On the structure of the aerial visual field of aquatic animals distorted by refraction

The aerial visual field of aquatic animals living near the water surface is distorted by refraction. The imaging of aerial objects by one or two submerged eyes is studied. The aerial binocular image field is determined for pairs of submerged eyes in horizonal and vertical planes. These two image spaces have significantly different structures. Aquatic animals have to correct for refraction, adapting themselves to the former aerial image field in order to recognize aerial predators or to capture such prey. The other aerial image space is only of theoretical interest.     

Harbor Seals (Phoca vitulina) Can Perceive Optic Flow under Water

Optic flow, the pattern of apparent motion elicited on the retina during movement, has been demonstrated to be widely used by animals living in the aerial habitat, whereas underwater optic flow has not been intensively studied so far. However optic flow would also provide aquatic animals with valuable information about their own movement relative to the environment; even under conditions in which vision is generally thought to be drastically impaired, e. g. in turbid waters. Here, we tested underwater optic flow perception for the first time in a semi-aquatic mammal, the harbor seal, by simulating a forward movement on a straight path through a cloud of dots on an underwater projection. The translatory motion pattern expanded radially out of a singular point along the direction of heading, the focus of expansion. We assessed the seal''s accuracy in determining the simulated heading in a task, in which the seal had to judge whether a cross superimposed on the flow field was deviating from or congruent with the actual focus of expansion. The seal perceived optic flow and determined deviations from the simulated heading with a threshold of 0.6 deg of visual angle. Optic flow is thus a source of information seals, fish and most likely aquatic species in general may rely on for e. g. controlling locomotion and orientation under water. This leads to the notion that optic flow seems to be a tool universally used by any moving organism possessing eyes.     

Visual orientation by the crown-of-thorns starfish (<Emphasis Type="Italic">Acanthaster planci</Emphasis>)

Photoreception in echinoderms has been known for over 200 years, but their visual capabilities remain poorly understood. As has been reported for some asteroids, the crown-of-thorns starfish (Acanthaster planci) possess a seemingly advanced eye at the tip of each of its 7–23 arms. With such an array of eyes, the starfish can integrate a wide field of view of its surroundings. We hypothesise that, at close range, orientation and directional movements of the crown-of-thorns starfish are visually guided. In this study, the eyes and vision of A. planci were examined by means of light microscopy, electron microscopy, underwater goniometry, electroretinograms and behavioural experiments in the animals’ natural habitat. We found that only animals with intact vision could orient to a nearby coral reef, whereas blinded animals, with olfaction intact, walked in random directions. The eye had peak sensitivity in the blue part (470 nm) of the visual spectrum and a narrow, horizontal visual field of approximately 100° wide and 30° high. With approximately 250 ommatidia in each adult compound eye and average interommatidial angles of 8°, crown-of-thorns starfish have the highest spatial resolution of any starfish studied to date. In addition, they have the slowest vision of all animals examined thus far, with a flicker fusion frequency of only 0.6–0.7 Hz. This may be adaptive as fast vision is not required for the detection of stationary objects such as reefs. In short, the eyes seem optimised for detecting large, dark, stationary objects contrasted against an ocean blue background. Our results show that the visual sense of the crown-of-thorns starfish is much more elaborate than has been thus far appreciated and is essential for orientation and localisation of suitable habitats.     

NO EVIDENCE OF ACCOMMODATION IN THE EYES OF THE BOTTLENOSE DOLPHIN, TURSIOPS TRUNCATUS

Bottlenose dolphins ( Tursiops truncatus ) are aquatic mammals that must come to the surface to breathe. As a result, it might be expected that their eyes are adapted for both aerial and underwater vision. Earlier studies suggest that dolphins are emmetropic ( i. e. , focused at infinity) in water, and in some cases, emmetropic in air, although the mechanisms that permit these animals to see well in both media are not well understood. Nor is it known whether they can accommodate to focus sharply on objects at different distances. We employed video photoretinoscopy to investigate the possibility of an active accommodative mechanism in the eyes of the bottlenose dolphin in water. Measurements of the refractive state in water indicated near emmetropia for two individuals and slight myopia (nearsightedness) for the third individual. No clear cases of accommodation were observed underwater in any of the subjects examined. Vision underwater may be used to supplement echolocation. If so, such a role might not require an accommodative mechanism.     

