Cephalopod versus vertebrate eyes.

Vertebrates and cephalopods are the two major animal groups that view the world through sophisticated camera-type eyes. There are of course exceptions: nautiloid cephalopods have more simply built pinhole eyes. Excellent camera type eyes are also found in other animals, such as some spider groups, a few snails, and certain marine worms, but the vast majority of large camera-type eyes belong to cephalopods and vertebrates. Vertebrates and cephalopods also devote major parts of their brains to the processing of visual information. Obviously, there are differences in eye performance among cephalopods and vertebrates, but there are no major subgroups where vision seems to have low priority. The similarity in eye geometry is striking, especially between fish and coleoid cephalopods, with a hemispherical retina centred around a spherical lens. Do these similarities mean that vertebrate and cephalopod eyes are equally good? Comparing the eyes of vertebrates and cephalopods reveals many fundamental differences with surprisingly small consequences for vision, but also one difference that means that cephalopods and vertebrates do not share the same visual world.

Description of Light Environment in Broiler Breeder Houses with Different Light Sources-And How It Differs from Natural Forest Light.

Light is a key factor in poultry production; however, there is still a lack of knowledge as to describing the light quality, how to measure the light environment as perceived by birds, and how artificial light compares with the light in the natural forest habitats of their wild ancestors. The aim of this study was to describe the light environment in broiler breeder houses with three different light sources, using two different methods of light assessment. We also aimed to compare an artificial light environment with the light in a range of relevant natural forest habitats. A total of 9 commercial broiler breeder houses with one of three different light sources-Lumilux 830 CFL (n = 3), Biolux 965 CFL (n = 3) or LED Evolys with UVA (n = 3) were visited. Assessments of the light environment in the breeder houses were conducted using both a spectrometer and the environmental light field (ELF) method. ELF measurements from three forest types in south India (Kerala) were also included. We found that most aspects of the light environment were similar between the nine breeder houses and were not dependent on the type of light sources. The only clear difference related to the light source was the spectral balance, wherein 830 CFL had the most red-dominated light, 965 CFL had the most blue-dominated light and Evolys was intermediate but with more UV than the latter two. Plumage color had minimal effect on the light environment. Both the spectrometer and the ELF method provided valuable information. The spectrometer gave detailed values about certain aspects of the light environment, while the ELF described the light more in line with human and avian visual perception. We also found that the light environment in the investigated broiler breeder houses differs dramatically in all measured aspects from the natural light habitats of wild junglefowl, suggesting improvement possibilities in artificial lighting systems.

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.

The Diversity of Eyes and Vision.

Every aspect of vision, from the opsin proteins to the eyes and the ways that they serve animal behavior, is incredibly diverse. It is only with an evolutionary perspective that this diversity can be understood and fully appreciated. In this review, I describe and explain the diversity at each level and try to convey an understanding of how the origin of the first opsin some 800 million years ago could initiate the avalanche that produced the astonishing diversity of eyes and vision that we see today. Despite the diversity, many types of photoreceptors, eyes, and visual roles have evolved multiple times independently in different animals, revealing a pattern of eye evolution strictly guided by functional constraints and driven by the evolution of gradually more demanding behaviors. I conclude the review by introducing a novel distinction between active and passive vision that points to uncharted territories in vision research.

Quantifying biologically essential aspects of environmental light.

Quantifying and comparing light environments are crucial for interior lighting, architecture and visual ergonomics. Yet, current methods only catch a small subset of the parameters that constitute a light environment, and rarely account for the light that reaches the eye. Here, we describe a new method, the environmental light field (ELF) method, which quantifies all essential features that characterize a light environment, including important aspects that have previously been overlooked. The ELF method uses a calibrated digital image sensor with wide-angle optics to record the radiances that would reach the eyes of people in the environment. As a function of elevation angle, it quantifies the absolute photon flux, its spectral composition in red-green-blue resolution as well as its variation (contrast-span). Together these values provide a complete description of the factors that characterize a light environment. The ELF method thus offers a powerful and convenient tool for the assessment and comparison of light environments. We also present a graphic standard for easy comparison of light environments, and show that different natural and artificial environments have characteristic distributions of light.

Lens eyes in protists.

Eyes are not unique to animals. As described by Nilsson and Marshall, prominent eyes, complete with retina and lens, have unexpectedly evolved in single cell dinoflagellates.

More than meets the eye: Predator-induced pupil size plasticity in a teleost fish.

