Ontogeny of Vision in Marine Crustaceans

Marine crustaceans present an extremely interesting set of examplesin which to examine visual development and metamorphosis. Larvaeof these animals are almost always planktonic, living in thelight field of open waters. The presence of a simple, predictablephotic environment, the relatively basic visual requirementsof larvae, and the need to remain transparent to reduce predationlead to the use of a single eye type throughout all marine crustaceanlarvae. Adult crustaceans, on the other hand, use a greaterdiversity of optical designs than all other animals combined,occupy habitats from the deep sea to mountaintops, and havevery complex visual systems and behaviors. Thus, visual developmentvaries tremendously among modern Crustacea. In this brief review,we consider the structure and development of marine crustaceaneyes, focusing on optics, retinal design, and metamorphosisof the visual pigments.     

Vision in the deep sea

The deep sea is the largest habitat on earth. Its three great faunal environments--the twilight mesopelagic zone, the dark bathypelagic zone and the vast flat expanses of the benthic habitat--are home to a rich fauna of vertebrates and invertebrates. In the mesopelagic zone (150-1000 m), the down-welling daylight creates an extended scene that becomes increasingly dimmer and bluer with depth. The available daylight also originates increasingly from vertically above, and bioluminescent point-source flashes, well contrasted against the dim background daylight, become increasingly visible. In the bathypelagic zone below 1000 m no daylight remains, and the scene becomes entirely dominated by point-like bioluminescence. This changing nature of visual scenes with depth--from extended source to point source--has had a profound effect on the designs of deep-sea eyes, both optically and neurally, a fact that until recently was not fully appreciated. Recent measurements of the sensitivity and spatial resolution of deep-sea eyes--particularly from the camera eyes of fishes and cephalopods and the compound eyes of crustaceans--reveal that ocular designs are well matched to the nature of the visual scene at any given depth. This match between eye design and visual scene is the subject of this review. The greatest variation in eye design is found in the mesopelagic zone, where dim down-welling daylight and bio-luminescent point sources may be visible simultaneously. Some mesopelagic eyes rely on spatial and temporal summation to increase sensitivity to a dim extended scene, while others sacrifice this sensitivity to localise pinpoints of bright bioluminescence. Yet other eyes have retinal regions separately specialised for each type of light. In the bathypelagic zone, eyes generally get smaller and therefore less sensitive to point sources with increasing depth. In fishes, this insensitivity, combined with surprisingly high spatial resolution, is very well adapted to the detection and localisation of point-source bioluminescence at ecologically meaningful distances. At all depths, the eyes of animals active on and over the nutrient-rich sea floor are generally larger than the eyes of pelagic species. In fishes, the retinal ganglion cells are also frequently arranged in a horizontal visual streak, an adaptation for viewing the wide flat horizon of the sea floor, and all animals living there. These and many other aspects of light and vision in the deep sea are reviewed in support of the following conclusion: it is not only the intensity of light at different depths, but also its distribution in space, which has been a major force in the evolution of deep-sea vision.     

Vision in the dimmest habitats on Earth

A very large proportion of the world's animal species are active in dim light, either under the cover of night or in the depths of the sea. The worlds they see can be dim and extended, with light reaching the eyes from all directions at once, or they can be composed of bright point sources, like the multitudes of stars seen in a clear night sky or the rare sparks of bioluminescence that are visible in the deep sea. The eye designs of nocturnal and deep-sea animals have evolved in response to these two very different types of habitats, being optimised for maximum sensitivity to extended scenes, or to point sources, or to both. After describing the many visual adaptations that have evolved across the animal kingdom for maximising sensitivity to extended and point-source scenes, I then use case studies from the recent literature to show how these adaptations have endowed nocturnal animals with excellent vision. Nocturnal animals can see colour and negotiate dimly illuminated obstacles during flight. They can also navigate using learned terrestrial landmarks, the constellations of stars or the dim pattern of polarised light formed around the moon. The conclusion from these studies is clear: nocturnal habitats are just as rich in visual details as diurnal habitats are, and nocturnal animals have evolved visual systems capable of exploiting them. The same is certainly true of deep-sea animals, as future research will no doubt reveal.     

