Comparative study of spectral sensitivity, irradiance sensitivity, spatial resolution and temporal resolution in the visual systems of Ocypode quadrata and Aratus pisonii.

Early pioneering studies by Autrum on terrestrial arthropods first revealed that the visual systems of arthropods reflected their lifestyles and habitats. Subsequent studies have examined and confirmed Autrum's hypothesis that visual adaptions are driven by predator-prey interactions and activity cycles, with rapidly moving predatory diurnal species generally possessing better temporal resolution than slower moving nocturnal species. However, few studies have compared the vision between diurnal herbivores and nocturnal predators. In this study, the visual physiology of a nocturnal fast-moving predatory crab, the Atlantic ghost crab (Ocypode quadrata) and a diurnal herbivorous crab, the mangrove tree crab (Aratus pisonii), was examined. Spectral sensitivity, irradiance sensitivity and temporal resolution of the crabs were quantified using the electroretinogram (ERG), while the spatial resolution was calculated utilizing morphological methods. Both O. quadrata and A. pisonii had a single dark-adapted spectral sensitivity peak (494 and 499 nm, respectively) and chromatic adaptation had no effect on their spectral sensitivity, indicating that both species have monochromatic visual systems. The temporal resolution of O. quadrata was not significantly different from that of A. pisonii, but O. quadrata did possess a significantly greater spatial resolution and irradiance sensitivity. Both species possess an acute zone in the anterior region of their eyes. The data presented in this study will aid in the current understanding of the correlation between visual physiology and the life history of the animal.

Measured and predicted acute toxicity of phenanthrene and MC252 crude oil to vertically migrating deep-sea crustaceans.

Deep-water column micronekton play a key role in oceanic food webs and represent an important trophic link between deep- and shallow-water ecosystems. Thus, the potential impacts of sub-surface hydrocarbon plumes on these organisms are critical to developing a more complete understanding of ocean-wide effects resulting from deep-sea oil spills. This work was designed to advance the understanding of hydrocarbon toxicity in several ecologically important deep-sea micronekton species using controlled laboratory exposures aimed at determining lethal threshold exposure levels. The current study confirmed the results previously determined for five deep-sea micronekton by measuring lethal threshold levels for phenanthrene between 81.2 and 277.5 µg/L. These results were used to calibrate the target lipid model and to calculate a critical target lipid body burden for each species. In addition, an oil solubility model was used to predict the acute toxicity of MC252 crude oil to vertically migrating crustaceans, Janicella spinacauda and Euphausiidae spp., and to compare the predictions with results of a 48-h constant exposure toxicity test with passive-dosing. Results confirmed that the tested deep-sea micronekton appear more sensitive than many other organisms when exposed to dissolved oil, but baseline stress complicated interpretation of results.

Author Correction: Light organ photosensitivity in deep-sea shrimp may suggest a novel role in counterillumination.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Light organ photosensitivity in deep-sea shrimp may suggest a novel role in counterillumination.

Extraocular photoreception, the ability to detect and respond to light outside of the eye, has not been previously described in deep-sea invertebrates. Here, we investigate photosensitivity in the bioluminescent light organs (photophores) of deep-sea shrimp, an autogenic system in which the organism possesses the substrates and enzymes to produce light. Through the integration of transcriptomics, in situ hybridization and immunohistochemistry we find evidence for the expression of opsins and phototransduction genes known to play a role in light detection in most animals. Subsequent shipboard light exposure experiments showed ultrastructural changes in the photophore similar to those seen in crustacean eyes, providing further evidence that photophores are light sensitive. In many deep-sea species, it has long been documented that photophores emit light to aid in counterillumination - a dynamic form of camouflage that requires adjusting the organ's light intensity to "hide" their silhouettes from predators below. However, it remains a mystery how animals fine-tune their photophore luminescence to match the intensity of downwelling light. Photophore photosensitivity allows us to reconsider the organ's role in counterillumination - not only in light emission but also light detection and regulation.

Ontogenetic adaptations in the visual systems of deep-sea crustaceans.

