Multiple spectral channels in branchiopods. I. Vision in dim light and neural correlates.

Animals that have true color vision possess several spectral classes of photoreceptors. Pancrustaceans (Hexapoda+Crustacea) that integrate spectral information about their reconstructed visual world do so from photoreceptor terminals supplying their second optic neuropils, with subsequent participation of the third (lobula) and deeper centers (optic foci). Here, we describe experiments and correlative neural arrangements underlying convergent visual pathways in two species of branchiopod crustaceans that have to cope with a broad range of spectral ambience and illuminance in ephemeral pools, yet possess just two optic neuropils, the lamina and the optic tectum. Electroretinographic recordings and multimodel inference based on modeled spectral absorptance were used to identify the most likely number of spectral photoreceptor classes in their compound eyes. Recordings from the retina provide support for four color channels. Neuroanatomical observations resolve arrangements in their laminas that suggest signal summation at low light intensities, incorporating chromatic channels. Neuroanatomical observations demonstrate that spatial summation in the lamina of the two species are mediated by quite different mechanisms, both of which allow signals from several ommatidia to be pooled at single lamina monopolar cells. We propose that such summation provides sufficient signal for vision at intensities equivalent to those experienced by insects in terrestrial habitats under dim starlight. Our findings suggest that despite the absence of optic lobe neuropils necessary for spectral discrimination utilized by true color vision, four spectral photoreceptor classes have been maintained in Branchiopoda for vision at very low light intensities at variable ambient wavelengths that typify conditions in ephemeral freshwater habitats.

Multiple spectral channels in branchiopods. II. Role in light-dependent behavior and natural light environments.

Light is a primary environmental factor used by aquatic invertebrates for depth selection behavior. Many branchiopod crustaceans live in ephemeral aquatic habitats. All branchiopod crustaceans studied to date express four or more visual opsins in their compound eyes. We asked whether two branchiopods, Triops longicaudatus and Streptocephalus mackini, use multiple spectral channels to regulate their position in the water column. At the lowest intensities that elicited photonegative behavior, both species had broad spectral bandwidths, suggesting they use multiple spectral photoreceptor classes. Male S. mackini were more likely to maintain a vertical position 8.0-12.0 cm below the surface than females, independently of whether females were present. Male photopositive behavior at low intensity was restricted to a narrow bandwidth centered at 532 nm, suggesting a single photoreceptor class is used to maintain position above females. We compared ephemeral pools from two regions in Arizona and found that diffuse light attenuation coefficients were two orders of magnitude greater than the most heavily attenuating coastal waters. At less than 1 m of depth, pools were often dimmer than terrestrial habitats under starlight. Soil particle size distribution in each region affected spectral light environments, and behavioral responses of field-caught shrimp were adapted to the spectral properties of their region. The results suggest that branchiopods predominantly use luminance vision summed from multiple spectral photoreceptor classes for depth selection in dim, spectrally variable environments. The neuroanatomical basis for summation is described in a companion paper.

Using electroretinograms and multi-model inference to identify spectral classes of photoreceptors and relative opsin expression levels.

Understanding how individual photoreceptor cells factor in the spectral sensitivity of a visual system is essential to explain how they contribute to the visual ecology of the animal in question. Existing methods that model the absorption of visual pigments use templates which correspond closely to data from thin cross-sections of photoreceptor cells. However, few modeling approaches use a single framework to incorporate physical parameters of real photoreceptors, which can be fused, and can form vertical tiers. Akaike's information criterion (AICc) was used here to select absorptance models of multiple classes of photoreceptor cells that maximize information, given visual system spectral sensitivity data obtained using extracellular electroretinograms and structural parameters obtained by histological methods. This framework was first used to select among alternative hypotheses of photoreceptor number. It identified spectral classes from a range of dark-adapted visual systems which have between one and four spectral photoreceptor classes. These were the velvet worm, Principapillatus hitoyensis, the branchiopod water flea, Daphnia magna, normal humans, and humans with enhanced S-cone syndrome, a condition in which S-cone frequency is increased due to mutations in a transcription factor that controls photoreceptor expression. Data from the Asian swallowtail, Papilio xuthus, which has at least five main spectral photoreceptor classes in its compound eyes, were included to illustrate potential effects of model over-simplification on multi-model inference. The multi-model framework was then used with parameters of spectral photoreceptor classes and the structural photoreceptor array kept constant. The goal was to map relative opsin expression to visual pigment concentration. It identified relative opsin expression differences for two populations of the bluefin killifish, Lucania goodei. The modeling approach presented here will be useful in selecting the most likely alternative hypotheses of opsin-based spectral photoreceptor classes, using relative opsin expression and extracellular electroretinography.

Visual physiology underlying orientation and diel behavior in the sand beach amphipod Talorchestia longicornis.

Talitrid amphipods employ vision for zonal recovery behaviors on sand beaches and for entraining circadian activity rhythms. Using a hierarchy of methods, we examined visual spectral and response-intensity functions in Talorchestia longicornis, a species in which orientation and rhythm entrainment are wavelength-specific behaviors. Microspectrophotometry, electroretinogram recording and behavioral assays were used to determine visual pigments, retinal spectral sensitivity and whole-animal spectral responsivity, respectively. Diel changes in absolute sensitivity were also investigated at retinal and whole-animal levels. Two receptor spectral classes were identified, with values for visual pigment λ(max) of 427 and 518 nm. Retinal spectral sensitivity varied with electrode position along the distal-proximal axis. Chromatic adaptation of distal and proximal photoreceptors resulted in sensitivity peaks at 430 and 522 nm, respectively. In accordance with identified visual pigments and spectral sensitivity, T. longicornis photobehavioral responsivity covered a broad range (420-580 nm). Collectively, a dual-pigment visual system underlies wavelength-specific behavior in T. longicornis, with the short-wavelength pigment likely to be localized in the distal R5 retinular cell. While response-intensity functions did not change over the diel cycle at the retinal level, behavioral photoresponsiveness varied between day and night. At a wavelength used by T. longicornis for celestial orientation (420 nm), photobehavior was heightened at night, potentially aiding in nocturnal orientation. By contrast, at a wavelength used to entrain its circadian rhythm (520 nm) and for routine visual tasks, photobehavior was heightened during the day, and spectral sensitivity matched to the twilight spectrum, facilitating crepuscular vision and entrainment by irradiance at sunrise and sunset.