Kerstin A. Fritsches

Warm Eyes Provide Superior Vision in Swordfishes

Large and powerful ocean predators such as swordfishes, some tunas, and several shark species are unique among fishes in that they are capable of maintaining elevated body temperatures (endothermy) when hunting for prey in deep and cold water . In these animals, warming the central nervous system and the eyes is the one common feature of this energetically costly adaptation . In the swordfish (Xiphias gladius), a highly specialized heating system located in an extraocular muscle specifically warms the eyes and brain up to 10 degrees C-15 degrees C above ambient water temperatures . Although the function of neural warming in fishes has been the subject of considerable speculation , the biological significance of this unusual ability has until now remained unknown. We show here that warming the retina significantly improves temporal resolution, and hence the detection of rapid motion, in fast-swimming predatory fishes such as the swordfish. Depending on diving depth, temporal resolution can be more than ten times greater in these fishes than in fishes with eyes at the same temperature as the surrounding water. The enhanced temporal resolution allowed by heated eyes provides warm-blooded and highly visual oceanic predators, such as swordfishes, tunas, and sharks, with a crucial advantage over their agile, cold-blooded prey.

Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus)

The visuotopic organisation of the primary visual cortex (V1) was studied by extracellular recordings in adult male marmosets (Callithrix jacchus) that were anaesthetised with sufentanil/nitrous oxide and paralysed with pancuronium bromide. Extensive sampling of the occipital region in four individuals and partial coverage of V1 in five others allowed not only the establishment of the normal visuotopy but also the study of interindividual variability. As in other primates, there was a single, continuous map of the contralateral hemifield in V1, with the upper visual quadrant represented ventrally and the lower quadrant represented dorsally. The surface area of V1, which was measured in two‐dimensional reconstructions of the cortical surface, varied from 192 to 217 mm2. There was a marked emphasis on the representation of the foveal and parafoveal visual fields: the representation of the central 5° of the visual field occupied 36–39% of the surface area of V1, whereas the central 10° occupied 57–59%. No asymmetry between the representations of the upper and lower quadrants was apparent. The visual topography of V1 was highly consistent between individuals, relative to both sulcal landmarks and stereotaxic coordinates. The entire contralateral hemifield was represented in V1; in addition, neurones with receptive fields whose borders invaded the ipsilateral hemifield were observed within V1, less than 800 μm from the V1/V2 boundary. The total invasion of the ipsilateral hemifield was less than 0.5° at the centre of the fovea but reached 8° at the periphery of the vertical meridian. Our results demonstrate that the organisation of V1 is similar in diurnal New and Old World simians, despite major variations in size, ecological niche, and timing of postnatal development across species.

Retinal specializations in the blue marlin: eyes designed for sensitivity to low light levels

The large eyes and well-developed visual system of billfishes suggest that vision is an important sense for the detection and interception of prey and lures. Investigations of visual abilities in these large pelagic fishes are difficult, however anatomical studies of billfish eyes and retinas allow prediction of a number of visual capabilities. From the density of ganglion cells in the blue marlin (Makaira nigricans) retina, visual acuities of less than 10 cycles per degree were derived, a surprisingly low visual resolution given the absolute size of the marlin eye. Cone photoreceptors, on the other hand, were present in high densities, resulting in a presumed summation of cones to ganglion cells at a ratio of 40:1, even in the area of best vision. The optical sensitivity of the marlin eye was high owing to the large dimensions of the cone photoreceptors. These results indicate that the marlin eye is specifically adapted to cope with the low light levels encountered during diving. Since the marlin is likely to use its vision at depth, it is suggested that this line of research could help estimate the limits of vertical distribution based on light level.

The second visual area in the marmoset monkey: visuotopic organisation, magnification factors, architectonical boundaries, and modularity.