For all visually competent organisms, the driving force behind the adaptation of photoreceptors involves obtaining the best balance of resolution to sensitivity in the prevailing light regime, as an increase in sensitivity often results in a decrease in resolution. A number of marine species have an additional problem to deal with, in that the juvenile stages live in relatively brightly lit shallow (100-200 m depth) waters, whereas the adult stages have daytime depths of more than 600 m, where little downwelling light remains. Here, I present the results of electrophysiological analyses of the temporal resolution and irradiance sensitivity of juvenile and adult stages of two species of ontogenetically migrating crustaceans (Gnathophausia ingens and Systellaspis debilis) that must deal with dramatically different light environments and temperatures during their life histories. The results demonstrate that there are significant effects of temperature on temporal resolution, which help to optimize the visual systems of the two life-history stages for their respective light environments.This article is part of the themed issue 'Vision in dim light'.

Spectral sensitivity, spatial resolution and temporal resolution and their implications for conspecific signalling in cleaner shrimp.

Cleaner shrimp (Decapoda) regularly interact with conspecifics and client reef fish, both of which appear colourful and finely patterned to human observers. However, whether cleaner shrimp can perceive the colour patterns of conspecifics and clients is unknown, because cleaner shrimp visual capabilities are unstudied. We quantified spectral sensitivity and temporal resolution using electroretinography (ERG), and spatial resolution using both morphological (inter-ommatidial angle) and behavioural (optomotor) methods in three cleaner shrimp species: Lysmata amboinensis, Ancylomenes pedersoni and Urocaridella antonbruunii. In all three species, we found strong evidence for only a single spectral sensitivity peak of (mean ± s.e.m.) 518 ± 5, 518 ± 2 and 533 ± 3 nm, respectively. Temporal resolution in dark-adapted eyes was 39 ± 1.3, 36 ± 0.6 and 34 ± 1.3 Hz. Spatial resolution was 9.9 ± 0.3, 8.3 ± 0.1 and 11 ± 0.5 deg, respectively, which is low compared with other compound eyes of similar size. Assuming monochromacy, we present approximations of cleaner shrimp perception of both conspecifics and clients, and show that cleaner shrimp visual capabilities are sufficient to detect the outlines of large stimuli, but not to detect the colour patterns of conspecifics or clients, even over short distances. Thus, conspecific viewers have probably not played a role in the evolution of cleaner shrimp appearance; rather, further studies should investigate whether cleaner shrimp colour patterns have evolved to be viewed by client reef fish, many of which possess tri- and tetra-chromatic colour vision and relatively high spatial acuity.

Phylogenetic and transcriptomic analyses reveal the evolution of bioluminescence and light detection in marine deep-sea shrimps of the family Oplophoridae (Crustacea: Decapoda).

Bioluminescence is essential to the survival of many organisms, particularly in the deep sea where light is limited. Shrimp of the family Oplophoridae exhibit a remarkable mechanism of bioluminescence in the form of a secretion used for predatory defense. Three of the ten genera possess an additional mode of bioluminescence in the form of light-emitting organs called photophores. Phylogenetic analyses can be useful for tracing the evolution of bioluminescence, however, the few studies that have attempted to reconcile the relationships within Oplophoridae have generated trees with low-resolution. We present the most comprehensive phylogeny of Oplophoridae to date, with 90% genera coverage using seven genes (mitochondrial and nuclear) across 30 oplophorid species. We use our resulting topology to trace the evolution of bioluminescence within Oplophoridae. Previous studies have suggested that oplophorid visual systems may be tuned to differentiate the separate modes of bioluminescence. While all oplophorid shrimp possess a visual pigment sensitive to blue-green light, only those bearing photophores have an additional pigment sensitive to near-ultraviolet light. We attempt to characterize opsins, visual pigment proteins essential to light detection, in two photophore-bearing species (Systellaspis debilis and Oplophorus gracilirostris) and make inferences regarding their function and evolutionary significance.

A physiological analysis of color vision in batoid elasmobranchs.