Most animals are visually oriented, and their eyes provide their 'window to the world'. Eye size correlates positively with visual performance, because larger eyes can house larger pupils that increase photon catch and contrast discrimination, particularly under dim light, which have positive effects on behaviours that enhance fitness, including predator avoidance and foraging. Recent studies have linked predation risk to selection for larger eyes and pupils, and such changes should be of importance for the majority of teleost fishes as they have a pupil that is fixed in size (eyes lack a pupillary sphincter muscle) and, hence, do not respond to changes in light conditions. Here, we quantify eye and pupil size of individual crucian carp, a common freshwater fish, following controlled manipulations of perceived predation risk (presence/absence). We also tested if crucian carp responded to increased predation risk by shifts in diel activity patterns. We found that crucian carp show phenotypic plasticity with regards to pupil size, but not eye size, as pupil size increased when exposed to predators (pike). Predator-exposed crucian carp also shifted from diurnal to nocturnal activity. Using a modelling exercise, we moreover show that the plastically enlarged pupils significantly increase visual range, especially for small objects under dim light conditions. Overall, our results provide compelling evidence for predator-induced pupil enlargement resulting in enhanced visual capabilities in a teleost fish. Pupil size plasticity in combination with the observed shift towards nocturnal activity may allow for efficient foraging also under dark conditions when predation risk from diurnal and visually oriented predators is reduced. The data highlight the powerful role of predation risk for eye development and evolution.

A millipede compound eye mediating low-resolution vision.

Millipedes are a species-rich and ancient arthropod clade which typically bear a pair of lateral compound eyes with a small number of large facets. To understand the visual tasks that underlie the evolution of millipede eyes, their spatial resolving performance is of key importance. We here investigate the spatial resolution of the millipede Cylindroiulus punctatus using behavioural assays. Individual animals were placed in the centre of a cylindrical arena under bright downwelling light, with dark stimuli of varying angular dimensions placed on the arena wall. We used continuous isoluminant stimuli based on a difference of Gaussians signal to test for orientation to the dark target via object taxis. Headings of individual animals were tracked in relation to the stimuli to determine whether the animals oriented towards the stimulus. We implemented a multilevel logistic regression model to identify the arc width of the stimulus that animals could resolve. We then modelled the angular sensitivity needed to identify this. We also related the visual performance to the 3D anatomy of the eye. We found that C. punctatus can resolve a stimulus of 56° period (sufficient to detect a 20° dark target). Assuming a contrast threshold of 10%, this requires a receptor acceptance angle of 72° or narrower. Spatial resolving power this low would only suffice for the simplest visual tasks, such as shelter-seeking.

Low-Resolution Vision-at the Hub of Eye Evolution.

Simple roles for photoreception are likely to have preceded more demanding ones such as vision. The driving force behind this evolution is the improvement and elaboration of animal behaviors using photoreceptor input. Because the basic role for all senses aimed at the external world is to guide behavior, we argue here that understanding this "behavioral drive" is essential for unraveling the evolutionary past of the senses. Photoreception serves many different types of behavior, from simple shadow responses to visual communication. Based on minimum performance requirements for different types of tasks, photoreceptors have been argued to have evolved from non-directional receptors, via directional receptors, to low-resolution vision, and finally to high-resolution vision. Through this sequence, the performance requirements on the photoreceptors have gradually changed from broad to narrow angular sensitivity, from slow to fast response, and from low to high contrast sensitivity during the evolution from simple to more advanced and demanding behaviors. New behaviors would only evolve if their sensory performance requirements to some degree overlap with the requirements of already existing behaviors. This need for sensory "performance continuity" must have determined the order by which behaviors have evolved and thus been an important factor guiding animal evolution. Naturally, new behaviors are most likely to evolve from already existing behaviors with similar neural processing needs and similar motor responses, pointing to "neural continuity" as another guiding factor in sensory evolution. Here we use these principles to derive an evolutionary tree for behaviors driven by photoreceptor input.

Evolution: An Irresistibly Clear View of Land.

Visually guided predation is range-limited in water, but works over long distances on land. This may have driven our last aquatic ancestors to evolve large eyes on the top of their head for spotting crunchy meals on ancient riverbanks.

Interpreting melanin-based coloration through deep time: a critical review.

