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Colour vision in marine organisms
1 2 3
Justin Marshall , Karen L Carleton and Thomas Cronin
Colour vision in the marine environment is on average simpler In this brief review we examine some of the recent
than in terrestrial environments with simple or no colour vision advances in our understanding of colour vision in the ocean
through monochromacy or dichromacy. Monochromacy is across both invertebrates and vertebrates and place this in
found in marine mammals and elasmobranchs, including context of previous hypotheses. Because the ocean is hard
whales and sharks, but not some rays. Conversely, there is also to work within and because its contrasting niches may
a greater diversity of colour vision in the ocean than on land, deliver highly speciose animal assemblages, there are still
examples being the polyspectral stomatopods and the many many knowledge gaps. Some of our discussion extends
colour vision solutions found among reef fish. Recent advances from what we know about colour vision systems in fresh-
in sequencing reveal more opsin (visual pigment) types than water fish as few marine species are well described.
functionally useful at any one time. This diversity arises through
opsin duplication and conversion. Such mechanisms allow Spectral sensitivities and colour vision
pick-and-mix adaptation that tunes colour vision on a variety of Nearly always, a sense of colour requires the comparison
very short non-evolutionary timescales. At least some of the of excitations between photoreceptor cells with different
diversity in marine colour vision is best explained as spectral sensitivities. At its simplest two such cells, each
unconventional colour vision or as neutral drift. containing visual pigments with peak sensitivity in dif-
Addresses ferent spectral regions, will detect the same colour signal
1
Queensland Brain Institute, University of Queensland, Brisbane, differently, so relative excitation ratios can be compared
Queensland 4070, Australia
2 to form a dichromatic colour-vision system. Visual pig-
Department of Biology, University of Maryland, College Park, MD
ments are constructed from an opsin protein with cen-
20742, USA
3 trally bound chromophore, often 11-cis retinal [1]. Their
Department of Biological Sciences, University of Maryland Baltimore
County, Baltimore, MD 21250, USA peak sensitivity, or l-max, depends both on variability in
specific opsin amino acids and on the particular chromo-
Corresponding author: Marshall, Justin ([email protected])
phore used [2 ].
Current Opinion in Neurobiology 2015, 34:86–94 Because both visual pigment absorption spectra and
object reflection spectra are broad, within the 300–
This review comes from a themed issue on Molecular biology of
sensation 750 nm range of light over which visual pigments operate,
three or four visual pigments are usually sufficient [3,4 ]
Edited by David Julius and John Carlson
(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
http://dx.doi.org/10.1016/j.conb.2015.02.002 crustaceans and other invertebrates, remain colour-blind
0959-4388/# 2015 Elsevier Ltd. All rights reserved. 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.
Introduction Like their terrestrial counterparts, nocturnal and crepus-
Colour vision in the marine environment operates be- cular marine animals generally forgo colour vision alto-
tween two extremes. For some organisms, it is less gether, evolving a single spectral sensitivity for optimal
developed, with animals able to survive as colour-blind light absorption [2 ,7]. While some nocturnal animals
monochromats or at most dichromats. A few possess three possess colour vision on land, in the ocean it is more
or four spectral channels, potentially but not always, common for the opposite to be true. Many diurnal ani-
allowing them to venture into trichromacy or tetrachro- mals, including the cephalopods and many crustaceans,
macy, depending on how information is combined sub- have elaborated polarisation vision more than colour.
retinally. However, the ocean also boasts animals with Their single spectral sensitivity peaks around 500 nm,
complex colour vision such as the stomatopod crusta- an optimum for polarisation vision for several reasons
ceans with up to twelve spectral channels. Several outside the scope of this review [8,9].
drivers contribute to this complexity including the
light environment, phylogeny and behaviour relative In order to absorb as much light as possible, the matching
to colour. of photoreceptor sensitivity to bioluminescent emissions
Current Opinion in Neurobiology 2015, 34:86–94 www.sciencedirect.com
Colour vision in marine organisms Marshall, Carleton and Cronin 87
Figure 1
Stomatopod Reef fish Human
Crab
Cuttlefish
300 400 500 600 700
Current Opinion in Neurobiology
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 Evaluating colour vision type and evolution
vertebrate and invertebrate marine species to focus sen- A good starting point for determining the performance
sitivity between 450 and 500 nm [4 ,7]. The early visual and limits of colour vision is to measure spectral sensitiv-
ecology literature developed the ‘sensitivity hypothesis’ ities. Such information can be determined by absorption
to explain this adaptation [7,11]. The exact match microspectrophotometry (MSP) of dissociated photo-
depends on the local environment, as estuarine or marine receptors (rods and cones in vertebrates, rhabdoms or
water peak transmission varies from green to blue, and to rhabdomeres in invertebrates [17–19] or spectral ab-
an extent on diurnal activity periods. Therefore, species sorption measurements from expressed visual pigments
in either habitat will possess spectral sensitivities that [20]. The sensitivities either method delivers should
generally sample within the envelope of available light be viewed as a first estimate however. MSP, unless
provided by spatial and temporal variations [7,12].
