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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 utility of UV vision for visualizing habitat structure is poorly known. Here, the authors use optical models and multispectral imaging to show that UV vision reveals sharp visual contrasts between leaf surfaces, potentially an advantage in navigating forest environments.

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.

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 behaviours 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 behaviours for finding a suitable habitat and position itself within it. Orientation based on spatial vision obviously involves active guidance of behaviours 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 behaviours 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 categorised.

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.

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.

Nocturnal dung beetles (Scarabaeus satyrus) are currently the only animals that have been demonstrated to use the Milky Way for reliable orientation. In this study, we tested the capacity of S. satyrus to orient under a range of artificial celestial cues, and compared the properties of these cues with images of the Milky Way simulated for a beetle's visual system. We find that the mechanism that permits accurate stellar orientation under the Milky Way is based on an intensity comparison between different regions of the Milky Way. We determined the beetles' contrast sensitivity for this task in behavioural experiments in the laboratory, and found that the resulting threshold of 13% is sufficient to detect the contrast between the southern and northern arms of the Milky Way under natural conditions. This mechanism should be effective under extremely dim conditions and on nights when the Milky Way forms a near symmetrical band that crosses the zenith. These findings are discussed in the context of studies of stellar orientation in migratory birds and itinerant seals. This article is part of the themed issue ‘Vision in dim light’.

Background Arthropod eyes have diversified during evolution to serve multiple needs, such as finding mates, hunting prey and navigating in complex surroundings under varying light conditions. This diversity is reflected in the optical apparatus, photoreceptors and neural circuits that underpin vision. Yet our ability to genetically manipulate the visual system to investigate its function is largely limited to a single species, the fruit fly Drosophila melanogaster . Here, we describe the visual system of Parhyale hawaiensis , an amphipod crustacean for which we have established tailored genetic tools. Results Adult Parhyale have apposition-type compound eyes made up of ~ 50 ommatidia. Each ommatidium contains four photoreceptor cells with large rhabdomeres (R1–4), expected to be sensitive to the polarisation of light, and one photoreceptor cell with a smaller rhabdomere (R5). The two types of photoreceptors express different opsins, belonging to families with distinct wavelength sensitivities. Using the cis- regulatory regions of opsin genes, we established transgenic reporters expressed in each photoreceptor cell type. Based on these reporters, we show that R1–4 and R5 photoreceptors extend axons to the first optic lobe neuropil, revealing striking differences compared with the photoreceptor projections found in related crustaceans and insects. Investigating visual function, we show that Parhyale have a positive phototactic response and are capable of adapting their eyes to different levels of light intensity. Conclusions We propose that the visual system of Parhyale serves low-resolution visual tasks, such as orientation and navigation, based on broad gradients of light intensity and polarisation. Optic lobe structure and photoreceptor projections point to significant divergence from the typical organisation found in other malacostracan crustaceans and insects, which could be associated with a shift to low-resolution vision. Our study provides the foundation for research in the visual system of this genetically tractable species.

Fossilized eyes permit inferences of the visual capacity of extinct arthropods 1 – 3 . However, structural and/or chemical modifications as a result of taphonomic and diagenetic processes can alter the original features, thereby necessitating comparisons with modern species. Here we report the detailed molecular composition and microanatomy of the eyes of 54-million-year-old crane-flies, which together provide a proxy for the interpretation of optical systems in some other ancient arthropods. These well-preserved visual organs comprise calcified corneal lenses that are separated by intervening spaces containing eumelanin pigment. We also show that eumelanin is present in the facet walls of living crane-flies, in which it forms the outermost ommatidial pigment shield in compound eyes incorporating a chitinous cornea. To our knowledge, this is the first record of melanic screening pigments in arthropods, and reveals a fossilization mode in insect eyes that involves a decay-resistant biochrome coupled with early diagenetic mineralization of the ommatidial lenses. The demonstrable secondary calcification of lens cuticle that was initially chitinous has implications for the proposed calcitic corneas of trilobites, which we posit are artefacts of preservation rather than a product of in vivo biomineralization 4 – 7 . Although trilobite eyes might have been partly mineralized for mechanical strength, a (more likely) organic composition would have enhanced function via gradient-index optics and increased control of lens shape. Comparing the eyes of crane-fly fossils with those of extant species demonstrates that they contain eumelanic screening pigments and that the lenses are calcified during fossilization, with implications for interpreting optical systems in other extinct arthropods such as trilobites.

Counterilluminating animals use ventral photogenic organs (photophores) to mimic the residual downwelling light and cloak their silhouette from upward-looking predators. To cope with variable conditions of pelagic light environments they typically adjust their luminescence intensity. Here, we found evidence that bioluminescent sharks instead emit a constant light output and move up and down in the water column to remain cryptic at iso-luminance depth. We observed, across 21 globally distributed shark species, a correlation between capture depth and the proportion of a ventral area occupied by photophores. This information further allowed us, using visual modelling, to provide an adaptive explanation for shark photophore pattern diversity: in species facing moderate predation risk from below, counterilluminating photophores were partially co-opted for bioluminescent signalling, leading to complex patterns. In addition to increase our understanding of pelagic ecosystems our study emphasizes the importance of bioluminescence as a speciation driver.

Fan worms, represented by sabellid and serpulid polychaetes, have an astonishing array of unusual eyes and photoreceptors located on their eponymous feeding appendages. Here we organize the previous descriptions of these eyes in serpulids and report new anatomical, molecular, and physiological data regarding their structure, function, and evolution and the likely identity of their phototransduction machinery. We report that, as in sabellids, serpulids display a broad diversity of radiolar eye arrangements and ocellar structures. Furthermore, the visual pigment expressed in the eyes of Spirobranchus corniculatus, a species of the charismatic Christmas tree worms, absorbs light maximally at 464 nm in wavelength. This visual pigment closely matches the spectrum of downwelling irradiance in shallow coral reef habitats and lends support to the hypothesis that these radiolar photoreceptors function as a silhouette-detecting “burglar alarm” that triggers a rapid withdrawal response when the worm is threatened by potential predators. Finally, we report on the transcriptomic sequencing results for the radiolar eyes of S. corniculatus, which express invertebrate c-type opsins in their ciliary radiolar photoreceptors, closely related to the opsin found in the radiolar eyes of the sabellid Acromegalomma interruptum. We explore the potential for a shared evolutionary lineage between the radiolar photoreceptors of serpulids and sabellids and consider these unique innovations in the broader context of metazoan eye evolution.