Diurnal and nocturnal African dung beetles use celestial cues, such as the sun, the moon, and the polarization pattern, to roll dung balls along straight paths across the savanna. Although nocturnal beetles move in the same manner through the same environment as their diurnal relatives, they do so when light conditions are at least 1 million-fold dimmer. Here, we show, for the first time to our knowledge, that the celestial cue preference differs between nocturnal and diurnal beetles in a manner that reflects their contrasting visual ecologies. We also demonstrate how these cue preferences are reflected in the activity of compass neurons in the brain. At night, polarized skylight is the dominant orientation cue for nocturnal beetles. However, if we coerce them to roll during the day, they instead use a celestial body (the sun) as their primary orientation cue. Diurnal beetles, however, persist in using a celestial body for their compass, day or night. Compass neurons in the central complex of diurnal beetles are tuned only to the sun, whereas the same neurons in the nocturnal species switch exclusively to polarized light at lunar light intensities. Thus, these neurons encode the preferences for particular celestial cues and alter their weighting according to ambient light conditions. This flexible encoding of celestial cue preferences relative to the prevailing visual scenery provides a simple, yet effective, mechanism for enabling visual orientation at any light intensity.he blue sky is a rich source of visual cues that are used by many animals during orientation or navigation (1, 2). Besides the sun, celestial phenomena, such as the skylight intensity gradient or the more complex polarization pattern, can serve as references for spatial orientation (3-5). Polarized skylight is generated by scattered sunlight in the atmosphere, and to a terrestrial observer, the resulting alignment of the electric field vectors extends across the entire sky, forming concentric circles around the position of the sun (Fig. 1A). A similar distribution of brightness and polarization pattern is also created around the moon (6). Although this nocturnal pattern is 1 million-fold dimmer than the daylight pattern (6), some animals, such as South African ball-rolling dung beetles, can use this lunar polarization pattern for orientation (7). To avoid competition for food at the dung pile, these beetles detach a piece of dung, shape it into a ball, and roll it away along a straightline path. For this type of straight-line orientation, nocturnal beetles seem to rely exclusively on celestial cues (8), such as the moon or polarized light.As with all nocturnal animals, night-active beetles have to overcome a major challenge: They need to maintain high orientation precision even under extremely dim light conditions. Indeed, recent experiments have shown that nocturnal dung beetles orient at night with the same precision as their diurnal relatives during the day (9), an ability partly due to the fact that their eyes are considerably more sensiti...
Many sea urchins can detect light on their body surface and some species are reported to possess image-resolving vision. Here, we measure the spatial resolution of vision in the long-spined sea urchin , using two different visual responses: a taxis towards dark objects and an alarm response of spine-pointing towards looming stimuli. For the taxis response we used visual stimuli, which were isoluminant to the background, to discriminate spatial vision from phototaxis. Individual animals were placed in the centre of a cylindrical arena under bright down-welling light, with stimuli of varying angular width placed on the arena wall at alternating directions from the centre. We tracked the direction of movement of individual animals in relation to the stimuli to determine whether the animals oriented towards the stimulus. We found that responds by taxis towards isoluminant stimuli with a spatial resolution in the range of 29-69 deg. This corresponds to a theoretical acceptance angle of 38-89 deg, assuming a contrast threshold of 10%. The visual acuity of the alarm response of was tested by exposing animals to different sized dark looming and appearing stimuli on a monitor. We found that displays a spine-pointing response to appearing black circles of 13-25 deg angular width, corresponding to an acceptance angle of 60-116 deg, assuming the same contrast threshold as above.
To escape competition at the dung pile, a ball-rolling dung beetle forms a piece of dung into a ball and rolls it away. To ensure their efficient escape from the dung pile, beetles rely on a 'celestial compass' to move along a straight path. Here, we analyzed the reliability of different skylight cues for this compass and found that dung beetles rely not only on the sun but also on the skylight polarization pattern. Moreover, we show the first evidence of an insect using the celestial light-intensity gradient for orientation. Using a polarizer, we manipulated skylight so that the polarization pattern appeared to turn by 90 deg. The beetles then changed their bearing close to the expected 90 deg. This behavior was abolished if the sun was visible to the beetle, suggesting that polarized light is hierarchically subordinate to the sun. When the sky was depolarized and the sun was invisible, the beetles could still move along straight paths. Therefore, we analyzed the use of the celestial light-intensity gradient for orientation. Artificial rotation of the intensity pattern by 180 deg caused beetles to orient in the opposite direction. This lightintensity cue was also found to be subordinate to the sun and could play a role in disambiguating the polarization signal, especially at low sun elevations.