Why is dichromacy common in many marine Figure 2
animals?
Based on our relatively scant knowledge of marine animal
colour vision, dichromacy emerges as the oceanic favour- Kasmira
Bohar reef
Outer
ite. This perhaps derives from what is thought to be the
Quinquelineatus
basal colour sense in all animals, an ultraviolet (UV) and a Adetii
Carponotatus
green (or a mid-wavelength) sensitivity, used to differen- reef
Russelli (adult) Middle
tiate UV-rich sky or open space [4 ] from substrate, Malabaricus
reef
which reflects UV poorly. This solution is still found in Sebae
Erythropterus
several invertebrates [13] including many crustaceans [5].
Russelli (juvenile)
It has also been postulated that two-channel colour vision Fulviflamma (juvenile)
evolved in the shallow Cambrian oceans in order to Johnii (adult)
Johnii (juvenile) Estuary Inner
remove luminance flicker via the differential subtractive
Argentimaculatus
input that two spectral sensitivities allows [4 ,14]. Final-
400 450 500 550 600
ly, since the available spectrum of light narrows with
increasing depth or viewing distance, a pair of spectral Wavelength (nm)
channels may provide all the information needed Current Opinion in Neurobiology
(Figure 2). John Lythgoe and others developed the ‘offset
hypothesis’, a slight variation on this, suggesting that two l-Max positions of cones and rods in 14 species of snapper (Lutjanus)
sensitivities are ideal under water. One is matched to the species from green coastal through clearer blue outer ocean waters
are compared. Rod sensitivities — vertical bars, single cones — filled
background, and one is offset to discriminate objects
circles, double cones — semicircles. Vertical lines plot the zones of
against that background [4 ,7]. The blue and green
greatest sensitivity for each water type for visual pigments within at
sensitivities of many oceanic predators (fish or marine least 90% of optimum. Note how double cones fall within this
mammals) support this hypothesis [15 ,16,17]. range.Adapted from [4 ,12].
www.sciencedirect.com Current Opinion in Neurobiology 2015, 34:86–94
88 Molecular biology of sensation
performed systematically, often misses photoreceptor clas- including polarisation vision [8,25] but cross-species
ses, while opsin expression almost invariably overestimates behavioural evidence is lacking.
what the animal actually uses for colour vision.
It is not always clear from a spectral sensitivity count
In a systematic MSP examination of 39 species of Hawai- alone, which receptor channels combine beneath the
ian reef fish, Losey and co-workers determined that retina and coordinate colour-relevant behaviours.
dichromatic or trichromatic colour vision apparently dom- Electrophysiological recording from photoreceptors,
inate in this ecosystem [19]. Analyses of these results interneurons, or brain areas associated with colour vision
[21,22] used the considerable overlap of double and single often detects opponent processing [26]. Barry and Hawry-
cone sensitivities in some species (Figure 3) to suggest shyn recorded extracellularly from retinal ganglion cells
that, as in birds [7], double cones may function as a and optic tectum in the Hawaiian wrasse, Thalassoma
luminance channel and that only the single cones partici- duperrey, and found at least two cone mechanisms that
pate in colour vision (for definitions of cone types, see appear well suited to their colour tasks [27]. Gruber and
[23]). This hypothesis is supported by the fact that among colleagues (1975) [28] and Bedore et al. [29 ] used elec-
several marine fish, double cone sensitivities match light troretinogram (ERG) recordings to demonstrate multiple
availability in the varying habitats occupied [7,12,22]. spectral sensitivity classes in rays. Recordings in inverte-
More recent behavioural observations, however, demon- brates are mostly limited to early work, confirming mono
strate that in one species of triggerfish, Rhinecanthus or dichromacy in crabs and other crustaceans (for review
aculeatus, double cone members are certainly used sepa- [5]). More recently they have been used to determine the
rately in the construction of a trichromatic colour sense sensitivities of stomatopod photoreceptors [30,31,32 ],
with the other single cone present [24 ]. It seems likely, confirming the general pattern of results from MSP
therefore, that double cone function is variable, possibly [18,31] but also identifying an extensive population of
Figure 3
Pervagor spilosoma Chromis verater 1.0 1.0
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0.0 0.0 300 400 500 600 700 300 400 500 600 700
Forcipiger flavissimus Chromis hanui 1.0 1.0
0.8 0.8 Spectral Sensitivity
0.6 0.6
0.4 0.4
0.2 0.2
0.0 0.0 300 400 500 600 700 300 400 500 600 700
Wavelength (nm)
Current Opinion in Neurobiology
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 www.sciencedirect.com
Colour vision in marine organisms Marshall, Carleton and Cronin 89
UV-sensitive photoreceptors (Figure 1 [30]). An interest- indicate a different approach to processing of their twelve
ing recent study of the ocular media filtering mechanisms channel input. Our current hypothesis is that the relative
stomatopods use to construct their UV sensitivities spectral excitations of these twelve bins are read off as a
revealed a rare instance of an animal multiplying spectral serial linear excitation pattern. Such an unconventional
channels using variable cut-off filtering and a single visual way to conduct colour vision requires specific subretinal
pigment [33]. wiring, currently under investigation. Comfortingly it
does explain away the worry of dodecachromatic colour
Ultimately it is the behaviour of the animal relative to vision [50 ].