Colour, derived primarily from melanin and/or carotenoid pigments, is integral to many aspects of behaviour in living vertebrates, including social signalling, sexual display and crypsis. Thus, identifying biochromes in extinct animals can shed light on the acquisition and evolution of these biological traits. Both eumelanin and melanin-containing cellular organelles (melanosomes) are preserved in fossils, but recognizing traces of ancient melanin-based coloration is fraught with interpretative ambiguity, especially when observations are based on morphological evidence alone. Assigning microbodies (or, more often reported, their 'mouldic impressions') as melanosome traces without adequately excluding a bacterial origin is also problematic because microbes are pervasive and intimately involved in organismal degradation. Additionally, some forms synthesize melanin. In this review, we survey both vertebrate and microbial melanization, and explore the conflicts influencing assessment of microbodies preserved in association with ancient animal soft tissues. We discuss the types of data used to interpret fossil melanosomes and evaluate whether these are sufficient for definitive diagnosis. Finally, we outline an integrated morphological and geochemical approach for detecting endogenous pigment remains and associated microstructures in multimillion-year-old fossils.

Computational visual ecology in the pelagic realm.

Visual performance and visual interactions in pelagic animals are notoriously hard to investigate because of our restricted access to the habitat. The pelagic visual world is also dramatically different from benthic or terrestrial habitats, and our intuition is less helpful in understanding vision in unfamiliar environments. Here, we develop a computational approach to investigate visual ecology in the pelagic realm. Using information on eye size, key retinal properties, optical properties of the water and radiance, we develop expressions for calculating the visual range for detection of important types of pelagic targets. We also briefly apply the computations to a number of central questions in pelagic visual ecology, such as the relationship between eye size and visual performance, the maximum depth at which daylight is useful for vision, visual range relations between prey and predators, counter-illumination and the importance of various aspects of retinal physiology. We also argue that our present addition to computational visual ecology can be developed further, and that a computational approach offers plenty of unused potential for investigations of visual ecology in both aquatic and terrestrial habitats.

The giant eyes of giant squid are indeed unexpectedly large, but not if used for spotting sperm whales.

BACKGROUND: We recently reported (Curr Biol 22:683-688, 2012) that the eyes of giant and colossal squid can grow to three times the diameter of the eyes of any other animal, including large fishes and whales. As an explanation to this extreme absolute eye size, we developed a theory for visual performance in aquatic habitats, leading to the conclusion that the huge eyes of giant and colossal squid are uniquely suited for detection of sperm whales, which are important squid-predators in the depths where these squid live. A paper in this journal by Schmitz et al. (BMC Evol Biol 13:45, 2013) refutes our conclusions on the basis of two claims: (1) using allometric data they argue that the eyes of giant and colossal squid are not unexpectedly large for the size of the squid, and (2) a revision of the values used for modelling indicates that large eyes are not better for detection of approaching sperm whales than they are for any other task. RESULTS AND CONCLUSIONS: We agree with Schmitz et al. that their revised values for intensity and abundance of planktonic bioluminescence may be more realistic, or at least more appropriately conservative, but argue that their conclusions are incorrect because they have not considered some of the main arguments put forward in our paper. We also present new modelling to demonstrate that our conclusions remain robust, even with the revised input values suggested by Schmitz et al.

Eye evolution and its functional basis.

Eye evolution is driven by the evolution of visually guided behavior. Accumulation of gradually more demanding behaviors have continuously increased the performance requirements on the photoreceptor organs. Starting with nondirectional photoreception, I argue for an evolutionary sequence continuing with directional photoreception, low-resolution vision, and finally, high-resolution vision. Calculations of the physical requirements for these four sensory tasks show that they correlate with major innovations in eye evolution and thus work as a relevant classification for a functional analysis of eye evolution. Together with existing molecular and morphological data, the functional analysis suggests that urbilateria had a simple set of rhabdomeric and ciliary receptors used for directional photoreception, and that organ duplications, positional shifts and functional shifts account for the diverse patterns of eyes and photoreceptors seen in extant animals. The analysis also suggests that directional photoreception evolved independently at least twice before the last common ancestor of bilateria and proceeded several times independently to true vision in different bilaterian and cnidarian groups. This scenario is compatible with Pax-gene expression in eye development in the different animal groups. The whole process from the first opsin to high-resolution vision took about 170 million years and was largely completed by the onset of the Cambrian, about 530 million years ago. Evolution from shadow detectors to multiple directional photoreceptors has further led to secondary cases of eye evolution in bivalves, fan worms, and chitons.

Molecular preservation of the pigment melanin in fossil melanosomes.