The potential for color vision in elasmobranchs has been studied in detail; however, a high degree of variation exists among the group. Evidence for ultraviolet (UV) vision is lacking, despite the presence of UV vision in every other vertebrate class. An integrative physiological approach was used to investigate color and ultraviolet vision in cownose rays and yellow stingrays, two batoids that inhabit different spectral environments. Both species had peaks in UV, short, medium, and long wavelength spectral regions in dark-, light-, and chromatic-adapted electroretinograms. Although no UV cones were found with microspectrophotometric analysis, both rays had multiple cone visual pigments with λ max at 470 and 551 nm in cownose rays (Rhinoptera bonasus) and 475, 533, and 562 nm in yellow stingrays (Urobatis jamaicensis). The same analysis demonstrated that both species had rod λ max at 500 and 499 nm, respectively. The lens and cornea of cownose rays maximally transmitted wavelengths greater than 350 nm and greater than 376 nm in yellow stingrays. These results support the potential for color vision in these species and future investigations should reveal the extent to which color discrimination is significant in a behavioral context.

Comparative visual function in predatory fishes from the Indian River Lagoon.

Visual temporal resolution and spectral sensitivity of three coastal teleost species (common snook [Centropomus undecimalis], gray snapper [Lutjanus griseus], and pinfish [Lagodon rhomboides]) were investigated by electroretinogram. Temporal resolution was quantified under photopic and scotopic conditions using response waveform dynamics and maximum critical flicker fusion frequency (CFFmax). Photopic CFFmax was significantly higher than scotopic CFFmax in all species. The snapper had the shortest photoreceptor response latency time (26.7 ms) and the highest CFFmax (47 Hz), suggesting that its eyes are adapted for a brighter photic environment. In contrast, the snook had the longest response latency time (36.8 ms) and lowest CFFmax (40 Hz), indicating that its eyes are adapted for a dimmer environment or nocturnal lifestyle. Species spectral responses ranged from 360 to 620 nm and revealed the presence of rods sensitive to dim and twilight conditions, as well as multiple cone visual pigments providing the basis for color and contrast discrimination. Collectively, our results demonstrate differences in visual function among species inhabiting the Indian River Lagoon system, representative of their unique ecology and life histories.

Light and vision in the deep-sea benthos: I. Bioluminescence at 500-1000 m depth in the Bahamian islands.

Bioluminescence is common and well studied in mesopelagic species. However, the extent of bioluminescence in benthic sites of similar depths is far less studied, although the relatively large eyes of benthic fish, crustaceans and cephalopods at bathyal depths suggest the presence of significant biogenic light. Using the Johnson-Sea-Link submersible, we collected numerous species of cnidarians, echinoderms, crustaceans, cephalopods and sponges, as well as one annelid from three sites in the northern Bahamas (500-1000 m depth). Using mechanical and chemical stimulation, we tested the collected species for light emission, and photographed and measured the spectra of the emitted light. In addition, in situ intensified video and still photos were taken of different benthic habitats. Surprisingly, bioluminescence in benthic animals at these sites was far less common than in mesopelagic animals from similar depths, with less than 20% of the collected species emitting light. Bioluminescent taxa comprised two species of anemone (Actinaria), a new genus and species of flabellate Parazoanthidae (formerly Gerardia sp.) (Zoanthidea), three sea pens (Pennatulacea), three bamboo corals (Alcyonacea), the chrysogorgiid coral Chrysogorgia desbonni (Alcyonacea), the caridean shrimp Parapandalus sp. and Heterocarpus ensifer (Decapoda), two holothuroids (Elasipodida and Aspidochirota) and the ophiuroid Ophiochiton ternispinus (Ophiurida). Except for the ophiuroid and the two shrimp, which emitted blue light (peak wavelengths 470 and 455 nm), all the species produced greener light than that measured in most mesopelagic taxa, with the emissions of the pennatulaceans being strongly shifted towards longer wavelengths. In situ observations suggested that bioluminescence associated with these sites was due primarily to light emitted by bioluminescent planktonic species as they struck filter feeders that extended into the water column.

Light and vision in the deep-sea benthos: II. Vision in deep-sea crustaceans.