colour that allows us to state what type of colour vision it
has. Reaction to colour varies from simple phototaxis,
Too many opsins?
moving to or away from coloured areas as shown in beach
It is increasingly common to estimate spectral sensitivi-
amphipods [34], through wavelength-specific behaviours,
ties through examining opsin expression. Many insects
to complex colour association and categorisation tasks
are molecularly trichromatic, with a UV, blue and green
(see [35,36] for useful summaries). Behavioural evidence
(or LWS for Long Wave Sensitive) classes of opsins. Of
in elasmobranch rays is consistent with the earlier electro-
marine invertebrates, so far only stomatopods and possi-
physiology [28,29 ], identifying likely trichromacy in the
bly fiddler crabs reveal more than two spectral classes
giant shovel-nosed ray Glaucostegus typus [37]. Aside from
[13,47,51 ]. Early in vertebrate evolution, at least as early as
the triggerfish studies already mentioned [24 ], the reef
lampreys, five classes of opsin arose [20,52]. These are the
damselfish, Pomacentrus ambionensis, is known to use
RH1 class found in rods and four cone opsin classes:
colour choice in operant conditioning and may extend
SWS1 — very short (often UV) sensitive, SWS2 — short
this to more complex tasks in the UV including individual
wavelength (often blue) sensitive, RH2 — a medium
facial recognition [38,39]. As indicated both by opsin
wavelength, green-sensitive rod-like opsin, and LWS —
types [40] and ocular media transmission [41], damselfish
long wavelength (up to red) sensitive class [2 ].
and other small fish on the reef [42] could use UV as a
private short-distance communication channel, as larger
It is surprising how often gene duplications, deletions and
predatory fish lack UV sensitivity [41]. Colour-vision
substitutions multiply and change opsins. For example,
models and field observation reveal that ‘cleaner blue’
among the visually unexciting ostracods, Oakley and
is used as a colour code by several cleaner fish and
colleagues identify eight opsin types [53] while in sto-
crustaceans [43]. In addition, such modelling shows that
matopods, Porter and colleagues find over thirty opsins in
fish with UV sensitivity are at a great advantage, not just
some species [51 ]. In fish, it is not uncommon to find
with UV spectra or UV silhouetted prey becoming more
seven to ten or more opsins expressed at a functional level
visible [39,41] but due to boosted colour discrimination
[2 ,54]. Serial duplications, deletions, gene conversions
across colour space [16].
and other transformations allow great plasticity, espe-
cially when coupled to subsequent differential gene
Marine invertebrates with behavioural evidence for col-
expression and modification [55 ,56]. For example,
our vision include the fiddler crabs [44] and blue crab [45].
in a recent survey of percomorph fish species, a new
Crab colour sense is most likely based both on two-
class of SWS2 gene was described [57 ]. Other recent
channel UV/violet — green retinal sensitivities and on
studies find RH2 gene loss in pufferfish [58] and loss of
achromatic cues [46]. Molecular evidence for more than
SWS1 and LWS in marine mammals [15 ]. Having this
two spectral sensitivities does exist in fiddler crabs [47];
variation available may contribute to rapid speciation in
however, it is not clear to what extent this reflects
fish [2 ].
seasonal or other environmental tuning as opposed to
an extension of dichromacy.