LASER SAFETY THRESHOLDS FOR CETACEANS AND PINNIPEDS

An increase in the use of oceanographic lidar has raised concern over laser safety for marine mammals. We were able to address some of these concerns by combining information about current laser safety standards, retinal damage mechanisms for humans, and research on eye anatomy for humans, cetaceans, and pinnipeds. To estimate the irradiance at the retina, the image size at the retina and pupil diameter must be known. We estimate the smallest spot size using retinal resolution or visual acuity for six species of cetaceans and five species of pinnipeds. A sensitivity ratio was calculated for each species using the ratio of the irradiance at the retina of the marine mammal to the irradiance at the retina of humans. The sensitivity ratio was used to suggest exposure limits for the various species. Because the human eye is more sensitive than either the cetacean or pinniped eye, we conclude that laser energies that are eye-safe for humans will also be safe for marine mammals, and higher laser irradiances may be permissible if illumination of humans is avoided.     

Tuning of photoreceptor function in three mantis shrimp species that inhabit a range of depths. I. Visual pigments

Visual pigments in many animal species, including stomatopod crustaceans, are adapted to the photic environments inhabited by that species. However, some species occupy a diversity of environments as adults (such as a range of depths in the ocean), and a single set of visual pigments would not be equally adaptive for all habitats in which individuals live. We characterized the visual pigment complements of three species of stomatopod crustaceans, Haptosquilla trispinosa, Gonodactylellus affinis, and Gonodactylopsis spongicola, which are unusual for this group in that each lives at depths from the subtidal to several tens of meters. Using microspectrophotometry, we determined the visual pigments in all classes of main rhabdoms in individuals of each species from shallow or deep habitats. Each species expressed the typical diversity of visual pigments commonly found in stomatopods, but there was little or no evidence of differential expression of visual pigments in animals of any species collected from different depths. Vision in these species, therefore, is not tuned to spectral characteristics of the photic environment by varying the assemblages of visual pigments appearing in their retinas.     

Temporal resolution in mesopelagic crustaceans

Mesopelagic crustaceans occupy a dim-light environment that is similar to that of nocturnal insects. In a light-limited environment, the requirement for greater sensitivity may result in slower photoreceptor transduction and increased summation time. This should be reflected by a lower temporal resolution, as indicated by a lower critical flicker fusion frequency (CFF). Therefore, one would predict that the CFFs of mesopelagic organisms would be relatively low compared with those of their shallow-water relatives, just as nocturnal insects tend to have lower CFFs than diurnal insects. Using an electrophysiological apparatus that was adapted for shipboard use, the dark-adapted CFFs of a variety of species of mesopelagic crustaceans were determined using the electroretinogram. The parameter examined was the maximum CFF--the point at which further increases in irradiance no longer result in a faster flicker fusion frequency. The results summarized here indicate that there is a trend towards lower CFFs with increasing habitat depth, with some interesting exceptions.     

Long-wave sensitivity in deep-sea stomiid dragonfish with far-red bioluminescence: evidence for a dietary origin of the chlorophyll-derived retinal photosensitizer of Malacosteus niger

Both residual downwelling sunlight and bioluminescence, which are the two main sources of illumination available in the deep sea, have limited wavebands concentrated around 450-500 nm. Consequently, the wavelengths of maximum absorption (lambdamax) of the vast majority of deep-sea fish visual pigments also cluster in this part of the spectrum. Three genera of deep-sea loose-jawed dragonfish (Aristostomias, Pachystomias and Malacosteus), however, in addition to the blue bioluminescence typical of most deep-sea animals, also produce far-red light (maximum emission >700 nm) from suborbital photophores. All three genera are sensitive in this part of the spectrum, to which all other animals of the deep sea are blind, potentially affording them a private waveband for illuminating prey and for interspecific communication that is immune from detection by predators and prey. Aristostomias and Pachystomias enhance their long-wave visual sensitivity by the possession of at least three visual pigments that are long-wave shifted (lambdamax values ca. 515, 550 and 590 nm) compared with those of other deep-sea fishes. Malacosteus, on the other hand, although it does possess two of these red-shifted pigments (lambdamax values ca. 520 and 540 nm), lacks the most long-wave-sensitive pigments found in the other two genera. However, it further enhances its long-wave sensitivity with a chlorophyll-derived photosensitizer within its outer segments. The fluorescence emission and excitation spectra of this pigment are very similar to spectra obtained from mesopelagic copepods, which are an important component of diet of Malacosteus, suggesting a dietary origin for this pigment.     

Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon

In deep‐water animals, the visual sensory system is often challenged by the dim‐light environment. Here, we focus on the molecular mechanisms involved in rapid deep‐water adaptations. We examined visual system evolution in a small‐scale yet phenotypically and ecologically diverse adaptive radiation, the species flock of cichlid fishes in deep crater lake Barombi Mbo in Cameroon, West Africa. We show that rapid adaptations of the visual system to the novel deep‐water habitat primarily occurred at the level of gene expression changes rather than through nucleotide mutations, which is compatible with the young age of the radiation. Based on retinal bulk RNA sequencing of all eleven species, we found that the opsin gene expression pattern was substantially different for the deep‐water species. The nine shallow‐water species feature an opsin palette dominated by the red‐sensitive (LWS) opsin, whereas the two unrelated deep‐water species lack expression of LWS and the violet‐sensitive (SWS2B) opsin, thereby shifting the cone sensitivity to the centre of the light spectrum. Deep‐water species further predominantly express the green‐sensitive RH2Aα over RH2Aβ. We identified one amino acid substitution in the RH2Aα opsin specific to the deep‐water species. We finally performed a comparative gene expression analysis in retinal tissue of deep‐ vs. shallow‐water species. We thus identified 46 differentially expressed genes, many of which are associated with functions in vision, hypoxia management or circadian clock regulation, with some of them being associated with human eye diseases.     

Visual perception of light organ patterns in deep‐sea shrimps and implications for conspecific recognition

Darkness and low biomass make it challenging for animals to find and identify one another in the deep sea. While spatiotemporal variation in bioluminescence is thought to underlie mate recognition for some species, its role in conspecific recognition remains unclear. The deep‐sea shrimp genus, Sergestes sensu lato (s.l.), is one group that is characterized by species‐specific variation in light organ arrangement, providing us the opportunity to test whether organ variation permits recognition to the species level. To test this, we analyzed the visual capabilities of three species of Sergestes s.l. in order to (a) test for sexual dimorphism in eye‐to‐body size scaling relationships, (b) model the visual ranges (i.e., sighting distances) over which these shrimps can detect intraspecific bioluminescence, and (c) assess the maximum possible spatial resolution of the eyes of these shrimps to estimate their capacity to distinguish the light organs of each species. Our results showed that relative eye size scaled negatively with body length across species and without sexual dimorphism. Though the three species appear capable of detecting one another's bioluminescence over distances ranging from < 1 to ~6 m, their limited spatial resolution suggests they cannot resolve light organ variation for the purpose of conspecific recognition. Our findings point to factors other than conspecific recognition (e.g., neutral drift, phenotypic constraint) that have led to the extensive diversification of light organs in Sergestes s.l and impart caution about interpreting ecological significance of visual characters based on the resolution of human vision. This work provides new insight into deep‐sea animal interaction, supporting the idea that—at least for these mesopelagic shrimps—nonvisual signals may be required for conspecific recognition.     

