Bennett ATD, Dyer AG, Hart NS, Marshall NJ, Whiting MJ: An integrative framework for the appraisal of coloration in nature. Am Nat 2015. (in press). This review or synopsis examines current methods and approaches in colour communication and colour vision in animals. It provides guidance in methods without being prescriptive and identifies two different views; first is the ‘top-down’ evolutionary/behavioural ecology school and second the more mechanistic ‘bottom-up’ neurophysiological/colour quantification school. Between these sit colour vision models which, as the article explains, are being misused due to a lack of communication between the two schools. Ways to remedy this and form a more unified, and to some extent standardised, approach to understanding aspects of colour vision are suggested.
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