Using new collecting techniques with the Johnson-Sea-Link submersible, eight species of deep-sea benthic crustaceans were collected with intact visual systems. Their spectral sensitivities and temporal resolutions were determined shipboard using electroretinography. Useable spectral sensitivity data were obtained from seven species, and in the dark-adapted eyes, the spectral sensitivity peaks were in the blue region of the visible spectrum, ranging from 470 to 497 nm. Under blue chromatic adaptation, a secondary sensitivity peak in the UV portion of the spectrum appeared for two species of anomuran crabs: Eumunida picta (λ(max)363 nm) and Gastroptychus spinifer (λ(max)383 nm). Wavelength-specific differences in response waveforms under blue chromatic adaptation in these two species suggest that two populations of photoreceptor cells are present. Temporal resolution was determined in all eight species using the maximum critical flicker frequency (CFF(max)). The CFF(max) for the isopod Booralana tricarinata of 4 Hz proved to be the lowest ever measured using this technique, and suggests that this species is not able to track even slow-moving prey. Both the putative dual visual pigment system in the crabs and the extremely slow eye of the isopod may be adaptations for seeing bioluminescence in the benthic environment.

Temporal resolution and spectral sensitivity of the visual system of three coastal shark species from different light environments.

Visual temporal resolution and scotopic spectral sensitivity of three coastal shark species (bonnethead Sphyrna tiburo, scalloped hammerhead Sphyrna lewini, and blacknose shark Carcharhinus acronotus) were investigated by electroretinogram. Temporal resolution was quantified under photopic and scotopic conditions using response waveform dynamics and maximum critical flicker-fusion frequency (CFF). Photopic CFF(max) was significantly higher than scotopic CFF(max) in all species. The bonnethead had the shortest photoreceptor response latency time (23.5 ms) and the highest CFF(max) (31 Hz), suggesting that its eyes are adapted for a bright photic environment. In contrast, the blacknose had the longest response latency time (34.8 ms) and lowest CFF(max) (16 Hz), indicating its eyes are adapted for a dimmer environment or nocturnal lifestyle. Scotopic spectral sensitivity revealed maximum peaks (480 nm) in the bonnethead and blacknose sharks that correlated with environmental spectra measured during twilight, which is a biologically relevant period of heightened predation.

A novel vertebrate eye using both refractive and reflective optics.

Sunlight is attenuated rapidly in the ocean, resulting in little visually useful light reaching deeper than approximately 1000 m in even the clearest water. To maximize sensitivity to the relatively brighter downwelling sunlight, to view the silhouette of animals above them, and to increase the binocular overlap of their eyes, many mesopelagic animals have developed upward-pointing tubular eyes. However, these sacrifice the ability to detect bioluminescent and reflective objects in other directions. Thus, some mesopelagic fish with tubular eyes extend their visual fields laterally and/or ventrally by lensless ocular diverticula, which are thought to provide unfocused images, allowing only simple detection of objects, with little spatial resolution. Here, we show that a medial mirror within the ventrally facing ocular diverticulum of the spookfish, Dolichopteryx longipes, consisting of a multilayer stack derived from a retinal tapetum, is used to reflect light onto a lateral retina. The reflective plates are not orientated parallel to the surface of the mirror. Instead, plate angles change progressively around the mirror, and computer modeling indicates that this provides a well-focused image. This is the first report of an ocular image being formed in a vertebrate eye by a mirror.

Giant deep-sea protist produces bilaterian-like traces.

One of the strongest paleontological arguments in favor of the origin of bilaterally symmetrical animals (Bilateria) prior to their obvious and explosive appearance in the fossil record in the early Cambrian, 542 million years ago, is the occurrence of trace fossils shaped like elongated sinuous grooves or furrows in the Precambrian. Being restricted to the seafloor surface, these traces are relatively rare and of limited diversity, and they do not show any evidence of the use of hard appendages. They are commonly attributed to the activity of the early nonskeletonized bilaterians or, alternatively, large cnidarians such as sea anemones or sea pens. Here we describe macroscopic groove-like traces produced by a living giant protist and show that these traces bear a remarkable resemblance to the Precambrian trace fossils, including those as old as 1.8 billion years. This is the first evidence that organisms other than multicellular animals can produce such traces, and it prompts re-evaluation of the significance of Precambrian trace fossils as evidence of the early diversification of Bilateria. Our observations also render indirect support to the highly controversial interpretation of the enigmatic Ediacaran biota of the late Precambrian as giant protists.