Visual accommodation and active pursuit of prey underwater in a plunge-diving bird: the Australasian gannet

Australasian gannets (Morus serrator), like many other seabird species, locate pelagic prey from the air and perform rapid plunge dives for their capture. Prey are captured underwater either in the momentum (M) phase of the dive while descending through the water column, or the wing flapping (WF) phase while moving, using the wings for propulsion. Detection of prey from the air is clearly visually guided, but it remains unknown whether plunge diving birds also use vision in the underwater phase of the dive. Here we address the question of whether gannets are capable of visually accommodating in the transition from aerial to aquatic vision, and analyse underwater video footage for evidence that gannets use vision in the aquatic phases of hunting. Photokeratometry and infrared video photorefraction revealed that, immediately upon submergence of the head, gannet eyes accommodate and overcome the loss of greater than 45 D (dioptres) of corneal refractive power which occurs in the transition between air and water. Analyses of underwater video showed the highest prey capture rates during WF phase when gannets actively pursue individual fish, a behaviour that very likely involves visual guidance, following the transition after the plunge dive's M phase. This is to our knowledge the first demonstration of the capacity for visual accommodation underwater in a plunge diving bird while capturing submerged prey detected from the air.     

Comparative aerial and underwater visual acuity of the mink, Mustela vison schreber, as a function of discrimination distance and stimulus luminance

The aerial threshold visual angle of mink rose from 15.4 min at 10 cm stimulus distance to 19.1 min at 90 cm and the underwater angle varied from 32.7 min at 10 cm to 46.6 min at 90 cm, all at 34 mL luminance. At constant 30 cm stimulus distance, the aerial angle rose from 15 min at 34 mL to 51.7 min at 0.012 mL, the underwater angle from 31.4 min at 34 mL to 95 min at 0.012 mL, the aerial and underwater data forming similar curves. If mink hunt in water at somewhat higher light levels than in air they can obtain equal acuities in the two media.     

Neural mechanisms of recovery following early visual deprivation

Natural patterned early visual input is essential for the normal development of the central visual pathways and the visual capacities they sustain. Without visual input, the functional development of the visual system stalls not far from the state at birth, and if input is distorted or biased the visual system develops in an abnormal fashion resulting in specific visual deficits. Monocular deprivation, an extreme form of biased exposure, results in large anatomical and physiological changes in terms of territory innervated by the two eyes in primary visual cortex (V1) and to a loss of vision in the deprived eye reminiscent of that in human deprivation amblyopia. We review work that points to a special role for binocular visual input in the development of V1 and vision. Our unique approach has been to provide animals with mixed visual input each day, which consists of episodes of normal and biased (monocular) exposures. Short periods of concordant binocular input, if continuous, can offset much longer episodes of monocular deprivation to allow normal development of V1 and prevent amblyopia. Studies of animal models of patching therapy for amblyopia reveal that the benefits are both heightened and prolonged by daily episodes of binocular exposure.     

Coherence in nervous system design: the visual system of Pantodon buchholzi

One of the more unusual visual systems of the Actinopterygii is that of Pantodon buchholzi (Osteoglossomorpha: Osteoglossidae). Its adaptations associate neuroanatomy at different levels of the visual system with ecological and behavioural correlates and demonstrate that the visual system of this fish has adapted for simultaneous vision in air and water. The visual field is divided into three distinct areas: for viewing into the water column, into air, and for viewing the aquatic reflection from the underside of the water surface. Cone diameters in different retinal areas correlate with the differing physical constraints in the respective visual field. Retinal differentiation between the aquatic and aerial views is paralleled at different levels of the central nervous system. A diencephalic nucleus receives both direct and indirect (tectal) afferent input from only the aerial visual system and a specific type of cell in the optic tectum is preferentially distributed in the tectum processing aerial inputs. Distinctions within a single sensory system suggest that some behaviours may be organized according to visual field. For Pantodon, feeding is initiated by stimuli seen by the ventral hemiretina so the anatomical specializations may well play an important role as elements in a feeding circuit.     

Scanning behavior by larvae of the predacious diving beetle, <Emphasis Type="Italic">Thermonectus marmoratus</Emphasis> (Coleoptera: Dytiscidae) enlarges visual field prior to prey capture

Larvae of the predaceous diving beetle Thermonectus marmoratus bear six stemmata on each side of their head, two of which form relatively long tubes with linear retinas at their proximal ends. The physical organization of these eyes results in extremely narrow visual fields that extend only laterally in the horizontal body plane. There are other examples of animals possessing eyes with predominantly linear retinas, or with linear arrangements of specific receptor types. In these animals, the eyes, or parts of the eyes, are movable and perform scanning movements to increase the visual field. Based on anatomical data and observations of relatively transparent, immobilized young larvae, we report here that T. marmoratus larvae are incapable of moving their eyes or any part of their eyes within the head capsule. However, they do perform a series of bodily dorso-ventral pivots prior to prey capture, behaviorally extending the vertical visual field from 2° to up to 50°. Frame-by-frame analysis shows that such behavior is performed within a characteristic distance to the prey. These data provide first insights into the function of the very peculiar anatomical eye organization of T. marmoratus larvae.     