Repeated eye reduction events reveal multiple pathways to degeneration in a family of marine snails

Eye reduction occurs in many troglobitic, fossorial, and deep‐sea animals but there is no clear consensus on its evolutionary mechanism. Given the highly conserved and pleiotropic nature of many genes instrumental to eye development, degeneration might be expected to follow consistent evolutionary trajectories in closely related animals. We tested this in a comparative study of ocular anatomy in solariellid snails from deep and shallow marine habitats using morphological, histological, and tomographic techniques, contextualized phylogenetically. Of 67 species studied, 15 lack retinal pigmentation and at least seven have eyes enveloped by surrounding epithelium. Independent instances of reduction follow numerous different morphological trajectories. We estimate eye loss has evolved at least seven times within Solariellidae, in at least three different ways: characters such as pigmentation loss, obstruction of eye aperture, and “lens” degeneration can occur in any order. In one instance, two morphologically distinct reduction pathways appear within a single genus, Bathymophila. Even amongst closely related animals living at similar depths and presumably with similar selective pressures, the processes leading to eye loss have more evolutionary plasticity than previously realized. Although there is selective pressure driving eye reduction, it is clearly not morphologically or developmentally constrained as has been suggested by previous studies.     

The long-term effectiveness of different regimens of occlusion on recovery from early monocular deprivation in kittens.

Although the behavioural effects of an early period of monocular deprivation imposed on kittens can be very severe, resembling an extreme form of the human clinical condition deprivation amblyopia, they are not necessarily irreversible. Considerable behavioural as well as physiological recovery can occur if normal visual input is restored to the deprived eye sufficiently early, particularly if the other (initially non-deprived) eye is occluded at the same time (reverse occlusion). However, past work has shown that in many situations the improvement in the vision of the initially deprived eye that occurs during reverse occlusion is not retained following the subsequent introduction of binocular visual input. Furthermore, the vision of the other eye is often reduced as well, with the result that the eventual outcome is a condition of bilateral amblyopia. This study first examines the consequences of several periods of reverse occlusion whose onset and duration would be thought to maximize the opportunity for good and long-standing recovery of vision in the initially deprived eye. However, only in a very restricted set of exposure conditions did animals acquire good vision in one or both eyes; in most situations the final outcome was one of bilateral amblyopia. A second set of experiments examined the consequences of various regimens of part-time reverse occlusion, where the initially non-deprived eye was occluded for only part of each day to allow a period of binocular visual exposure, on kittens that had been monocularly deprived until 6, 8, 10 or 12 weeks of age. Whereas short or long daily periods of occlusion of the initially non-deprived eye resulted eventually in amblyopia in one, or usually both, eyes, certain intermediate occlusion times (3.5 or 5 h each day) resulted in recovery of normal acuities, contrast sensitivity and vernier acuity in both eyes, in animals that had been monocularly deprived until 6, 8 or 10 weeks of age, but not in animals deprived for longer periods. Experiments were done to establish some of the factors that contributed to the successful outcome associated with certain of the regimens of part-time reverse occlusion. It was established that recovery was just as good in animals in which the visual axes were vertically misaligned by means of prisms during the daily period of binocular visual exposure, thereby indicating that the visual input to the two eyes need not be concordant. However, animals that received equivalent visual exposure of the two eyes each day, but successively rather than simultaneously, all developed very severe bilateral amblyopia.(ABSTRACT TRUNCATED AT 400 WORDS)     

Evidence for Permo-Triassic colonization of the deep sea by isopods

The deep sea is one of the largest ecosystems on Earth and is home to a highly diverse fauna, with polychaetes, molluscs and peracarid crustaceans as dominant groups. A number of studies have proposed that this fauna did not survive the anoxic events that occurred during the Mesozoic Era. Accordingly, the modern fauna is thought to be relatively young, perhaps having colonized the deep sea after the Eocene/Oligocene boundary. To test this hypothesis, we performed phylogenetic analyses of nuclear ribosomal 18S and 28S and mitochondrial cytochrome oxidase I and 16S sequences from isopod crustaceans. Using a molecular clock calibrated with multiple isopod fossils, we estimated the timing of deep-sea colonization events by isopods. Our results show that some groups have an ancient origin in the deep sea, with the earliest estimated dates spanning 232–314 Myr ago. Therefore, anoxic events at the Permian–Triassic boundary and during the Mesozoic did not cause the extinction of all the deep-sea fauna; some species may have gone extinct while others survived and proliferated. The monophyly of the ‘munnopsid radiation’ within the isopods suggests that the ancestors of this group evolved in the deep sea and did not move to shallow-water refugia during anoxic events.     