Hofmann et al. showed that in damselfish, varying light
Stomatopods have been known for some time to possess environment has shaped opsin diversity, particularly in
true colour vision in colour versus grey-card tests [48], the SWS and LWS classes [40]. Important to note is that
hardly a surprise given their diverse spectral sensitivities not all opsins are necessarily functional at any one time,
and colourful lifestyle [49]. Early speculation pointed and how and when each subclass is used throughout life is
towards a series of dichromatic mechanisms, based on poorly understood. A number of factors including the
anatomy and subretinal neural connections. However following require careful consideration.
more recent results indicate a far more interesting system
of processing. Thoen et al. [32 ] demonstrate that sto- (a) Co-expression of different visual pigments in the
matopods discriminate wavelengths up to ten times less same photoreceptor is now recognised in both
well than other animals, such as humans, honey bees and invertebrates [51 ] and vertebrates [59 ]. In some
goldfish. Theoretically, if their colour sense were based examples this widens the overall spectral response of
on photoreceptor comparisons, mantis shrimp hue dis- the cell; however, it may sometimes reflect a
crimination should be extremely fine, so these results photoreceptor transitory phase.
www.sciencedirect.com Current Opinion in Neurobiology 2015, 34:86–94
90 Molecular biology of sensation
(b) Spectral sensitivities may change during the life of an species as their retinas often mirror the vertical
animal on a developmental, seasonal, sexual, or other change in photic environment underwater. Higher
basis (see e below). This may be achieved through sensitivity double cones are dense in the dorsal retina,
opsin expression differences and/or a change in which looks into dim deeper water, while more single
chromophore from A1 to A2, a transformation that cones for colour specific tasks are present in the
extends sensitivities to longer wavelengths [7]. ventral and medial retina [62]. In this way, retinal
Almost all marine fish, including tuna [56] or bream sensitivities vary across the retina to match the
[60] go through a larval stage, and where examined spatially varying light environment. This above any
these often have a different opsin quota to the adult. other reason may explain the supernumerary spectral
Functionally this may reflect a change in foraging sensitivity diversity seen in fish.
mode and/or light environment. (d) Short-term spectral sensitivity plasticity is known in
(c) Retinal functional subdivision is common in inverte- both fish and invertebrates, a surprise given our
brates with compound eyes but is also found in fish, assumption that an animal’s colour sense was fixed for
with different areas expressing different opsins life or at least long-term life periods. Diurnal opsin
[59 ,61 ]. Although examples of this are currently expression changes have been recorded in freshwater
limited to freshwater, it is also likely in marine cichlids and killifish [63,64]. Sensitivities also change
Figure 4
(a) (b)
(c) (d)
1.0 1.0
0.8 0.8
0.6 0.6
0.4 0.4 Sensitivity 0.2 0.2
0.0 Normalised Reflectance / 0.0
Normalised Reflectance
300 400 500 600 700 300 400 500 600 700
(e) (f) 1.0 1.0
0.8 0.8
0.6 0.6
0.4 0.4 Radiance 0.2 0.2
0.0 0.0
Normalised Reflectance
Normalised Reflectance /
300 400 500 600 700 300 400 500 600 700
Wavelength (nm)
Current Opinion in Neurobiology
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 www.sciencedirect.com
Colour vision in marine organisms Marshall, Carleton and Cronin 91
with the spectral content of light available, correlating
Fluorescence of stomatopods and fish (among other ani-
to different settlement depths as larvae take up their
mals including jumping spiders and birds) has been
adult habitat [65].
implicated as a means of boosting colour communication
(e) Unconventional colour vision, such as that seen in
[68,69]. The fluorescent emission of stomatopods
stomatopods (or on land in butterflies [50 ]) may
increases the underlying colour signal by 15%, enough
result in a large number of opsin types, aimed not at
to be seen; however, behavioural evidence of the signifi-
allowing finer colour chromatic evaluation, but
cance of the fluorescent component is lacking. Triple-
either to deliver to stomatopods the required
fins, wrasse, and now more than 180 other species of
spectral coverage that their spectral-pattern recog-
marine fish [70] are known to fluoresce and may do so at
nition system requires or to add sensitivities for
specific depths where the longer wavelengths (yellow-
specific colour tasks. This latter wavelength-
red) of these blue-water-excited emissions are prominent.
specific colour vision, with or without accompa-
Despite several attempts [71], behavioural evidence for
nying retinal subdivision, is worth more attention in
fluorescent function in fish remains unconvincing, as it
the ocean.
fails to differentiate other colour pattern elements. Many
pigments in nature fluoresce, and it remains possible that
fluorescence in fish serves no visual function.
Colours, colour vision and spectral sensitivity
spacing
Conclusions and future perspectives
The colours and colour vision systems around coral reefs
There is great diversity in opsin complements amongst
have received recent attention [16,21,22,43,66,67].
marine animals suggesting excellent colour vision capa-
These studies re-confirm many of the original visual
bilities. However, before assuming animals with multiple
ecological observations of Lythgoe and colleagues, such
opsins are attempting higher levels of spectral discrimi-
as the use of yellow and blue in marine waters for
nation, two other explanations must be considered. First-
efficient signal transmission [7]. The relatively poor
ly, large opsin numbers are clearly a dynamic way to tune
spatial acuity of fish vision is also important in colour
colour vision to the needs of animal on a variety of
communication, as many of the fine colour patterns of
evolutionary or within-lifetime timescales [57 ]. Addi-
reef fish, for example, while conspicuous close up, add
tionally, multiple spectral sensitivities may also reflect
together through resolution breakdown to give grey or
unconventional processing and/or a colour sense that is
match to blue background space-light at a distance [67]
functionally subdivided across the retina.
