UV vision is prevalent, but we know little about its utility in common general tasks, as in resolving habitat structure. Here we visualize vegetated habitats using a multispectral camera with ...channels mimicking bird photoreceptor sensitivities across the UV-visible spectrum. We find that the contrast between upper and lower leaf surfaces is higher in a UV channel than in any visible channel, and that this makes leaf position and orientation stand out clearly. This was unexpected since both leaf surfaces reflect similarly small proportions (1-2%) of incident UV light. The strong UV-contrast can be explained by downwelling light being brighter than upwelling, and leaves transmitting < 0.06% of incident UV light. We also find that mirror-like specular reflections of the sky and overlying canopy, from the waxy leaf cuticle, often dwarf diffuse reflections. Specular reflections shift leaf color, such that maximum leaf-contrast is seen at short UV wavelengths under open canopies, and at long UV wavelengths under closed canopies.
The morphology and molecular mechanisms of animal photoreceptor cells and eyes reveal a complex pattern of duplications and co-option of genetic modules, leading to a number of different ...light-sensitive systems that share many components, in which clear-cut homologies are rare. On the basis of molecular and morphological findings, I discuss the functional requirements for vision and how these have constrained the evolution of eyes. The fact that natural selection on eyes acts through the consequences of visually guided behaviour leads to a concept of task-punctuated evolution, where sensory systems evolve by a sequential acquisition of sensory tasks. I identify four key innovations that, one after the other, paved the way for the evolution of efficient eyes. These innovations are (i) efficient photopigments, (ii) directionality through screening pigment, (iii) photoreceptor membrane folding, and (iv) focusing optics. A corresponding evolutionary sequence is suggested, starting at non-directional monitoring of ambient luminance and leading to comparisons of luminances within a scene, first by a scanning mode and later by parallel spatial channels in imaging eyes.
How animals follow the stars Foster, James J.; Smolka, Jochen; Nilsson, Dan-Eric ...
Proceedings - Royal Society. Biological sciences/Proceedings - Royal Society. Biological Sciences,
01/2018, Letnik:
285, Številka:
1871
Journal Article
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Throughout history, the stars have provided humans with ever more information about our world, enabling increasingly accurate systems of navigation in addition to fuelling some of the greatest ...scientific controversies. What information animals have evolved to extract from a starry sky and how they do so, is a topic of study that combines the practical and theoretical challenges faced by both astronomers and field biologists. While a number of animal species have been demonstrated to use the stars as a source of directional information, the strategies that these animals use to convert this complex and variable pattern of dim-light points into a reliable ‘stellar orientation’ cue have been more difficult to ascertain. In this review, we assess the stars as a visual stimulus that conveys directional information, and compare the bodies of evidence available for the different stellar orientation strategies proposed to date. In this context, we also introduce new technologies that may aid in the study of stellar orientation, and suggest how field experiments may be used to characterize the mechanisms underlying stellar orientation.
Most known starfish species possess a compound eye at the tip of each arm, which, except for the lack of true optics, resembles an arthropod compound eye. Although these compound eyes have been known ...for about two centuries, no visually guided behaviour has ever been directly associated with their presence. There are indications that they are involved in negative phototaxis but this may also be governed by extraocular photoreceptors. Here, we show that the eyes of the coral-reef-associated starfish Linckia laevigata are slow and colour blind. The eyes are capable of true image formation although with low spatial resolution. Further, our behavioural experiments reveal that only specimens with intact eyes can navigate back to their reef habitat when displaced, demonstrating that this is a visually guided behaviour. This is, to our knowledge, the first report of a function of starfish compound eyes. We also show that the spectral sensitivity optimizes the contrast between the reef and the open ocean. Our results provide an example of an eye supporting only low-resolution vision, which is believed to be an essential stage in eye evolution, preceding the high-resolution vision required for detecting prey, predators and conspecifics.
Just like other complex biological features, image vision (multi-pixel light sensing) did not evolve suddenly. Animal visual systems have a long prehistory of non-imaging light sensitivity. The first ...spatial vision was likely very crude with only few pixels, and evolved to improve orientation behaviors previously supported by single-channel directional photoreception. The origin of image vision was simply a switch from single to multiple spatial channels, which improved the behaviors for finding a suitable habitat and position itself within it. Orientation based on spatial vision obviously involves active guidance of behaviors but, by necessity, also assessment of habitat suitability and environmental conditions. These conditions are crucial for deciding when to forage, reproduce, seek shelter, rest, etc. When spatial resolution became good enough to see other animals and interact with them, a whole range of new visual roles emerged: pursuit, escape, communication and other interactions. All these new visual roles require entirely new types of visual processing. Objects needed to be separated from the background, identified and classified to make the correct choice of interaction. Object detection and identification can be used actively to guide behaviors but of course also to assess the over-all situation. Visual roles can thus be classified as either ancient non-object-based tasks, or object vision. Each of these two categories can also be further divided into active visual tasks and visual assessment tasks. This generates four major categories of vision into which I propose that all visual roles can be categorized.
