Ellis R. Loew

The underwater visual environment

What does the term ‘vision’ mean when applied to non-human animals, and how is the structure and function of a visual system adaptive for the animal that possesses it? These fundamental questions drive the visual ecologist and differentiate her or him from the photoecologist, who is interested in general sensitivity problems. How these questions are attacked will depend on the interests and expertise of the investigator, but ultimately all information regarding the properties of a particular visual system must be referred to the nature of the photic environment, the interactions of targets with the ambient light field, and the relevant visual tasks of the organism. Perhaps nowhere has this approach been more successfully applied than in studies defining the processes driving the evolution of visual systems in aquatic organisms. It follows that the visual ecologist must not only understand the biology, biophysics and perceptual qualities of vision, but must also have a basic understanding of optical physics and those properties of the medium that can influence the visible light field. We shall start with a discussion of basic optical quantities and hydrologic optics as they relate to vision, and then concentrate on three areas that are currently receiving particular attention by ‘fish’ visual ecologists: the near-ultraviolet light field, the polarized light field, and time-dependent changes in the light field produced by oceanic waves.

Visual sensitivities tuned by heterochronic shifts in opsin gene expression

BackgroundCichlid fishes have radiated into hundreds of species in the Great Lakes of Africa. Brightly colored males display on leks and vie to be chosen by females as mates. Strong discrimination by females causes differential male mating success, rapid evolution of male color patterns and, possibly, speciation. In addition to differences in color pattern, Lake Malawi cichlids also show some of the largest known shifts in visual sensitivity among closely related species. These shifts result from modulated expression of seven cone opsin genes. However, the mechanisms for this modulated expression are unknown.ResultsIn this work, we ask whether these differences might result from changes in developmental patterning of cone opsin genes. To test this, we compared the developmental pattern of cone opsin gene expression of the Nile tilapia, Oreochromis niloticus, with that of several cichlid species from Lake Malawi. In tilapia, quantitative polymerase chain reaction showed that opsin gene expression changes dynamically from a larval gene set through a juvenile set to a final adult set. In contrast, Lake Malawi species showed one of two developmental patterns. In some species, the expressed gene set changes slowly, either retaining the larval pattern or progressing only from larval to juvenile gene sets (neoteny). In the other species, the same genes are expressed in both larvae and adults but correspond to the tilapia adult genes (direct development).ConclusionDifferences in visual sensitivities among species of Lake Malawi cichlids arise through heterochronic shifts relative to the ontogenetic pattern of the tilapia outgroup. Heterochrony has previously been shown to be a powerful mechanism for change in morphological evolution. We found that altering developmental expression patterns is also an important mechanism for altering sensory systems. These resulting sensory shifts will have major impacts on visual communication and could help drive cichlid speciation.

The visual ecology of Puerto Rican anoline lizards: habitat light and spectral sensitivity

Abstract The visual ecology of six closely related species of Puerto Rican anoline lizards was investigated and they were found to occupy four distinct habitat types in terms of light conditions: “full shade”, “partial shade”, “no shade”, and “forest canopy.”The habitats differed substantially in total radiance and irradiance as well as in the shape of the irradiance spectrum. The shape of the radiance spectrum was similar in all of the habitats. We used electroretinogram (ERG) flicker photometry to measure spectral sensitivity and found the curves for all six species to be similar. The spectral sensitivity peaked in the range 550–560 nm, which matched the peak in spectral radiance for all of the habitats. The shape of the spectral-sensitivity curve was similar to those of a number of other terrestrial vertebrates. We suggest that the convergence of the shape of the photopic ERG-determined spectral-sensitivity curve in many terrestrial vertebrates may, in part, be due to the fact that the background radiance of many terrestrial habitats is dominated by the reflectance spectrum of green vegetation which peaks at 550 nm.

The photoreceptors and visual pigments of the garter snake (Thamnophis sirtalis): A microspectrophotometric, scanning electron microscopic and immunocytochemical study

Abstract Scanning electron microscopy, immunocytochemistry, and single cell microspectrophotometry were employed to characterize the photoreceptors and visual pigments in the retina of the garter snake, Thamnophis sirtalis. The photoreceptor population was found to be comprised entirely of cones, of which four distinct types were identified. About 45.5% of the photoreceptors are double cones consisting of a large principal member joined near the outer segment with a much smaller accessory member. About 40% of the photoreceptors are large single cones, and about 14.5% are small single cones forming two subtypes. The outer segments of the large single cones and both the principal and accessory members of the doubles contain the same visual pigment, one with peak absorbance near 554 nm. The small single cones contain either a visual pigment with peak absorbance near 482 nm or one with peak absorbance near 360 nm. Two classes of small single cones could be distinguished also by immunocytochemistry and scanning electron microscopy. The small single cones with the 360-nm pigment provide the garter snake with selective sensitivity to light in the near ultraviolet region of the spectrum. This ultraviolet sensitivity might be important in localization of pheromone trails.

Ultraviolet visual pigments in marine fishes of the family pomacentridae.