Recent research has focused on the different types of compass cues available to ball-rolling beetles for orientation, but little is known about the relative precision of each of these cues and how they interact. In this study, we find that the absolute orientation error of the celestial compass of the day-active dung beetle Scarabaeus lamarcki doubles from 168 at solar elevations below 608 to an error of 298 at solar elevations above 758. As ball-rolling dung beetles rely solely on celestial compass cues for their orientation, these insects experience a large decrease in orientation precision towards the middle of the day. We also find that in the compass system of dung beetles, the solar cues and the skylight cues are used together and share the control of orientation behaviour. Finally, we demonstrate that the relative influence of the azimuthal position of the sun for straight-line orientation decreases as the sun draws closer to the horizon. In conclusion, ball-rolling dung beetles possess a dynamic celestial compass system in which the orientation precision and the relative influence of the solar compass cues change over the course of the day.
An interesting feature of dung beetle behaviour is that once they have formed a piece of dung into a ball, they roll it along a straight path away from the dung pile. This straight-line orientation ensures that the beetles depart along the most direct route, guaranteeing that they will not return to the intense competition (from other beetles) that occurs near the dung pile. Before rolling a new ball away from the dung pile, dung beetles perform a characteristic “dance,” in which they climb on top of the ball and rotate about their vertical axis. This dance behaviour can also be observed during the beetles' straight-line departure from the dung pile. The aim of the present study is to investigate the purpose of the dung beetle dance. To do this, we explored the circumstances that elicit dance behaviour in the diurnal ball-rolling dung beetle, Scarabaeus (Kheper) nigroaeneus. Our results reveal that dances are elicited when the beetles lose control of their ball or lose contact with it altogether. We also find that dances can be elicited by both active and passive deviations of course and by changes in visual cues alone. In light of these results, we hypothesise that the dung beetle dance is a visually mediated mechanism that facilitates straight-line orientation in ball-rolling dung beetles by allowing them to 1) establish a roll bearing and 2) return to this chosen bearing after experiencing a disturbance to the roll path.
SUMMARYGiven the great range of visual systems, tasks and habitats, there is surprisingly little experimental evidence of how visual limitations affect behavioural strategies under natural conditions. Analysing this relationship will require an experimental system that allows for the synchronous measurement of visual cues and visually guided behaviour. The first step in quantifying visual cues from an animal's perspective is to understand the filter properties of its visual system. We examined the first stage of visual processing -sampling by the ommatidial array -in the compound eye of the fiddler crab Uca vomeris. Using an in vivo pseudopupil method we determined sizes and viewing directions of ommatidia and created a complete eye map of optical and sampling resolution across the visual field. Our results reveal five distinct eye regions (ventral, dorsal, frontal, lateral and medial) which exhibit clear differences in the organisation of the local sampling array, in particular with respect to the balance of resolution and contrast sensitivity. We argue that, under global eye space constraints, these regional optimisations reflect the information content and behavioural relevance of the corresponding parts of the visual field. In demonstrating the tight link between visual sampling, visual cues and behavioural strategies, our analysis highlights how the study of natural behaviour and natural stimuli is essential to our understanding and interpretation of the evolution and ecology of animal behaviour and the design of sensory systems.
Night sky orientation with diurnal and nocturnal eyes: dim-light adaptations are critical when the moon is out of sight
To efficiently provide an animal with relevant information, the design of its visual system should reflect the distribution of natural signals and the animal's tasks. In many behavioural contexts, however, we know comparatively little about the moment-to-moment information-processing challenges animals face in their daily lives. In predator avoidance, for instance, we lack an accurate description of the natural signal stream and its value for risk assessment throughout the prey's defensive behaviour. We characterized the visual signals generated by real, potentially predatory events by video-recording bird approaches towards an Uca vomeris colony. Using four synchronized cameras allowed us to simultaneously monitor predator avoidance responses of crabs. We reconstructed the signals generated by dangerous and non-dangerous flying animals, identified the cues that triggered escape responses and compared them with those triggering responses to dummy predators. Fiddler crabs responded to a combination of multiple visual cues (including retinal speed, elevation and visual flicker) that reflect the visual signatures of distinct bird and insect behaviours. This allowed crabs to discriminate between dangerous and non-dangerous events. The results demonstrate the importance of measuring natural sensory signatures of biologically relevant events in order to understand biological information processing and its effects on behavioural organization.
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