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...
In order to protect their food from competitors, ball-rolling dung beetles detach a piece of dung from a pile, shape it into a ball, and roll it away along a straight path [1]. They appear to rely exclusively on celestial compass cues to maintain their bearing [2-8], but the mechanism that enables them to use these cues for orientation remains unknown. Here, we describe the orientation strategy that allows dung beetles to use celestial cues in a dynamic fashion. We tested the underlying orientation mechanism by presenting beetles with a combination of simulated celestial cues (sun, polarized light, and spectral cues). We show that these animals do not rely on an innate prediction of the natural geographical relationship between celestial cues, as other navigating insects seem to [9, 10]. Instead, they appear to form an internal representation of the prevailing celestial scene, a "celestial snapshot," even if that scene represents a physical impossibility for the real sky. We also find that the beetles are able to maintain their bearing with respect to the presented cues only if the cues are visible when the snapshot is taken. This happens during the "dance," a behavior in which the beetle climbs on top of its ball and rotates about its vertical axis [11]. This strategy for reading celestial signals is a simple but efficient mechanism for straight-line orientation.
Nocturnal dung beetles () 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 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'.
Highlights d Visual compass cues are obscured by skyglow in lightpolluted skies d Starlight at a light-polluted site is insufficient for dung beetle orientation d Light pollution led dung beetles to adopt a beaconing strategy
To transport their balls of dung along a constant bearing, diurnal savannah-living dung beetles rely primarily on the sun for compass information. However, in more cluttered environments, such as woodlands, this solitary compass cue is frequently hidden from view by surrounding vegetation. In these types of habitats, insects can, instead, rely on surrounding landmarks, the canopy pattern, or wide-field celestial cues, such as polarised skylight, for directional information. Here, we investigate the compass orientation strategy behind straight-line orientation in the diurnal woodland-living beetle Sisyphus fasciculatus. We found that, when manipulating the direction of polarised skylight, Si. fasciculatus responded to this change with a similar change in bearing. However, when the apparent position of the sun was moved, the woodland-living beetle did not change its direction of travel. In contrast, the savannah-living beetle Scarabaeus lamarcki responded to the manipulation of the solar position with a corresponding change in bearing. These results suggest that the dominant compass cue used for straight-line orientation in dung beetles may be determined by the celestial cue that is most prominent in their preferred habitat.
The sun is the most prominent source of directional information in the heading direction network of the diurnal, ball-rolling dung beetle Kheper lamarcki. If this celestial body is occluded from the beetle's field of view, the distribution of the relative weight between the directional cues that remain shifts in favour of the celestial pattern of polarised light. In this study, we continue to explore the interplay of the sun and polarisation pattern as directional cues in the heading direction network of K. lamarcki. By systematically altering the intensity and degree of the two cues presented, we effectively change the relative reliability of these directional cues as they appear to the dung beetle. The response of the ball-rolling beetle to these modifications allows us to closely examine how the weighting relationship of these two sources of directional information is influenced and altered in the heading direction network of the beetle. We conclude that the process in which K. lamarcki relies on directional information is very likely done based on Bayesian reasoning, where directional information conveying the highest certainty at a particular moment is afforded the greatest weight.
A degree-of-polarization threshold for orientation behaviour is 15 reported for nocturnal dung beetle Escarabaeus satyrus in the context 16 of measurements showing changes in the degree of polarization of 17 skylight with lunar phase. 18 Abstract 19For polarized light to inform behaviour, the typical range of degrees of 20 polarization observable in the animal's natural environment must be 21 above the threshold for detection and interpretation. Here we present 22 the first investigation of the degree of linear polarization threshold for 23 orientation behaviour in a nocturnal species, with specific reference to 24 the range of degrees of polarization measured in the night sky. An 25 effect of lunar phase on the degree of polarization of skylight was 26 found, with smaller illuminated fractions of the moon's surface 27 corresponding to lower degrees of polarization in the night sky. We 28 found that South African dung beetle Escarabaeus satyrus 29 (Boheman, 1860) can orient to polarized light for a range of 30 degrees of polarization similar to that observed in diurnal insects, 31 reaching a lower threshold between 0.04 and 0.32, possibly as low as 32 2 0.11. For degrees of polarization lower than 0.23, as measured on a 33 crescent moon night, orientation performance was considerably 34 weaker than that observed for completely linearly-polarized stimuli, 35 but was nonetheless stronger than in the absence of polarized light. 36
Moving along a straight path is a surprisingly difficult task. This is because, with each ensuing step, noise is generated in the motor and sensory systems, causing the animal to deviate from its intended route. When relying solely on internal sensory information to correct for this noise, the directional error generated with each stride accumulates, ultimately leading to a curved path. In contrast, external compass cues effectively allow the animal to correct for errors in its bearing. Here, we studied straight-line orientation in two different sized dung beetles. This allowed us to characterize and model the size of the directional error generated with each step, in the absence of external visual compass cues ( motor error ) as well as in the presence of these cues ( compass and motor errors ). In addition, we model how dung beetles balance the influence of internal and external orientation cues as they orient along straight paths under the open sky. We conclude that the directional error that unavoidably accumulates as the beetle travels is inversely proportional to the step size of the insect, and that both beetle species weigh the two sources of directional information in a similar fashion.
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