Near-UV visual pigments have been reported in single cones of several freshwater and euryhaline fishes. The presence of UV visual pigments in stenohaline marine fishes have, as yet, not been identified. In the pomacentridae near-UV visual pigments are present in single cones from the three species we examined--the tropical coral fishes Dascyllus trimaculatus and Pomacentrus coelestis, and the temperate Chromis punctipinnis. Maximum absorption of the UV pigments is centered around 360 nm. In juvenile Chromis, however, the UV visual pigment is not present. Instead there is a single cone containing a violet-sensitive pigment absorbing maximally around 420 nm. All three species are obligate diurnal planktivores. The UV sensitivity may function to enhance their ability to forage on zooplankton.

Visual pigments and oil droplets in genetically manipulated and carotenoid deprived quail : a microspectrophotometric study

The spectral absorbances of visual pigments and retinal oil droplets were studied in three groups of Japanese quail (Coturnix coturnix japonica): an unselected control population and two artificially selected strains that exhibited different early approach preferences between blue and red stimuli. The oil droplets were examined with and without prior carotenoid deprivation. Four cone pigments and five oil droplet types were identified, resembling those in other avian species. Carotenoid deprivation eliminated all pigmentation detectable in oil droplets by microspectrophotometry. Placement of chicks on normal diet gradually reintroduced normal pigmentation within the span of about a week. No statistically significant differences were found between normal and genetically selected birds in either visual pigments or oil droplet types, or in their relative proportions. It is concluded that differences in the early colour preferences of quail are unlikely to be a result of variation in the spectral properties of their photoreceptors.

AN ETHOGRAM OF BODY PATTERNING BEHAVIOR IN THE BIOMEDICALLY AND COMMERCIALLY VALUABLE SQUID LOLIGO PEALEI OFF CAPE COD, MASSACHUSETTS

Squids have a wide repertoire of body patterns; these patterns contain visual signals assembled from a highly diverse inventory of chromatic, postural, and locomotor components. The chromatic components reflect the activity of dermal chromatophore organs that, like the postural and locomotor muscles, are controlled directly from the central nervous system. Because a thorough knowledge of body patterns is fundamental to an understanding of squid behavior, we have compiled and described an ethogram (a catalog of body patterns and associated behaviors) for Loligo pealei. Observations of this species were made over a period of three years (> or = 440 h) and under a variety of behavioral circumstances. The natural behavior of the squid was filmed on spawning grounds off Cape Cod (northwestern Atlantic), and behavioral trials in the laboratory were run in large tanks. The body pattern components--34 chromatic (including 4 polarization components), 5 postural, and 12 locomotor--are each described in detail. Eleven of the most common body patterns are also described. Four of them are chronic, or long-lasting, patterns for crypsis; an example is Banded Bottom Sitting, which produces disruptive coloration against the substrate. The remaining seven patterns are acute; they are mostly used in intraspecific communication among spawning squids. Two of these acute patterns--Lateral Display and Mate Guarding Pattern--are used during agonistic bouts and mate guarding; they are visually bright and conspicuous, which may subject the squids to predation; but we hypothesize that schooling and diurnal activity may offset the disadvantage presented by increased visibility to predators. The rapid changeability and the diversity of body patterns used for crypsis and communication are discussed in the context of the behavioral ecology of this species.

Wave produced changes in underwater light and their relations to vision

SynopsisMaximal visual sensitivity of most vertebrates and invertebrates coincides with the dominant wave-induced flicker frequencies associated with underwater light. Waves also produce patterns off reflective objects that resemble many of the body markings found on fishes. The close relationship that exists between the physiological properties of spatial and temporal vision thus suggests an ancient adaptation to the wave-induced fluctuations and spatial patterns associated with underwater light.

Vitamin A2-based visual pigments in fully terrestrial vertebrates.

As part of a broad study of the ocular and extraocular photoreceptors of reptiles, we have used high performance liquid chromatography (HPLC) to identify the retinoids present in whole eye extracts of the arboreal lizard Anolis carolinensis and the non-arboreal ruin lizard Podarcis sicula. Unexpectedly, only vitamin A2-derived chromophore was detected in Anolis, while a mixture of vitamin A1- and vitamin A2-derived chromophores was detected in Podarcis. These are the first examples of fully terrestrial vertebrates using vitamin A2-derived chromophore for visual pigment generation. Furthermore, microspectrophotometric (MSP) data for Anolis show a class of photoreceptor having a visual pigment with maximum absorbance at about 625 nm, some 40 nm further into the red than has been found in any terrestrial vertebrate examined to date.

A short-wavelength sensitive cone mechanism in juvenile yellow perch, Perca flavescens

The retinal cone mosaic of adult yellow perch, Perca flavescens, consists of square units each having a central single cone surrounded by four identical twin cones. No cones are present at the corners of the square units. However, the cone types and organization of the retinal mosaic in juvenile P. flavescens has not been thoroughly described. We report here the presence of small, single cones at the corner positions of the square units in juvenile P. flavescens. Not every corner, nor every unit has these cones, and their distribution over the retina is not uniform. Microspectrophotometry places the visual pigment absorbance maximum of these short single cones in the region of 400 nm. Electrophysiological measurements of spectral sensitivity demonstrate a short-wavelength mechanism in juveniles that is absent, as are the small corner cones, in adults. Possible advantages of such a mechanism to juvenile perch are discussed.