Spectral tuning and the visual ecology of mantis shrimps

The compound eyes of mantis shrimps (stomatopod crustaceans) include an unparalleled diversity of visual pigments and spectral receptor classes in retinas of each species. We compared the visual pigment and spectral receptor classes of 12 species of gonodactyloid stomatopods from a variety of photic environments, from intertidal to deep water (> 50 m), to learn how spectral tuning in the different photoreceptor types is modified within different photic environments. Results show that receptors of the peripheral photoreceptors, those outside the midband which are responsible for standard visual tasks such as spatial vision and motion detection, reveal the well-known pattern of decreasing lambdamax with increasing depth. Receptors of midband rows 5 and 6, which are specialized for polarization vision, are similar in all species, having visual lambdamax-values near 500nm, independent of depth. Finally, the spectral receptors of midband rows 1 to 4 are tuned for maximum coverage of the spectrum of irradiance available in the habitat of each species. The quality of the visual worlds experienced by each species we studied must vary considerably, but all appear to exploit the full capabilities offered by their complex visual systems.     

Optical parameters of the eyes of some benthic decapods as a function of habitat depth (Crustacea,Decapoda)

Summary Eye diameter relative to body length, and interommatidial angle, rhabdom length and rhabdom width as a function of eye size, were determined for specimens of 19 benthic macruran decapod species in 8 genera and 5 families, spanning a wide range of habitat depths. For these species, eye diameter relative to body length tends to increase with adult habitat. In addition, rate of eye growth relative to body growth increases with habitat depth, a trend opposite to that of pelagic crustaceans previously investigated. Interommatidial angle decreases with increasing eye diameter, and therefore with depth for an individual of a particular size. Rhabdom length and width tend to increase with eye diameter. Visual sensitivity may increase with depth among these species as a result of both larger eyes and the associated increase in rhabdom dimensions. Differences in energetic limitations and visual environments might produce the difference in trends of eye size relative to body size between benthic and pelagic crustaceans.     

Adaptation of Arctic and Antarctic ice metazoa to their habitat

Sea ice is a unique habitat in polar seas. A diverse assemblage of plants and animals lives in its interior parts and at the ice-water interface. Their distribution is to a large extent controlled by abiotic parameters such as light, salinity and space, as well as food availability. In both the Arctic and Antarctic, the highest metazoan concentrations occur mostly in the bottom centimetres of the sea ice. Dominant metazoans are nematodes, turbellarians, rotifers and crustaceans. The ice-water interface itself houses in addition to endemic amphipods migrants from both the ice and the pelagic realm. To survive with the environmental conditions of the sea ice habitat, the ice biota is adapted, specifically to seasonal salinity variations from below 5 to above 60 PSU. Sea ice metazoans feed mainly on the algae growing within the sea ice. The loss of habitat during ice melt periods can lead to substantial sedimentation of ice fauna to the sea floor, where it might act as food source for the benthos.     

Tuning of photoreceptor function in three mantis shrimp species that inhabit a range of depths. II. Filter pigments

Within single species of stomatopod crustaceans, visual pigment classes of homologous photoreceptors throughout the retina are identical in all individuals and do not vary with the spectral characteristics of local habitats. We examined whether spectral sensitivities of stomatopod photoreceptors are differentially tuned through variations in the filter pigments associated with particular receptor classes. All classes of intrarhabdomal filters were characterized using microspectrophotometry in retinas of three stomatopod species, Haptosquilla trispinosa, Gonodactylellus affinis, and Gonodactylopsis spongicola, comparing individuals of each species collected from shallow or deep water. Depending on the depth of collection, filters varied among individuals both in optical density and in spectral shape, and the variation that was observed was similar in all three species. The changes in filter density and spectrum increased absolute sensitivity in retinas of animals living at greater depths, and tuned their long-wavelength photoreceptors for improved function in the bluer light available in deep water. Plasticity in retinal spectral function may be common in mantis shrimp species that occupy a range of habitat depths.     