The organisation of the second visual area (V2) in marmoset monkeys was studied by means of extracellular recordings of responses to visual stimulation and examination of myelin‐ and cytochrome oxidase‐stained sections. Area V2 forms a continuous cortical belt of variable width (1–2 mm adjacent to the foveal representation of V1, and 3–3.5 mm near the midline and on the tentorial surface) bordering V1 on the lateral, dorsal, medial, and tentorial surfaces of the occipital lobe. The total surface area of V2 is approximately 100 mm2, or about 50% of the surface area of V1 in the same individuals. In each hemisphere, the receptive fields of V2 neurones cover the entire contralateral visual hemifield, forming an ordered visuotopic representation. As in other simians, the dorsal and ventral halves of V2 represent the lower and upper contralateral quadrants, respectively, with little invasion of the ipsilateral hemifield. The representation of the vertical meridian forms the caudal border of V2, with V1, whereas a field discontinuity approximately coincident with the horizontal meridian forms the rostral border of V2, with other visually responsive areas. The bridge of cortex connecting dorsal and ventral V2 contains neurones with receptive fields centred within 1° of the centre of the fovea. The visuotopy, size, shape and location of V2 show little variation among individuals. Analysis of cortical magnification factor (CMF) revealed that the V2 map of the visual field is highly anisotropic: for any given eccentricity, the CMF is approximately twice as large in the dimension parallel to the V1/V2 border as it is perpendicular to this border. Moreover, comparison of V2 and V1 in the same individuals demonstrated that the representation of the central visual field is emphasised in V2, relative to V1. Approximately half of the surface area of V2 is dedicated to the representation of the central 5° of the visual field. Calculations based on the CMF, receptive field scatter, and receptive field size revealed that the point‐image size measured parallel to the V1/V2 border (2–3 mm) equals the width of a full cycle of cytochrome oxidase stripes in V2, suggesting a close correspondence between physiological and anatomical estimates of the dimensions of modular components in this area. J. Comp. Neurol. 387:547–567, 1997.

Ocular morphology of the Leatherback sea turtle (Dermochelys coriacea)

OBJECTIVE The Leatherback sea turtle is the largest extant reptile and the sole member of the family Dermochelyidae. Here, the eye of this critically endangered marine turtle was investigated to determine the anatomy, optics, and optical sensitivity. ANIMALS STUDIED Three Leatherback sea turtles, Dermochelys coriacea. RESULTS The eye is small in proportion to body size of the adult compared to other vertebrates, with prominence of the retractor bulbi and pyramidalis muscles. The nictitans shows extensive folding of the bulbar conjunctiva as an apparent mechanism to increase the surface area for mucus secretion. The intraocular anatomy is consistent with an eye adapted to aquatic vision with minimal curvature of the cornea, a near-spherical lens, deep ciliary cleft and highly vascularized ciliary body. The optical sensitivity, a measure of the sensitivity to light of a given optical system, is higher than in other marine turtles studied but lower than those found in teleost fish that share a habitat with the Leatherback sea turtle. CONCLUSIONS The Leatherback sea turtle shows ocular features that are characteristic of Chelonians with similarities to aquatic mammals. The calculated optical sensitivity suggests that compared to pelagic fishes, for instance, the Leatherback sea turtle eye is not particularly well adapted for vision in dim light even though this species is known to venture into deep, dark waters, and might feed at night.

An Anatomical Study of the Visual Capabilities of the Green Turtle, Chelonia mydas

Abstract Several aspects of vision in juvenile and adult Green Turtles (Chelonia mydas) are examined, with special reference to retinal anatomy such as oil droplet topography, transmission electron microscopy of photoreceptors, spectral transmission measurements of the ocular media (cornea, lens, and vitreous humor), and measurements of focal length and optical sensitivity. A detailed study of the distribution of the different color classes of oil droplets shows that all oil droplets are found in high concentrations (>1000 mm−2) in the central/temporal parts of the retina. Red oil droplets were the largest, followed by yellow and clear. Oil droplet size varied in different parts of the retina. On average, red oil droplets were found in fewer numbers compared to yellow and clear oil droplets. Two types of clear oil droplets were identified: those that fluoresced under UV illumination and those that did not. We found that the majority (78.5%) of colorless oil droplets fluoresced when viewed under UV light. Spectral transmission measurements of the ocular media show that wavelengths to approximately 325 nm are transmitted. This may suggest ultraviolet (UV) vision in Green Turtles. The optical sensitivity of the Green Turtle eye was relatively low, suggesting an adaptation to high light intensities commonly experienced by this species.

Lens optical properties in the eyes of large marine predatory teleosts

The optical properties of the crystalline lenses were studied in a variety of large predatory teleosts (bony fishes) that forage in the open ocean, some of them at considerable depths. We found the first fish lenses that are free of measurable longitudinal spherical aberration, i.e., are perfectly monofocal, in contrast to the multifocal lenses that are typical for smaller fishes living close to the surface. In fact, none of the lenses investigated in this study were clearly multifocal. Most, but not all, of the lenses had long normalized focal lengths (focal length/lens radius) of up to 3.3 lens radii. A monofocal lens of long focal length, combined with spectrally suitably placed cone pigments, may be the optimal solution for vision of high spatial and spectral resolutions in a habitat where the available spectrum of light is limited.