Visual physiology of the Antarctic amphipod Abyssorchomene plebs.

Although the visual systems of animals living in the cold, dark water of the deep sea have been investigated for some time, little is known about vision in animals inhabiting polar oceans, where temperatures are even colder and irradiance fluctuates dramatically with ice cover and season. Physiology of the compound eye of the amphipod Abyssorchomene plebs (Gammaridea: Lysianassoidea), a common Antarctic benthic scavenger, was studied electrophysiologically by electroretinography. A. plebs has a monochromatic visual system with a spectral sensitivity maximum at 487 nm, and higher sensitivity at ultraviolet wavelengths than predicted by a visual pigment template. While irradiance sensitivity determined from V/log I curves is comparable to that of mesopelagic crustaceans, temporal resolution calculated from response waveform dynamics and as determined by critical flicker fusion frequency suggest that the A. plebs eye is slower than that of crustaceans from the deep sea. A. plebs photoreceptors are physiologically adapted for a slow lifestyle in a low-light environment, where maximizing photon capture occurs at the expense of detecting fast events in the visual scene.

Effects of Light Adaptation on the Temporal Resolution of Deep-sea Crustaceans.

The effects of light adaptation on flicker fusion frequency were examined in the photoreceptors of 13 species of deep-sea crustaceans. Light adaptation produced a significant increase in the maximum critical flicker fusion frequency (CFF(max)) in 7 species-all 6 species of euphausiids in the study, and 1 species of oplophorid (Group 1). This is the first example of an increase in temporal resolution due to light adaptation in a deep-sea species. In the other six species-2 oplophorids, 1 pandalid, 1 pasiphaeid, 1 penaeid and 1 sergestid (Group 2)-light adaptation had no effect, or resulted in a decrease in the flicker fusion frequency. The mean dark-adapted CFF(max) of the Group 1 species was significantly higher, and the mean response latency significantly lower, than those of the Group 2 species. Possible explanations for these differences include the activity and bioluminescence mode of preferred prey items, as well as the retention of larval/juvenile adaptations in adult eyes.

VARIABILITY IN FLASH CHARACTERISTICS OF A BIOLUMINESCENT COPEPOD.

Bioluminescence of the copepod, Pleuromamma xiphias, was investigated with an optical multichannel analyzer(OMA) to measure emission spectra, an integrating sphere-photon counting detector system to determine flash kinetics and quantum emission, and an ISIT video system to image spatial patterns of emission. Light emission was in the blue spectral region, with maximum emission at approximately 492 nm. Spectral waveforms were unimodal, or bimodal with the secondary peak at 472 nm. Flashes in response to a single stimulus consisted of two components: a fast component attaining maximum intensity in under 100 ms, and a slow element which peaked after 600 ms. The fast component originated from thoracic and abdominal light organs while the slow component represented a large expulsion of luminescent material from the abdominal organ only. Both components exhibited first order exponential decay although the decay rate of the fast component was approximately one order of magnitude greater. The typical flash response to a single stimulus exhibited a response latency of 30 ms, initial rise time of 87 ms, duration of 2.4 s, and quantum emission of 1.4 x 1010 photons flash-1. Quantum emission increased with increasing stimulus strength. Both response waveform and total quantum emission were affected by the frequency of electrical stimuli. Stimulation at 1 Hz generated the greatest luminescence, averaging 1.1 x 1011 photons response-1 for 11 s emissions. Higher rates of stimulation decreased total quantum emission and response episode duration, and resulted in greater temporal summation of the emission waveform. Variability in flash characteristics due to electrical stimulation suggests a versatility of luminescent displays in situ.