(Figure 4). The blue-shifted spectral sensitivities of
reef fish also deliver another camouflage surprise, as
At present, there is a great need for behavioural observa-
yellow (a common colour on the reef) is in fact well
tion to back up hypotheses and ideas gleaned from more
matched to an average coral colour up to around 600 nm
immediate methods, and this necessarily includes in situ
[67]. Yellow fish seem conspicuous to us, as our primate
observation of how colour is used. The ocean is not an
colour vision is particularly concerned with ripening
easy place to work, but there is clearly a great diversity of
fruit and leaves in this spectral region. As with colour
colour vision systems within it that make it worth the
mixing, yellow may be both conspicuous and camou-
effort, and our greater knowledge of freshwater systems
flaged as required on the reef, as it contrasts well to a
provides tantalising glimpses of discoveries-in-waiting.
blue water background but matches the yellow/green
We also suggest that the top-down approach of phyloge-
corals [16,67].
ny, evolution and molecular genetics needs a more effec-
tive dialogue with the functional, anatomical or
Characterisation of reef fish colour vision has revealed a
neurobiological side of colour vision as identified in the
greater diversity than might be expected (Figure 3)
recent review of Kemp et al. [72 ].
[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 Conflicts of interest
related to their species-specific colour task needs, these Nothing declared.
are not obvious. Modelling of a number of colour tasks
with different spectral sensitivity combinations suggests Acknowledgements
that the exact placement of the colour channels may vary The opinion expressed here are very clearly a distillation of many years
work, not just from ourselves, but from many exceptional and enlightened
without greatly affecting performance [4 ,16]. This is
colleagues. These include John Lythgoe, Horace Barlow, Bill McFarland,
also seen in the variability of spectral sensitivities in
Ellis Loew, Craig Hawryshyn, Tom Kocher, Roy Caldwell, George Losey,
40 species of flower-visiting hymenopterans [4 ]. The Misha Vorobyev and Daniel Osorio. We apologise for necessarily citing
secondary references that also summarise their seminal work.
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
JM is supported by funding from the Australian Research Council, the Asian
are found. Office of Aerospace Research and Development and the Airforce Office of
www.sciencedirect.com Current Opinion in Neurobiology 2015, 34:86–94
92 Molecular biology of sensation
Scientific Research (AFOSR). TC through the National Science Pinnipeds also are thought to have lost blue cones. Colour vision there-
Foundation (NSF) and AFOSR. KC through NSF. fore seems unlikely or at least rudimentary in marine mammals, although
there remains behavioural evidence suggesting that some dolphins and
References and recommended reading
some pinnipeds do make colour choices. This may be the result of rod-
Papers of particular interest, published within the period of review,
cone dichromatic-like subretinal processes.
have been highlighted as:
16. Marshall NJ, Vorobyev M: The design of color signals and color
of special interest vision in fishes. In Sensory Processing in Aquatic Environments.
of outstanding interest Edited by Collin SP, Marshall NJ. Springer; 2003:194-222.
17. Hart NS, Lisney TJ, Marshall NJ, Collin SP: Multiple cone visual
1. Wald G: The molecular basis of visual excitation. Nature 1968,
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two species of elasmobranch. J Exp Biol 2004, 207:4587-4594.
2. Hunt DM, Hankins MW, Collin SP, Marshall NJ (Eds): Evolution of
18. Cronin TW, Marshall NJ: A retina with at least ten spectral
Visual and Non-visual Pigments. Springer; 2014.
types of photoreceptors in a mantis shrimp. Nature 1989,
This recent review captures the latest research on visual pigments, within 339:137-140.
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brates. Data from several streams including electrophysiological, beha- 19. Losey GS, McFarland WN, Loew ER, Zamzow JP, Nelson PA,
vioural and molecular biology are included with highlights being the Marshall NJ: Visual biology of Hawaiian coral reef fishes. I.