Prey capture and accommodation in the sandlance, Limnichthyes fasciatus (Creediidae; Teleostei).

Abstract The eyes of the sandlance, Limnichthyes fasciatus (Creediidae, Teleostei) move independently and possess a refractive cornea, a convexiclivate fovea and a non-spherical lens giving rise to a wide separation of the nodal point from the axis of rotation of the eye much like that of a chameleon. To investigate this apparent convergence of the visual optics in these phylogenetically disparate species, we examine feeding behaviour and accommodation in the sandlance with special reference to the possibility that sandlances use accommodation as a depth cue to judge strike length. Frame-by-frame analysis of over 2000 strikes show a 100% success rate. Explosive strikes are completed in 50 ms over prey distances of four body lengths. Close-up video confirms that successful strikes can be initiated monocularly (both normally and after monocular occlusion) showing that binocular cues are not necessary to judge the length of a strike. Additional means of judging prey distance may also be derived from parallax information generated by rotation of the eye as suggested for chameleons. Using photorefraction on anaesthetised sandlances, accommodative changes were induced with acetylcholine and found to range between 120 D and 180 D at a speed of 600–720 D s−1. The large range of accommodation (25% of the total power) is also thought to be mediated by corneal accommodation where the contraction of a unique cornealis muscle acts to change the corneal curvatures.

Eye growth in sharks: Ecological implications for changes in retinal topography and visual resolution

The visual abilities of sharks show substantial interspecific variability. In addition, sharks may change their habitat and feeding strategy throughout life. As the eyes of sharks continue to grow throughout the animals lifetime, ontogenetic variability in visual ability may also occur. The topographic analysis of the photoreceptor and ganglion cell distributions can identify visual specializations and assess changes in visual abilities that may occur concurrently with eye growth. This study examines an ontogenetic series of whole-mounted retinas in two elasmobranch species, the sandbar shark, Carcharhinus plumbeus, and the shortspine spurdog, Squalus mitsukurii, to identify regional specializations mediating zones for improved spatial resolution. The study examines retinal morphology and presents data on summation ratios between photoreceptor and ganglion cell layers, anatomically determined peak spatial resolving power, and the angular extent of the visual field. Peak densities of photoreceptors and ganglion cells occur in similar retinal locations. The topographic distribution of neurons in the ganglion cell layer does not differ substantially with eye growth. However, predicted peak spatial resolution increases with eye growth from 4.3 to 8.9 cycles/deg in C. plumbeus and from 5.7 to 7.2 cycles/deg in S. mitsukurii. The topographic distribution of different-sized ganglion cells is also mapped in C. plumbeus, and a population of large ganglion cells (soma area 120-350 microm2) form a narrow horizontal streak across the retinal meridian, while the spatial distribution of ordinary-sized ganglion cells (soma area 30-120 microm2) forms an area in the central retina. Species-specific retinal specializations highlight differences in visually mediated behaviors and foraging strategies between C. plumbeus and S. mitsukurii.

Australian Loggerhead sea turtle hatchlings do not avoid yellow

When emerging from the nest, sea turtle hatchlings primarily orient using visual stimuli, with light pollution known to disrupt effective sea localization behavior. Previous studies have shown that sea turtle hatchlings respond differently to different wavelengths of light but Loggerhead hatchlings, exclusively among species tested, have a strong aversion to yellow light (at 600 nm). This study repeats these experiments with an Australian population of Loggerhead hatchlings (Caretta caretta) and Flatback hatchlings (Natator depressus). The orientation preference was measured using a modified y-maze set-up with the animals response observed using an infrared camera. This study showed that both Loggerhead and Flatback hatchlings can see and are attracted to light in the ultraviolet waveband (365 nm) and, to a lesser extent to longer wavelengths of 600 nm and above. The surprising finding was that the Loggerhead hatchlings tested here, unlike their conspecifics in Florida, do not show any avoidance to yellow but are attracted to bright lights of wavelength between 365 nm (UV) and 600 nm. This suggests potential differences in the visual behavior among different populations of sea turtles of the same species. No difference was detected in the response of Loggerhead hatchlings to flickering or steady light stimuli.