Animal eyes have evolved to process behaviorally important visual information, but how retinas deal with statistical asymmetries in visual space remains poorly understood. Using hyperspectral imaging ...in the field, in vivo 2-photon imaging of retinal neurons, and anatomy, here we show that larval zebrafish use a highly anisotropic retina to asymmetrically survey their natural visual world. First, different neurons dominate different parts of the eye and are linked to a systematic shift in inner retinal function: above the animal, there is little color in nature, and retinal circuits are largely achromatic. Conversely, the lower visual field and horizon are color rich and are predominately surveyed by chromatic and color-opponent circuits that are spectrally matched to the dominant chromatic axes in nature. Second, in the horizontal and lower visual field, bipolar cell terminals encoding achromatic and color-opponent visual features are systematically arranged into distinct layers of the inner retina. Third, above the frontal horizon, a high-gain UV system piggybacks onto retinal circuits, likely to support prey capture.
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•The larval zebrafish retina is anatomically and functionally asymmetric•The upper-frontal visual field is dominated by UV-sensitive prey-capture circuits•Circuits for tetrachromatic color vision survey the horizon and lower visual field•This organization matches natural chromatic statistics and behavioral demands
With half of their brain located inside the eyes, every neuron counts in the larval zebrafish retina. By 2-photon and hyperspectral natural imaging, Zimmermann et al. show how their near-360° visual field is functionally divided into tetrachromatic, achromatic, and UV prey-capture regions to match available visual information in nature.
In the vertebrate eye, photoreceptors are covered beneath a thick sheet of neural retina and face away from the light. This seemingly awkward arrangement has led to the popular notion that our ...retinas are upside down, implying a deep design flaw. Baden and Nilsson argue that, from an evolutionary perspective, an inverted design actually offers many notable benefits that might have never been exploited if things had started off the other way round.
To expand our understanding of what tasks are particularly helped by UV vision and may justify the costs of focusing high-energy light onto the retina, we used an avian-vision multispectral camera to ...image diverse vegetated habitats in search of UV contrasts that differ markedly from visible-light contrasts. One UV contrast that stood out as very different from visible-light contrasts was that of nutrient-dense non-signaling plant foods (such as young leaves and immature fruits) against their natural backgrounds. From our images, we calculated color contrasts between 62+ species of such foods and mature foliage for the two predominant color vision systems of birds, UVS and VS. We also computationally generated images of what a generalized tetrachromat, unfiltered by oil droplets, would see, by developing a new methodology that uses constrained linear least squares to solve for optimal weighted combinations of avian camera filters to mimic new spectral sensitivities. In all visual systems, we found that nutrient-dense non-signaling plant foods presented a lower, often negative figure-ground contrast in the UV channels, and a higher, often positive figure-ground contrast in the visible channels. Although a zero contrast may sound unhelpful, it can actually enhance color contrast when compared in a color opponent system to other channels with nonzero contrasts. Here, low or negative UV contrasts markedly enhanced color contrasts. We propose that plants may struggle to evolve better UV crypsis since UV reflectance from vegetation is largely specular and thus highly dependent on object orientation, shape, and texture.
Box jellyfish have an impressive set of 24 eyes of four different types, including eyes structurally similar to those of vertebrates and cephalopods 1, 2. However, the known visual responses are ...restricted to simple phototaxis, shadow responses, and object avoidance responses 3–8, and it has been a puzzle why they need such a complex set of eyes. Here we report that medusae of the box jellyfish Tripedalia cystophora are capable of visually guided navigation in mangrove swamps using terrestrial structures seen through the water surface. They detect the mangrove canopy by an eye type that is specialized to peer up through the water surface and that is suspended such that it is constantly looking straight up, irrespective of the orientation of the jellyfish. The visual information is used to navigate to the preferred habitat at the edge of mangrove lagoons.
► Box jellyfish actively navigate to their preferred habitat at the shoreline ► They navigate by detecting terrestrial visual structures of the shoreline ► A specialized type of eye is constantly peering through the water surface
Combining studies of animal visual systems with exact imaging of their visual environment can get us a step closer to understand how animals see their “Umwelt”. Here, we have combined both methods to ...better understand how males of the speckled wood butterfly,
Pararge aegeria
, see the surroundings of their perches. These males are well known to sit and wait for a chance to mate with a passing females, in sunspot territories in European forests. We provide a detailed description of the males' body and head posture, viewing direction, visual field and spatial resolution, as well as the visual environment.
Pararge aegeria
has sexually dimorphic eyes, the smallest interommatidial angles of males are around 1°, those of females 1.5°. Perching males face the antisolar direction with their retinal region of the highest resolution pointing at an angle of about 45° above the horizon; thus, looking at a rather even and dark background in front of which they likely have the best chance to detect a sunlit female passing through the sunspot.
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