Respiration in air and water of three mangrove snails

The oxygen consumption of three species of Malaysian mangrove gastropods was measured in air and sea water at the temperatures commonly recorded in the mangrove. The experiments in air were carried out after the animals had regained fluid lost from the mantle due to handling. Fluid loss can have considerable effects on rate of oxygen consumption. Nerita arliculata (Gould) was found throughout the mangrove and experiences from 50 to 92% aerial exposure. It has a gill and a ratio of aerial to aquatic respiration rates of 2.7 at 28°C. 50% of the animals can survive underwater for 72 h at 28°C. The other two species, Cerithidea obtusa (Lamarck) and Cassidula aurisfelis (Brugière) experience over 95% aerial exposure, have their mantle cavities modified as lungs and have air : water respiration rate ratios of 5.5 and 6.0, respectively. 50% can survive from 48 to 36 h underwater at 28°C. Acclimated animals have Q₁₀'s of about 1.6 in air and 1.4 in water. The respiratory physiology of the snails is compared with that of rocky shore species.     

Brief daily periods of binocular vision prevent deprivation-induced acuity loss

The role of experience in the development of the central visual pathways has been explored in the past through examination of the consequences of imposed periods of continuously abnormal or biased visual input. The massive changes in the visual cortex (area 17) induced by selected early visual experience, especially monocular deprivation (MD) or experience (ME) where patterned visual input is provided to just one eye, are accompanied by profound and long-standing visual deficits. Although the use of exclusively abnormal experience permits identification of those aspects of the visual cortex and of visual function that can be influenced by visual experience during development, this approach may provide a distorted view of the nature of the role of visual experience because of the absence of any normal visual input. In this study a different approach was used whereby animals were provided daily with separate periods of normal (i.e., binocular exposure) and abnormal (monocular exposure) visual experience. We show that 2 hr of daily normal concordant binocular experience (BE) can outweigh or protect against much longer periods of monocular deprivation (MD) and permit the development of normal visual acuities in the two eyes. This result is not what would be expected if all visual input had equal influence on visual development.     

Inapparent visual field defects in multiple sclerosis patients

To assess inapparent visual field defects in patients with multiple sclerosis free from optic neuritis. During 5 years period 120 patients with multiple sclerosis were examined at the University Department of Ophthalmology, Zagreb University Hospital Center. They were divided into three groups with 40 patients each: patients with acute unilateral optic neuritis, referred to ophthalmologist and treated with pulsed steroid therapy; patients with subjective feeling of blurred vision, normal visual acuity and no signs of acute optic neuritis; and patients free from subjective signs of visual impairment. Study patients underwent standard ophthalmologic examination and visual field testing in photopia by use of quantitative kinetic Goldmann perimetry. The initial and control examination by visual field testing were performed at least 6 months apart. Study results showed 65% of multiple sclerosis patients to have visual field defects without subjective signs of impaired vision. The most common defects were mild to moderate visual field narrowing with blind spot enlargement and depression from above. The following results were recorded: acute optic neuritis group: normal in 13/40 (32.5%) for the affected eyes and 27/40 (67.5%) for fellow eyes; mild visual field narrowing in 4/40 (10%) for the affected eyes and 10/40 (25%) for fellow eyes; moderate visual field narrowing with blind spot enlargement in 14/40 (35%) for the affected eyes and 1/40 (2.5%) for fellow eyes; and paracentral and arcuate scotomata in 9/40 (22.5%) for the affected eyes and 2/40 (5%) for fellow eyes; subjective symptom group: normal in 8/40 (20%) for the affected eyes and 11/40 (27.5%) for fellow eyes; mild visual field narrowing in 11/40 (27.5%) for the affected eyes and 16/40 (40%) for fellow eyes; moderate visual field narrowing with blind spot enlargement in 18/40 (45%) for the affected eyes and 10/40 (25%); andparacentral and arcuate scotomata in 3/40 (7.5%) for both affected and fellow eyes; and subjective symptom-free group: normal in 24/80 (30%), mild visual field narrowing in 22/80 (27.5%) moderate visual field narrowing with blind spot enlargement in 24/80 (30%); and paracentral and arcuate scotomata in 10/80 (12.5%). The presence of subclinical form of optic nerve involvement could be demonstrated in a very early stage of multiple sclerosis by the introduction of visual field testing in the standard examination protocol.     