Propagation and perception of bioluminescence: factors affecting counterillumination as a cryptic strategy

Many deep-sea species, particularly crustaceans, cephalopods, and fish, use photophores to illuminate their ventral surfaces and thus disguise their silhouettes from predators viewing them from below. This strategy has several potential limitations, two of which are examined here. First, a predator with acute vision may be able to detect the individual photophores on the ventral surface. Second, a predator may be able to detect any mismatch between the spectrum of the bioluminescence and that of the background light. The first limitation was examined by modeling the perceived images of the counterillumination of the squid Abralia veranyi and the myctophid fish Ceratoscopelus maderensis as a function of the distance and visual acuity of the viewer. The second limitation was addressed by measuring downwelling irradiance under moonlight and starlight and then modeling underwater spectra. Four water types were examined: coastal water at a depth of 5 m and oceanic water at 5, 210, and 800 m. The appearance of the counterillumination was more affected by the visual acuity of the viewer than by the clarity of the water, even at relatively large distances. Species with high visual acuity (0.11 degrees resolution) were able to distinguish the individual photophores of some counterilluminating signals at distances of several meters, thus breaking the camouflage. Depth and the presence or absence of moonlight strongly affected the spectrum of the background light, particularly near the surface. The increased variability near the surface was partially offset by the higher contrast attenuation at shallow depths, which reduced the sighting distance of mismatches. This research has implications for the study of spatial resolution, contrast sensitivity, and color discrimination in deep-sea visual systems.     

The spectral sensitivity of eye movements in response to light flashes inDaphnia magna

Summary The crustaceanDaphnia magna responds to a flash of light with a ventral rotation of its compound eye; this behavior is termed eye flick. We determined the spectral sensitivity for the threshold of eye flick in response to light flashes having three different spatial characteristics: (1) full-field, extending 180° from dorsal to ventral in the animal's field of view; (2) dorsal, 30° wide and located in the dorsal region of the visual field; (3) ventral, same as dorsal but located ventrally. All three stimuli extended 30° to the right and to the left of the animal's midplane. We found that spectral sensitivity varies with the spatial characteristics of the stimulus. For full-field illumination, the relative sensitivity was maximal at 527 nm and between 365 nm and 400 nm, with a significant local minimum at 420 nm. For the dorsal stimulus, the relative sensitivity was greatest at 400 nm, but also showed local maxima at 440 nm and 517 nm. For the ventral stimulus, the relative sensitivity maxima occurred at the same wavelengths as those for the full-field stimulus. At wavelengths of 570 nm and longer, the responses to both dorsal and ventral stimuli showed lower relative sensitivity than the full-field stimulus. No circadian or other periodic changes in threshold spectral sensitivity were observed under our experimental conditions. Animals which had their nauplius eyes removed by means of laser microsurgery had the same spectral sensitivity to full-field illumination as normal animals. Our results are discussed in terms of our current knowledge of the spectral classes of photoreceptors found in theDaphnia compound eye.     

Binocular visual integration in the crustacean nervous system

Although the behavioral repertoire of crustaceans is largely guided by visual information their visual nervous system has been little explored. In search for central mechanisms of visual integration, this study was aimed at identifying and characterizing brain neurons in the crab involved in binocular visual processing. The study was performed in the intact animal, by recording intracellularly the response to visual stimuli of neurons from one of the two optic lobes. Identified neurons recorded from the medulla (second optic neuropil), which include sustaining neurons, dimming neurons, depolarizing and hyperpolarizing tonic neurons and on-off neurons, all presented exclusively monocular (ipsilateral) responses. In contrast, all wide field movement detector neurons recorded from the lobula (third optic neuropil) responded to moving stimuli presented to the ipsilateral and to the contralateral eye. In these cells, the responses evoked by ipsilateral or contralateral stimulation were almost identical, as revealed by analysing the number and amplitude of the elicited postsynaptic potentials and spikes, and the ability to habituate upon repeated visual stimulation. The results demonstrate that in crustaceans important binocular processing takes place at the level of the lobula.