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Princeton University Press; 2014. 21. Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS:
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between the design of visual systems and the environment, as well as
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Physiological approaches were used to examine colour and specifically
UV vision in two species of sting ray. ERG revealed multiple sensitivity
11. Munz FW, McFarland WN: The significance of spectral position
peaks, including in the UV although no UV cones were identified. MSP
in the rhodopsins of tropical marine fishes. Vis Res 1973,
13:1829-1874. showed two or three cone visual types, consolidating the previous work of
Hart and colleagues [17] and the behavioural evidence of Van-Eyk
12. Lythgoe J, Muntz W, Partridge JC, Shand J, Williams DM: The et al. [37] showing likely trichromatic colour vision in shovel nosed rays.
ecology of the visual pigments of snappers (Lutjanidae) on the
30. Marshall NJ, Oberwinkler J: The colourful world of the mantis
Great Barrier Reef. J Comp Physiol A 1994, 174:461-467.
shrimp. Nature 1999, 401:873-874.
13. Briscoe AD, Chittka L: The evolution of colour vision in insects.
31. Marshall J, Cronin TW, Kleinlogel S: Stomatopod eye structure
Annu Rev Entomol 2001, 46:471-510.
and function: a review. Arthropod Struct Dev 2007, 36:420-448.
14. Maximov V: Environmental factors which may have led to the
32. Thoen HH, How MJ, Chiou T-H, Marshall NJ: A different form of
appearance of colour vision. Philos Trans R Soc Lond B 2000,
355:1239-1242. color vision in mantis shrimp. Science 2014, 343:411-413.
Using both intracellular electrophysiology and behaviour, the colour
15. Meredith RW, Gatesy J, Emerling CA, York VM, Springer MS: Rod vision system of the stomatopod Haptosquilla trispinosa is described.
monochromacy and the coevolution of cetacean retinal Wavelength discrimination experiments are used to show that, in some
opsins. PLoS Genet 2013, 9:e1003432. ways unexpectedly, stomatopods possess discrimination levels around
Shows that cetaceans have dispensed with all cone pigments and thus ten times worse than those of other animals similarly tested, including
maintain all-rod retinas, other marine mammals express green opsins but humans, butterflies, bees and goldfish. The hypothesis suggested to
no cetacean is known to express a blue-sensitive cone pigment. The explain this relies on a completely new form of colour coding in which the
narrow spectral deep-water foraging habitats of many marine mammals spectrum is coded as a serially related colour pattern, rather than colours
and lack of colour in mate choice may have driven this reduction. being judged from analogue comparison of two (or more) receptor output.
Current Opinion in Neurobiology 2015, 34:86–94 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 increasingly being recognised in vertebrates also, including fish [59 ,61 ].
need for full spectral coverage and twelve spectral sensitivities. The neural Stomatopod colour vision is defined as particularly unconventional with
connection requirements underlying this are currently under investigation. colour coding via spectral pattern recognition over the entire spectrum
rather than spectral channel comparisons as found in all other colour
33. Bok MJ, Porter ML, Place AR, Cronin TW: Biological sunscreens
vision types [32 ].
tune polychromatic ultraviolet vision in mantis shrimp. Curr
Biol 2014, 24:1636-1642. 51. Porter ML, Speiser DI, Zaharoff AK, Caldwell RL, Cronin TW,
This examination of the UV sensitivities in stomatopods revealed several Oakley TH: The evolution of complexity in the visual systems of
new features to this unusual visual system. They include: the use of stomatopods: insights from transcriptomics. Integr Comp Biol
mycosporine amino acids (MAAs) within the optical elements of the eye 2013, 53:39-49.
(crystalline cones) as variable UV filters to tune spectral sensitivity; The research described here uses transcriptomics to examine the diver-
selective filtering of visual pigment using short-pass filtering (long-pass sity of opsins in stomatopod crustaceans and attempts to place this in an
is more common); multiplication of UV sensitivities using two visual evolutionary context. Some species express up to 33 opsins while the
pigments and several differential UV filters. This is unusual in the animal retina has a maximum of 16 photoreceptor types at the functional level.
kingdom with animals generally providing a new visual pigment for every
52. Collin SC, Davies W, Hart NS, Hunt D: The evolution of early
new added spectral sensitivity.
vertebrate photoreceptors. Philos Trans R Soc Lond B 2009,
34. Ugolini A, Vignali B, Castellini C, Lindstrom M: Zonal orientation 364:2925-2940.
and spectral filtering in Talitrus saltator (Amphipoda,
53. Oakley TH, Huber D: Differential expression of duplicated opsin
Talitridae). J Mar Biol Assoc UK 1996, 76:377-389.
genes in two eyetypes of ostracod crustaceans. J Mol Evol
35. Kelber A, Vorobyev M, Osorio D: Animal colour vision — 2004, 59:239-249.
behavioural tests and physiological concepts. Biol Rev 2003,
78:81-118. 54. Carleton KL, Spady T, Streelman JT, Kidd M, McFarland W,
Loew E: Visual sensitivities tuned by heterochronic shifts in
36. Kelber A, Osorio D: From spectral information to animal colour opsin gene expression. BMC Biol 2008, 6:22.
vision: experiments and concepts. Proc Biol Sci 2010,
277:1617-1625. 55. Hofmann C, Carleton KL: Gene duplication and differential gene
expression play an important role in the diversification of
37. Van-Eyk SM, Siebeck UE, Champ CM, Marshall NJ, Hart NS: visual pigments in fish. Integr Comp Biol 2009, 49:630-643.
Behavioural evidence for colour vision in an elasmobranch. J
56. Nakamura Y, Mori K, Saitoh K, Oshima K, Mekuchi M, Sugaya T,
Exp Biol 2011, 214:4186-4192.