The Spectral Sensitivities of Single Receptor Cells in the Lateral, Median, and Ventral Eyes of Normal and White-Eyed Limulus

Spectral sensitivity curves can be distorted by screening pigments. We have determined whether this is true for Limulus polyphemus by determining, from receptor potentials recorded using intracellular microelectrodes, spectral sensitivity curves for normal animals and for white-eyed animals (which lack screening pigment). Our results show: (a) In median ocelli, the curve for UV-sensitive receptor cells peaks at 360 nm and does not depend on the presence of screening pigment, (b) The curve for ventral eye photoreceptors is identical to that for retinular cells from the lateral eyes of white-eyed animals and peaks at 520–525 nm. (c) In normal lateral eyes, when the stimulating light passes through screening pigment, the curve indicates relatively more sensitivity in the red region of the spectrum than does the curve for white-eyed animals. Therefore, the screening pigment is probably red-transmitting, (d) In median ocelli, the curve for visible-sensitive cells peaks at 525 nm and is approximately the same whether the ocelli are from normal or white-eyed animals. However, the curve is significantly broader than that for ventral eyes and for lateral eyes from white-eyed animals.     

A spitting image: specializations in archerfish eyes for vision at the interface between air and water

Archerfish are famous for spitting jets of water to capture terrestrial insects, a task that not only requires oral dexterity, but also the ability to detect small camouflaged prey against a visually complex background of overhanging foliage. Because detection of olfactory, auditory and tactile cues is diminished at air–water interfaces, archerfish must depend almost entirely on visual cues to mediate their sensory interactions with the aerial world. During spitting, their eyes remain below the water''s surface and must adapt to the optical demands of both aquatic and aerial fields of view. These challenges suggest that archerfish eyes may be specially adapted to life at the interface between air and water. Using microspectrophotometry to characterize the spectral absorbance of photoreceptors, we find that archerfish have differentially tuned their rods and cones across their retina, correlated with spectral differences in aquatic and aerial fields of view. Spatial resolving power also differs for aquatic and aerial fields of view with maximum visual resolution (6.9 cycles per degree) aligned with their preferred spitting angle. These measurements provide insight into the functional significance of intraretinal variability in archerfish and infer intraretinal variability may be expected among surface fishes or vertebrates where different fields of view vary markedly.     

How birds use their eyes: Opposite left-right specialization for the lateral and frontal visual hemifield in the domestic chick

Recent evidence has demonstrated that, in animals with laterally placed eyes, functional cerebral asymmetry is revealed by preferential use of either the left or right eye in a range of behaviors (birds: [1, 2, 3]; fish: [4, 5]; reptiles: [6, 7]). These findings pose a theoretical problem. It seems that there would be disadvantages in having a substantial degree of asymmetry in the use of the two eyes; a deficit on one side would leave the organism vulnerable to attack on that side or unable to exploit resources appearing on one side. We here report a possible solution to the problem. We have found that domestic chicks show selective use of the lateral visual field of the left eye and of the right hemifield in the binocular, frontal visual field when they peck at strangers but not at cagemates. Thus, during social recognition, there seems to be opposite and complementary left-right specialization for the lateral and frontal visual fields of the two eyes. These findings can reconcile the computational advantages associated with asymmetry of the left and right sides of the brain with the ecological demands for an animal to perceive and respond equally well to the left and right sides of its midline.     

Comparative assessment of amphibious hearing in pinnipeds

Auditory sensitivity in pinnipeds is influenced by the need to balance efficient sound detection in two vastly different physical environments. Previous comparisons between aerial and underwater hearing capabilities have considered media-dependent differences relative to auditory anatomy, acoustic communication, ecology, and amphibious life history. New data for several species, including recently published audiograms and previously unreported measurements obtained in quiet conditions, necessitate a re-evaluation of amphibious hearing in pinnipeds. Several findings related to underwater hearing are consistent with earlier assessments, including an expanded frequency range of best hearing in true seals that spans at least six octaves. The most notable new results indicate markedly better aerial sensitivity in two seals (Phoca vitulina and Mirounga angustirostris) and one sea lion (Zalophus californianus), likely attributable to improved ambient noise control in test enclosures. An updated comparative analysis alters conventional views and demonstrates that these amphibious pinnipeds have not necessarily sacrificed aerial hearing capabilities in favor of enhanced underwater sound reception. Despite possessing underwater hearing that is nearly as sensitive as fully aquatic cetaceans and sirenians, many seals and sea lions have retained acute aerial hearing capabilities rivaling those of terrestrial carnivores.     

