Jochen Smolka

Neural coding underlying the cue preference for celestial orientation

Significance Many animals use the sun or moon and the polarization pattern for navigation. We combined behavioral experiments with physiological measurements of brain activity to reveal which celestial cue dominates the orientation compass of diurnal and nocturnal dung beetles. The preference found behaviorally precisely matches the preference encoded neurally and shows how the brain dynamically controls the cue preference for orientation at different levels: The sun or moon always dominates the orientation behavior and neural tuning of diurnal beetles, whereas in nocturnal beetles, celestial bodies dominate tuning only in bright light, with a switch to polarized light at night. This flexible neural tuning in the nocturnal species provides a simple mechanism that allows it to use the most reliable available orientation cue. 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.

Topography of vision and behaviour

SUMMARY Given 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 animals 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.

Natural visual cues eliciting predator avoidance in fiddler crabs

To efficiently provide an animal with relevant information, the design of its visual system should reflect the distribution of natural signals and the animals 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 preys 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.

Diurnal dung beetles use the intensity gradient and the polarization pattern of the sky for orientation.

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 light-intensity 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.

Dung beetles ignore landmarks for straight-line orientation

Upon locating a suitable dung pile, ball-rolling dung beetles shape a piece of dung into a ball and roll it away in a straight line. This guarantees that they will not return to the dung pile, where they risk having their ball stolen by other beetles. Dung beetles are known to use celestial compass cues such as the sun, the moon and the pattern of polarised light formed around these light sources to roll their balls of dung along straight paths. Here, we investigate whether terrestrial landmarks have any influence on straight-line orientation in dung beetles. We find that the removal or re-arrangement of landmarks has no effect on the beetle’s orientation precision. Celestial compass cues dominate straight-line orientation in dung beetles so strongly that, under heavily overcast conditions or when prevented from seeing the sky, the beetles can no longer orient along straight paths. To our knowledge, this is the only animal with a visual compass system that ignores the extra orientation precision that landmarks can offer.

The role of the sun in the celestial compass of dung beetles.

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 16° at solar elevations below 60° to an error of 29° at solar elevations above 75°. 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.

Night sky orientation with diurnal and nocturnal eyes: dim-light adaptations are critical when the moon is out of sight

The visual systems of many animals feature energetically costly specializations to enable them to function in dim light. It is often unclear, however, how large the behavioural benefit of these specializations is, because a direct comparison in a behaviourally relevant task between closely related day- and night-active species is not usually possible. Here we compared the orientation performance of diurnal and nocturnal species of dung beetles, Scarabaeus (Kheper) lamarcki and Scarabaeus satyrus, respectively, attempting to roll dung balls along straight paths both during the day and at night. Using video tracking, we quantified the straightness of paths and the repeatability of roll bearings as beetles exited a flat arena in their natural habitat or under controlled conditions indoors. Both species oriented equally well when either the moon or an artificial point light source was available, but when the view of the moon was blocked and only wide-field cues such as the lunar polarization pattern or the stars were available for orientation, nocturnal beetles were oriented substantially better. We found no evidence that ball-rolling speed changed with light level, which suggests little or no temporal summation in the visual system. Finally, we found that both diurnal and nocturnal beetles tended to choose bearings that led them towards a bright light source, but away from a dim one. Our results show that even diurnal insects, at least those with superposition eyes, could orient by the light of the moon, but that dim-light adaptations are needed for precise orientation when the moon is not visible. (Less)

Dung beetles use their dung ball as a mobile thermal refuge

At midday, surface temperatures in the desert often exceed 60°C. To be active at this time, animals need extraordinary behavioural or physiological adaptations. Desert ants, for instance, spend up to 75% of their foraging time cooling down on elevated thermal refuges such as grass stalks. Ball-rolling dung beetles work under similar thermal conditions in South African savannahs. After landing at a fresh dung pile, a beetle quickly forms a dung ball and rolls it away in a straight line, head down, walking backwards. Earlier studies have shown that some dung beetles maintain an elevated body temperature to gain a competitive advantage, and that heat shunting may prevent overheating during flight. However, we know little about the behavioural strategies beetles might employ to mitigate heat stress while rolling their dung balls. Using infrared thermography and behavioural experiments, we show here that dung beetles use their dung ball as a mobile thermal refuge onto which they climb to cool down while rolling across hot soil. We further demonstrate that the moist ball functions not only as a portable platform, but also as a heat sink, which effectively cools the beetle as it rolls or climbs onto it.

A new galloping gait in an insect

An estimated three million insect species all walk using variations of the alternating tripod gait [1]. At any one time, these animals hold one stable triangle of legs steady while swinging the opposite triangle forward. Here, we report the discovery that three different flightless desert dung beetles use an additional gallop-like gait, which has never been described in any insect before. Like a bounding hare, the beetles propel their body forward by synchronously stepping with both middle legs and then both front legs. Surprisingly, this peculiar galloping gait delivers lower speeds than the alternating tripod gait. Why these beetles have shifted so radically away from the most widely used walking style on our planet is as yet unknown.

Flicker is part of a multi-cue response criterion in fiddler crab predator avoidance

SUMMARY Predator avoidance behaviour costs time, energy and opportunities, and prey animals need to balance these costs with the risk of predation. The decisions necessary to strike this balance are often based on information that is inherently imperfect and incomplete because of the limited sensory capabilities of prey animals. Our knowledge, however, about how prey animals solve the challenging task of restricting their responses to the most dangerous stimuli in their environment is very limited. Using dummy predators, we examined the contribution of visual flicker to the predator avoidance response of the fiddler crab Uca vomeris. The results illustrate that crabs let purely black or purely white dummies approach significantly closer than black-and-white flickering dummies. We show that this effect complements other factors that modulate escape timing such as retinal speed and the crabs distance to its burrow, and is therefore not due exclusively to an earlier detection of the flickering signal. By combining and adjusting a range of imperfect response criteria in a way that relates to actual threats in their natural environment, prey animals may be able to measure risk and adjust their responses more efficiently, even under difficult or noisy sensory conditions.