Colours and colour vision in reef fishes: Past, present and future research directions

Abstract

Many fishes, both freshwater or marine, have colour vision that may outperform humans. As a result, to understand the behavioural tasks that vision enables; including mate choice, feeding, agonistic behaviour and camouflage, we need to see the world through a fish's eye. This includes quantifying the variable light environment underwater and its various influences on vision. As well as rapid loss of light with depth, light attenuation underwater limits visual interaction to metres at most and in many instances, less than a metre. We also need to characterize visual sensitivities, fish colours and behaviours relative to both these factors. An increasingly large set of techniques over the past few years, including improved photography, submersible spectrophotometers and genetic sequencing, have taken us from intelligent guesswork to something closer to sensible hypotheses. This contribution to the special edition on the Ecology of Fish Senses under a shifting environment first reviews our knowledge of fish colour vision and visual ecology, past, present and very recent, and then goes on to examine how climate change may impinge on fish visual capability. The review is limited to mostly colour vision and to mostly reef fishes. This ignores a large body of work, both from other marine environments and freshwater systems, but the reef contains examples of many of the challenges to vision from the aquatic environment. It is also a concentrate of life, perhaps the most specious and complex on earth, suffering now catastrophically from the consequences of our lack of action on climate change. A clear course of action to prevent destruction of this habitat is the need to spend more time in it, in the study of it and sharing it with those not fortunate enough to see coral reefs first‐hand. Sir David Attenborough on The Great Barrier Reef: “Do we really care so little about the Earth upon which we live that we don't wish to protect one of its greatest wonders from the consequences of our behaviours?”

Cardinalfishes (Apogonidae) show visual system adaptations typical of nocturnally and diurnally active fish

“…This data also supports anatomical studies, which found high rod‐to‐cone ratios in the retinas of several members of this family (Fishelson et al, ). However, we also found a high diversity in cone opsin expression between species, which ranged in expression from two to six cone opsin genes, similar in number to diurnal reef fishes (reviewed in Marshall et al, and Losey et al, for MSP data).…”

“…They all live in the same water type (Jerlov, ) over a similar depth range and feed against and in many cases on similarly coloured objects (e.g., coral, algae, turf‐algae or sand‐substrate). The variation seen in spectral sensitivity must be explained by other factors (Marshall et al, ), including environmental or behavioural ones. Finer‐scale habitat choice (i.e.…”

“…The diversity of spectral sensitivities among coral reef fish, living in one of the most colourful ecosystems on earth, is yet to be explained and probably has no simple answer (for review see Marshall, Cortesi, de Busserolles, Siebeck, & Cheney, ). Part of this diversity is known to be facilitated by differential opsin gene expression and amino acid substitutions at opsin gene tuning sites, e.g., in damselfishes (Pomacentridae) (Hofmann et al, ; Stieb, Carleton, Cortesi, Marshall, & Salzburger, ; Stieb et al, ), wrasses (Labridae) (Phillips, Carleton, & Marshall, ), and dottybacks (Pseudochromidae) (Cortesi, Feeney, et al, ; Cortesi et al, ).…”

Microhabitat partitioning correlates with opsin gene expression in coral reef cardinalfishes (Apogonidae)

“…Consequently, competition for shelter may drive microhabitat partitioning in this family, with those forced into the open needing to develop other means of protection. Indeed, several species generally found in microhabitats away from structure (microhabitat A and B), such as R. gracilis , Z. viridiventer , T. zosterophora or Z. leptacantha , are of silvery‐translucent or pale appearance, providing excellent camouflage when viewed against a blue water background (Marshall, Cortesi, de Busserolles, Siebeck, & Cheney, ; Marshall & Johnsen, ). These species also form large schools, possibly further reducing predation risk (Pitcher, ).…”

Opsin gene evolution in amphibious and terrestrial combtooth blennies (Blenniidae)

“…All of the species appear to have red-shifted visual systems hinting towards the importance of 368 detecting longer-wavelengths of light for survival. Mounting evidence suggests that long-369 wavelength reception in coral reef fishes is especially beneficial when feeding on algae or 370 similar chlorophyll containing organic matter, which strongly reflect the red part of the light 371 spectrum (for a recent review on the topic see Marshall et al 2018). It is also possible that the 372 red-orange dorsal fin that appears unique to the terrestrial species (TJ Ord, unpublished data) 373 has evolved to exploit the pre-existing (ancestral) visual state of seeing red as a means of maximizing the efficiency of territorial and courtship signalling on land (Bhikajee and Green 375 2002, Shimizu et al 2006, Ord and Tonia Hsieh 2011.…”