Modelling heterogeneity in detection probabilities in land and aerial abundance surveys in humpback whales (<Emphasis Type="Italic">Megaptera novaeangliae</Emphasis>)

The effective management and conservation of animal populations relies on statistically-sound and replicable surveys to obtain estimates of abundance and assess trends. Surveys of cetaceans, such as humpback whales Megaptera novaeangliae, are difficult to conduct and are particularly affected by bias in detection probability. For example, the probability of detection of whales from land decreases substantially with increased distance from the platform. This distance effect is also true for aerial surveys, combined with the problem that animals are unavailable for detection (underwater) whilst in the field of view. We present a novel approach that combines corrected double-platform land surveys with corrected aerial surveys to obtain a robust estimate of g(0), the probability of detection on the survey line, for aerial surveys of migrating humpback whales. Several sources of heterogeneity in detection probabilities were identified within the land and aerial surveys (including group composition, bearing of first sighting, number of groups being tracked simultaneously and cloud cover). After including these into our estimate of ĝ(0), we found that only 29% of available whales are being detected on the survey line (ĝ(0) = 0.288), which is a considerably smaller estimate than many available for humpback whales using other methods. Incorporating heterogeneity into the population surveys shows that we are likely to be underestimating the population size of whales on the east coast of Australia. The implications of this result for their conservation and management in light of increased whale-human conflict is discussed.     

Modelling the visual world of a velvet worm

In many animal phyla, eyes are small and provide only low-resolution vision for general orientation in the environment. Because these primitive eyes rarely have a defined image plane, traditional visual-optics principles cannot be applied. To assess the functional capacity of such eyes we have developed modelling principles based on ray tracing in 3D reconstructions of eye morphology, where refraction on the way to the photoreceptors and absorption in the photopigment are calculated incrementally for ray bundles from all angles within the visual field. From the ray tracing, we calculate the complete angular acceptance function of each photoreceptor in the eye, revealing the visual acuity for all parts of the visual field. We then use this information to generate visual filters that can be applied to high resolution images or videos to convert them to accurate representations of the spatial information seen by the animal. The method is here applied to the 0.1 mm eyes of the velvet worm Euperipatoides rowelli (Onychophora). These eyes of these terrestrial invertebrates consist of a curved cornea covering an irregular but optically homogeneous lens directly joining a retina packed with photoreceptive rhabdoms. 3D reconstruction from histological sections revealed an asymmetric eye, where the retina is deeper in the forward-pointing direction. The calculated visual acuity also reveals performance differences across the visual field, with a maximum acuity of about 0.11 cycles/deg in the forward direction despite laterally pointing eyes. The results agree with previous behavioural measurements of visual acuity, and suggest that velvet worm vision is adequate for orientation and positioning within the habitat.     

Orienting behaviour during aerial and underwater visual discrimination by the mink (Mustela vison schreber)

Orienting responses by mink during aerial and underwater visual discrimination tests were most frequent when the grating lines subtended angles at the eye near the visual threshold angle. Factorial analysis showed that in air and in water at ranges from 10 to 90 cm most responses occurred at 30 cm discrimination distance and more occurred to marginally supra-threshold than to marginally sub-threshold stimuli. Between media, more responses occurred in air than in water. At longer ranges the mink oriented less readily than at 30 cm but if orienting occurred better discrimination followed than if the mink did not orient.     

The visual ecology of fiddler crabs

With their eyes on long vertical stalks, their panoramic visual field and their pronounced equatorial acute zone for vertical resolving power, the visual system of fiddler crabs is exquisitely tuned to the geometry of vision in the flat world of inter-tidal mudflats. The crabs live as burrow-centred grazers in dense, mixed-sex, mixed-age and mixed-species colonies, with the active space of an individual rarely exceeding 1 m². The full behavioural repertoire of fiddler crabs can thus be monitored over extended periods of time on a moment to moment basis together with the visual information they have available to guide their actions. These attributes make the crabs superb subjects for analysing visual tasks and the design of visual processing mechanisms under natural conditions, a prerequisite for understanding the evolution of visual systems. In this review we show, on the one hand, how deeply embedded fiddler crab vision is in the behavioural and the physical ecology of these animals and, on the other hand, how their behavioural options are constrained by their perceptual limitations. Studying vision in fiddler crabs reminds us that vision has a topography, that it is context-dependent and pragmatic and that there are perceptual limits to what animals can know and therefore care about. For Mike Land