Fossil feathers, hairs and eyes are regularly preserved as carbonized traces comprised of masses of micrometre-sized bodies that are spherical, oblate or elongate in shape. For a long time, these minute structures were regarded as the remains of biofilms of keratinophilic bacteria, but recently they have been reinterpreted as melanosomes; that is, colour-bearing organelles. Resolving this fundamental difference in interpretation is crucial: if endogenous then the fossil microbodies would represent a significant advancement in the fields of palaeontology and evolutionary biology given, for example, the possibility to reconstruct integumentary colours and plumage colour patterns. It has previously been shown that certain trace elements occur in fossils as organometallic compounds, and hence may be used as biomarkers for melanin pigments. Here we expand this knowledge by demonstrating the presence of molecularly preserved melanin in intimate association with melanosome-like microbodies isolated from an argentinoid fish eye from the early Eocene of Denmark.

Temporal properties of the lens eyes of the box jellyfish Tripedalia cystophora.

Box jellyfish (Cubomedusae) are visually orientating animals which possess a total of 24 eyes of 4 morphological types; 2 pigment cup eyes (pit eye and slit eye) and 2 lens eyes [upper lens-eye (ule) and lower lens-eye (lle)]. In this study, we use electroretinograms (ERGs) to explore temporal properties of the two lens eyes. We find that the ERG of both lens eyes are complex and using sinusoidal flicker stimuli we find that both lens eyes have slow temporal resolution. The average flicker fusion frequency (FFF) was found to be approximately 10 Hz for the ule and 8 Hz for the lle. Differences in the FFF and response patterns between the two lens eyes suggest that the ule and lle filter information differently in the temporal domain and thus are tuned to perform different visual tasks. The data collected in this study support the idea that the visual system of box jellyfish is a collection of special purpose eyes.

Structure and optics of the eyes of the box jellyfish Chiropsella bronzie.

Cubomedusae have a total of 24 eyes of four morphologically different types. Two of these eye types are camera-type eyes (upper and lower lens-eye), while the other two eye types are simpler pigment pit eyes (pit and slit eye). Here, we give a description of the visual system of the box jellyfish species Chiropsella bronzie and the optics of the lens eyes in this species. One aim of this study is to distinguish between general cubozoan features and species-specific features in the layout and optics of the eyes. We find that both types of lens eyes are more severely under-focused in C. bronzie than those in the previously investigated species Tripedalia cystophora. In the lower lens-eye of C. bronzie, blur circles subtend 20 and 52 degrees for closed and open pupil, respectively, effectively removing all but the coarsest structures of the image. Histology reveals that the retina of the lower lens-eye, in addition to pigmented photoreceptors, also contains long pigment-cells, with both dark and white pigment, where the dark pigment migrates on light/dark adaptation. Unlike the upper lens-eye lens of T.cystophora, the same eye in C.bronzie did not display any significant optical power.

Eye evolution: the blurry beginning.

Recent work on the expression of retinal transcription factors and other molecular cues delivers interesting but partly contradictory information on the early phases of eye evolution.

Unique structure and optics of the lesser eyes of the box jellyfish Tripedalia cystophora.

The visual system of box jellyfish comprises a total of 24 eyes. These are of four types and each probably has a special function. To investigate this hypothesis the morphology and optics of the lesser eyes, the pit and slit eyes, were examined. The pit eyes hold one cell type only and are probably mere light meters. The slit eyes, comprising four cell types, are complex and highly asymmetric. They also hold a lens-like structure, but its optical power is minute. Optical modeling suggests spatial resolution, but only in one plane. These unique and intriguing traits support strong peripheral filtering.

A functional analysis of compound eye evolution.

New data on the phylogenetic relationships of various arthropod groups have spurred interesting attempts to reconstruct the evolution of arthropod nervous and visual systems. Some of the relevant new data are cell identities and developmental processes in the nervous and sensory systems, which is particularly useful for reconstructing the evolution of these systems. Here, we focus on the structure of compound eye ommatidia, and make an evolutionary analysis with functional arguments. We investigate possible routes of evolution that can be understood in terms of selection for improved visual function, and arrive at a number of conclusions that are discussed in the light of recent phylogenetic hypotheses. On the basis of ommatidial focusing structures and the arrangement of receptor cells we show that the evolution of compound eyes proceeded largely independently along at least two lineages from very primitive ancestors. A common ancestor of insects and crustaceans is likely to have had ommatidia with focusing crystalline cones, and colour and/or polarization vision. In contrast, the compound eyes in myriapods and chelicerates are likely to date back to ancestors with corneal lenses and probably without the ability to discriminate colour and polarization.