Shigenobu Y, Ojima N, Muta S, Fujiwara A et al.: Evolutionary
38. Siebeck UE, Wallis GM, Litherland L: Colour vision in coral reef changes of multiple visual pigment genes in the complete
fish. J Exp Biol 2008, 211:354-360. genome of Pacific bluefin tuna. Proc Nat Acad Sci USA 2013,
110:11061-11066.
39. Siebeck UE, Losey GS, Marshall NJ: UV communication in Fish.
Here the tuna genome has been sequenced to show that opsin genes
In Communication in Fishes, Vol 2. Edited by Laddich F, Collin SP,
duplicate in tandem and also undergo gene conversion.
Moller P, Kapoor BG. Science Publications Inc.; 2006:423-455.
57. Cortesi F, Musilova´ Z, Stieb S, Hart NS, Siebeck UE,
40. Hofmann CM, Marshall NJ, Abdilleh K, Patel Z, Siebeck UE,
Malmstrøm M, Tørresen OK, Jentoft S, Cheney KL, Marshall NJ,
Carleton KL: Opsin evolution in Damselfish: convergence,
Carleton KL, Salzburger W: Ancestral duplications and highly
reversal, and parallel evolution across tuning sites. J Mol Evol
dynamic opsin gene evolution in percomorph fishes. PNAS
2012, 75:79-91.
2015, 112:1493-1498.
A comprehensive survey of 100 fish species that documents the evolu-
41. Siebeck UE, Marshall NJ: Ocular media transmission of coral
tionary history of the SWS2 gene. A new gene duplication is identified
reef fish — can coral reef fish see ultraviolet light? Vis Res
along with, in some groups, losses and conversions in this violet/blue
2001, 41:133-149.
sensitive opsin class, coinciding with radiation of the highly diverse
percomorphs. One species, Pseudochromis fuscus, is used to exemplify
42. Losey GS, Cronin TW, Goldsmith T, Hyde D, Marshall NJ,
how gene differences occur within one species ontogenetically.
McFarland WN: The UV visual world of fishes: a review. J Fish
Biol 1999, 54:921-943.
58. Neafsey DE, Hartl DL: Convergent loss of an anciently
duplicated, functionally divergent RH2 opsin gene in the fugu
43. Cheney KL, Grutter AS, Blomberg SP, Marshall NJ: Blue and
and Tetraodon pufferfish lineages. Gene 2005, 350:161-171.
yellow signal cleaning behavior in coral reef fishes. Curr Biol
2009, 19:1283-1287.
59. Dalton BE, Loew ER, Cronin TW, Carleton KL: Spectral tuning by
opsin coexpression in retinal regions that view different parts
44. Detto T: The fiddler crab Uca mjoebergi uses colour vision in
of the visual field. Proc Biol Soc 2014, 281:1797.
mate choice. Proc Biol Sci 2007, 274:2785-2790.
60. Shand J, Davies W, Thomas N, Balmer L, Cowing J, Pointer M: The
45. Baldwin J, Johnsen S: The importance of color in mate choice
influence of ontogeny and light environment on the expression
of the blue crab Callinectes sapidus. J Exp Biol 2009,
212:3762-3768. of visual pigment opsins in the retina of the black bream
Acanthopagrus butcheri. J Exp Biol 2008, 211:1495-1503.
46. Baldwin J, Johnsen S: The male blue crab, Callinectes sapidus,
61. Temple SE: Why different regions of the retina have different
uses both chromatic and achromatic cues during mate
spectral sensitivities: a review of mechanisms and functional
choice. J Exp Biol 2012, 215:1184-1191.
significance of intraretinal variability in spectral sensitivity in
47. Rajkumar P, Rollmann SM, Cook TA, Layne JE: Molecular vertebrates. Vis Neurosci 2011, 28:281-293.
evidence for color discrimination in the Atlantic sand fiddler
62. Fritsches KA, Marshall NJ, Warrant EJ: Retinal specializations in
crab, Uca pugilator. J Exp Biol 2010, 213:4240-4248.
the blue marlin: eyes designed for sensitivity to low light levels.
