Comparative Study of Temporal Resolution in the Visual Systems of Mesopelagic Crustaceans

The temporal characteristics of the visual systems of eight species of mesopelagic crustaceans were studied using the electroretinogram (ERG). Experiments were conducted on shipboard, using dark-captured specimens collected off the south coast of Cuba. As one would expect based on the relative intensity differences in their light environments, the deepest living species, Systellaspis debilis and Sergia filictum, have low maximum critical flicker fusion frequencies (CFFs) of 21-25 Hz, whereas the shallower living species Oplophorus gracilirostris and Janicella spinacauda have higher maximum CFFs (31-32 Hz). One of the shallowest living species, Funchalia villosa, has an unusually low maximum CFF (24 Hz), which may be a function of working with a dark-adapted eye. Two of the bilobed euphausiid species. Nematobrachion flexipes and N. sexspinosus, have very high maximum CFFs (44-57 Hz), comparable to those of surface-dwelling crabs, even though they live between 400 and 600 m. The maximum CFF of Stylocheiron maximum, a shallower living bilobed euphausiid, is only 36 Hz, indicating that maximum CFF among the euphausiids cannot be correlated with depth of occurrence. The unusually high flicker fusion frequency of the deeper living euphausiids may be correlated to their preference for bioluminescent prey

The Role of Inositol Phosphate Cascade in Visual Excitation of Invertebrate Microvillar Photoreceptors

The identity of the transmitter(s) involved in visual transduction in invertebrate microvillar photoreceptors remains unresolved. In this study, the role of inositol 1,4,5-trisphosphate (IP3) was examined in Limulus ventral photoreceptors by studying the effects on the light response of heparin and neomycin, agents that inhibit the production or action of IP3. Both heparin and neomycin reduce responses to brief flashes of light and the transient component of responses to steps of light, and also inhibit IP3-induced calcium release, indicating that IP3 plays a direct role in invertebrate visual excitation. The effects of BAPTA, a calcium buffer, were also examined and shown to be consistent with a role for IP3-mediated calcium release in visual excitation. However, all three agents fail to block the plateau component of the response to a step of light, indicating that a single pathway involving IP3 and calcium cannot solely be responsible for visual excitation in invertebrates. We suggest that the inositol phosphate cascade and a second parallel process that is not dependent on IP3 are involved in the production of the light response

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

Vision in the Hyperiid Amphipod Scina crassicornis

Light microscopy and extracellular electrophysiology were used to investigate eye structure and visual physiology of the hyperiid amphipod Scina crassicornis, a mesopelagic species that emits unusually short-wavelength luminescence (λmax=435-444 nm). The overall eye morphology is most similar to some previously described deep-dwelling amphipods, though not other hyperiids. Electroretinograms suggest that S. crassicornis possesses a relatively sensitive eye with slow temporal dynamics, and a monochromatic visual system (λmax=472 nm). Vision in S. crassicornis is well-suited for life in mesopelagic waters, and its short-wavelength luminescence does not play a role in intraspecific sexual signalling

A Short-Wavelength Photoreceptor Class in a Deep-Sea Shrimp

In the world of midwater, mesopelagic animals, downwelling sunlight is filtered by the overlying water to a limited waveband centered near 475 nm. Consequently, the visual pigments of most of these species absorb maximally between 450 and 500 nm. The only exceptions occur in some fishes, which have additional visual pigments absorbing at long wavelengths (550-580 nm) matched to their red bioluminescence. We now find that the mesopelagic decapod shrimp Systellaspis debilis has two visual pigments. One of these absorbs maximally in the expected range (λmax = 498 nm). but the other is maximally sensitive at very short wavelengths, approaching the near-ultraviolet (λmax = 410 nm). The discovery of a visual receptor class absorbing at such short wavelengths in a mesopelagic animal suggests that visual systems in the deep sea may be far more diverse, and potentially more complex, than previously suspected

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

Excitation of Limulus Photoreceptors by Hydrolysis-Resistant Analogs of cGMP and cAMP

cGMP was proposed to be the agent which directly opens the light-sensitive channel in Limulus ventral photoreceptors. However, the light-sensitive rhabdomeral-lobe (R-lobe) is not uniformly responsive to cGMP injection; that is, there are ‘hot spots’ of sensitivity. A potent phosphodiesterase which rapidly hydrolyses cGMP was suggested to explain the existence of these ‘hot spots’. To test this idea we injected ventral photoreceptors with hydrolysis-resistant cyclic nucleotide analogues. Whereas there can be a lack of a response to cGMP injection into the R-lobe, we find a reproducible depolarization upon R-lobe injection of hydrolysis-resistant cGMP analogues. Furthermore, the depolarization resulting from the injection of cGMP analogues does not require a rise in intracellular Ca2+, as it is not blocked by the Ca2+ buffer, BAPTA. Surprisingly, R-lobe injection of a hydrolysis-resistant cAMP analogue also depolarized ventral photoreceptors. Further work will be needed to resolve the role of cGMP in Limulus visual transduction

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 (λmax 363 nm) and Gastroptychus spinifer (λmax 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 (CFFmax). The CFFmax for the isopodBooralana 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

Correlation Between Photosensitivity and Downwelling Irradiance in Mesopelagic Crustaceans

The current study determined behavioral and electrophysiological photosensitivities for three species of mesopelagic crustaceans: Pasiphaea multidentata Esmark, 1866 (Decapoda: Pasiphaeidae), Sergestes arcticus Kröyer, 1855 (Decapoda: Sergestidae), and Meganyctiphanes norvegica M. Sars, 1857 (Euphausiacea: Euphausiidae). In addition, in situ quantifications of the species’ vertical distributions in relation to downwelling irradiances were also determined in two locations in the northwest Atlantic Ocean, Wilkinson Basin (WB) and Oceanographer Canyon (OC). Data are from six 2-week cruises between June and September from 1995 to 2001. P. multidentata and M. norvegica were the most abundant large crustaceans in WB, and S. arcticus and M. norvegica were the most abundant large crustaceans in OC. The behavioral light sensitivity thresholds of P. multidentata and M. norvegica from WB were both 107 photons cm−2 s−1 and those of S. arcticus and M. norvegica from OC were both 108 photons cm−2 s−1. Electrophysiologically, P. multidentata was significantly more sensitive than M. norvegica from either location, S. arcticus was significantly more sensitive than M. norvegica from OC, and M. norvegica from WB was significantly more sensitive than M. norvegica from OC. A correlation was found between electrophysiologically measured photosensitivity and downwelling irradiance, with the most sensitive species, P. multidentata and S. arcticus, associated with the lowest irradiance at daytime depths. The photosensitivities of M. norvegicacollected from the clearer waters of OC were significantly lower than those of individuals collected from the more turbid WB waters. These results indicate that downwelling irradiance has a significant impact on interspecies and intraspecies vertical distribution patterns in the mesopelagic realm