Neural coding underlying the cue preference for celestial orientation

Abstract

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...

Spectral information as an orientation cue in dung beetles

“…The distribution of the changes of direction was tested using a V-test with an expected mean of 08 or 1808. Similar to previous studies [3,11,13], the reliability of the V-test was analysed using permutation tests (electronic supplementary material, figure S1). Mardia -Watson -Wheeler tests were used to test for differences between circular data.…”

“…While the relative intensity of green light is much higher in the direction of the sun, the intensity of ultraviolet (UV) light is relatively higher in the opposite sky hemisphere. Some insects, such as bees [8][9][10] and dung beetles [11], interpret an artificial green light spot as the sun direction. In addition, an artificial UV light stimulus is interpreted by bees during their waggle dances to be in the antisolar hemisphere, indicating that they can use the celestial chromatic gradient for navigation, as has also been suggested for ants [12].…”

How animals follow the stars

“…These ball-rolling beetles use celestial cues to maintain their initial heading and prevent them from returning to their point of origin. For crepuscular and nocturnal beetles, the moon [2] and patterns of lunar skylight [31,32] form part of this celestial compass. One nocturnal species, Scarabaeus satyrus, remains oriented in the absence of lunar skylight, but not in the absence of starlight, indicating a capacity to use stellar cues [11,33].…”

Polarization Vision—Overcoming Challenges of Working with a Property of Light We Barely See

“…A great number of insect species possess a specialised 173 polarization sensitive region in the dorsal eye, the dorsal rim area (DRA), which is used 174 to detect this skylight pattern (Wehner & Strasser, 1985;Labhart & Meyer, 1999). At 175 night, when scattered sunlight is no longer present, moonlight scattered via the same 176 process provides an equivalent polarization pattern that can be used by crepuscular 177 and nocturnal dung beetles, and perhaps other night active insects, for orientation 178 (Dacke et al, 2004;el Jundi et al, 2015). 179…”

“…189 6 led to clear demonstrations of the extraordinary polarization vision of cephalopods and 191 crustaceans How et al, 2012Daly et al, 2016). Careful 192 study of the neuronal processing of skylight polarization cues in insects has led to an 193 improved model for how skylight polarization is interpreted (Pfeiffer & Homberg, 2007;194 Bech et al, 2014) and combined with other orientation cues (el Jundi et al, 2015). As 195 we come closer to understanding the details of this aspect of the animal visual world 196 that remains alien to our intuition, it continues to be important to focus on the methods 197 we use to produce, control and measure polarized stimuli.…”