48. Marshall NJ, Jones J, Cronin TW: Behavioural evidence for Mar Freshwater Res 2003, 54:333-341.
colour vision in stomatopod crustaceans. J Comp Physiol A
63. Halstenberg S, Lindgren K, Samagh S, Nadal-Vicens M, Balt S,
1996, 179:473-481.
Fernald R: Diurnal rhythm of cone opsin expression in the teleost
49. Caldwell RL, Dingle H: Stomatopods. Sci Am 1976, 234:80-89. fish Haplochromis burtoni. Vis Neurosci 2005, 22:135-141.
50. Marshall NJ, Arikawa K: Unconventional colour vision. Curr Biol 64. Johnson AM, Stanis S, Fuller RC: Diurnal lighting patterns and
2014, 24:R1150. habitat alter opsin expression and colour preferences in a
Unconventional colour vision is explored and defined. It is suggested that killifish. Proc R Soc Lond B 2013:280.
multiple colour channels, including up to nine in butterflies and 12 in This paper shows opsin expression varying on a diurnal basis, following
stomatopods are not attempts at increasing colour space dimensionality. to some extent lighting levels. While this example is in freshwater fish,
In the butterflies, spectral channels are added to conduct specific colour this is likely to occur in the marine environment also, reflecting changes
tasks or wavelength specific behaviours. Segregation of the retina also in light over the 24 h period. Such changes as with [63] are quantitative
contributes to spectral sensitivity multiplication, with different photore- amplification of expression within one opsin type rather appearance or
ceptor combinations examining different regions of visual space. This is disappearance of different types.
www.sciencedirect.com Current Opinion in Neurobiology 2015, 34:86–94
94 Molecular biology of sensation
65. Cronin TW, Caldwell RL, Marshall NJ: Sensory adaptation — the potentially new fluorescing compounds that it identifies. It does point
tunable colour vision in a mantis shrimp. Nature 2001, out in passing that the yellow filters found in the ocular media of several
411:547-548. fish, including many wrasse, may help enhance the fluorescent signal.
66. Marshall NJ: The visual ecology of reef fish colours. In Animal 71. Gerlach T, Sprenge D, Michiels NK: Fairy wrasses perceive and
Signals: Signalling and Signal Design in Animal Communication. respond to their deep red fluorescent coloration. Proc R Soc
Edited by Espmark Y, Amundsen T, Rosenqvist G. Tapir Press; Lond B 2014, 281:20140787.
2000:83-120. Part of an extended effort by Michiels and colleagues to show that
fluorescence is used in visual behaviour in fish. Mate choice tests
67. Marshall NJ: Conspicuousness and camouflage with the same
demonstrate that fish including the fluorescent component of their col-
‘bright’ colours. Colours for concealment and camouflage in
ours are favoured over those that have it removed by selective lighting.
reef fish. Philos Trans R Soc Lond B 2000, 355:1243-1248.
However behavioural arena lighting conditions are not natural and fail to
differentiate the added component of the fluorescence that forms part of
68. Mazel C, Cronin TW, Caldwell RL, Marshall NJ: Fluorescent
an underlying and otherwise obvious colour pattern.
enhancement of signaling in a mantis shrimp. Science 2004,
303:51.
72. Kemp DJ, Herberstein ME, Fleishman LJ, Endler JA, Bennett ATD,
Dyer AG, Hart NS, Marshall NJ, Whiting MJ: An integrative
69. Michiels N, Anthes N, Hart NS, Herler J, Meixner A,
framework for the appraisal of coloration in nature. Am Nat
Schleifenbaum F, Schulte G, Siebeck UE, Sprenger D,
2015. (in press).
Wucherer M: Red fluorescence in reef fish: a novel signalling
This review or synopsis examines current methods and approaches in
mechanism? BMC Ecol 2008, 8:16.
colour communication and colour vision in animals. It provides guidance
70. Sparks JS, Schelly RC, Smith WL, Davis MP, Tchernov D: The in methods without being prescriptive and identifies two different views;
covert world of fish biofluorescence: a phylogenetically first is the ‘top-down’ evolutionary/behavioural ecology school and sec-
widespread and phenotypically variable phenomenon. PLoS ond the more mechanistic ‘bottom-up’ neurophysiological/colour quan-
ONE 2014, 9:e83259. tification school. Between these sit colour vision models which, as the
This extensive survey of fish fluorescence using high-intensity excitation article explains, are being misused due to a lack of communication
sources notes over 180 species of fish that fluoresce. Whether this between the two schools. Ways to remedy this and form a more unified,
fluorescence is also visually relevant to the fish themselves under ambient and to some extent standardised, approach to understanding aspects of
illumination is not demonstrated and this work may be more interesting for colour vision are suggested.
Current Opinion in Neurobiology 2015, 34:86–94 www.sciencedirect.com