Proceedings of the National Academy of Sciences, 2015
Significance Many animals use the sun or moon and the polarization pattern for navigation. We com... more 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.
We describe here the detection of polarized light by the simple eyes of spiders. Using behavioura... more We describe here the detection of polarized light by the simple eyes of spiders. Using behavioural, morphological, electrophysiological and optical studies, we show that spiders have evolved two different mechanisms to resolve the e-vector of light. Wolf spiders (Lycosidae), are able to turn in response to rotation of a polarized pattern at the zenith of their visual fields, and we also describe a strip in the ventral retina of the principal (anterio-median) eyes that views this location and has receptors tiered into two layers. This provides each pair of receptors with a similar optical solution to that provided by the 'dorsal rim area' of the insect compound eye. In contrast, gnaphosid spiders have evolved a pair of lensless secondary eyes for the detection of polarized light. These two eyes, each sensitive to orthogonal directions of polarization, are perfectly designed to integrate signals from the larger part of the sky and cooperate to analyse the polarization of light...
Simple Summary To escape competition for food at the dung pat, ball-rolling dung beetles shape a ... more Simple Summary To escape competition for food at the dung pat, ball-rolling dung beetles shape a piece of dung into a sphere and roll it away. To maintain their bearing, these beetles integrate directional information from a range of celestial cues. For the majority of diurnal dung beetles living in open habitats, the most dominant of these cues is the sun. It has recently been demonstrated that beetles living in closed habitats, with closely spaced trees and tall grass, rely predominantly on directional information provided by polarised skylight rather than the sun. Taken together, these findings suggests that the orientation strategy of the beetle is influenced by the animal’s visual ecology. To further investigate the relative weighting of cues in the orientation system of beetles, and its relation to their visual ecology, we investigated the orientation strategy of ball-rollers from three different dung beetle tribes, all present within the same savanna biome. We find that speci...
Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction... more Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction are findable, accessible and reusable. To promote an open data culture, we have therefore developed the InsectBrainDatabase (IBdb), a free online platform for insect neuroanatomical and functional data. The IBdb facilitates biological insight by enabling effective cross-species comparisons, by linking neural structure with function, and by serving as general information hub for insect neuroscience. The IBdb allows users to not only effectively locate and visualize data, but to make them widely available for easy, automated reuse via an application programming interface. A unique private mode of the database expands the IBdb functionality beyond public data deposition, additionally providing the means for managing, visualizing, and sharing of unpublished data. This dual function creates an incentive for data contribution early in data management workflows and eliminates the additional ef...
Moving along a straight path is a surprisingly difficult task. This is because, with each ensuing... more 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 direction...
Visually-guided behaviour is constrained by the capacity of the visual system to resolve detail. ... more Visually-guided behaviour is constrained by the capacity of the visual system to resolve detail. This is, in turn, limited by the spatial resolution and contrast sensitivity of the underlying visual system. Because these properties are interdependent and vary non-uniformly, it is only possible to fully understand the limits of a specific visually guided behaviour when they are investigated in combination. To understand the visual limits of flight control in bees, which rely heavily on vision to control flight, and to explore whether they vary between species, we tested how changes in spatial resolution and contrast sensitivity affect the speed and position control of the Asian and European honeybees (Apis cerana and A. mellifera). Despite their apparent similarity, we found some interesting and surprising differences between the visual limits of these species. While the effect of spatial frequency and contrast on position control is similar between the species, ground speed is diffe...
Throughout history, the stars have provided humans with ever more information about our world, en... more 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...
Philosophical transactions of the Royal Society of London. Series B, Biological sciences, Jan 5, 2017
Nocturnal dung beetles (Scarabaeus satyrus) are currently the only animals that have been demonst... more 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 discuss...
Despite their tiny eyes and brains, nocturnal insects have evolved a remarkable capacity to visua... more Despite their tiny eyes and brains, nocturnal insects have evolved a remarkable capacity to visually navigate at night. Whereas some use moonlight or the stars as celestial compass cues to maintain a straight-line course, others use visual landmarks to navigate to and from their nest. These impressive abilities rely on highly sensitive compound eyes and specialized visual processing strategies in the brain.
To make a smooth touchdown when landing, an insect must be able to reliably control its approach ... more To make a smooth touchdown when landing, an insect must be able to reliably control its approach speed as well as its body and leg position-behaviors that are thought to be regulated primarily by visual information. Bumblebees forage and land under a broad range of light intensities and while their behavior during the final moments of landing has been described in detail in bright light, little is known about how this is affected by decreasing light intensity. Here, we investigate this by characterizing the performance of bumblebees, B. terrestris, landing on a flat platform at two different orientations (horizontal and vertical) and at four different light intensities (ranging from 600 lx down to 19 lx). As light intensity decreased, the bees modified their body position and the distance at which they extended their legs, suggesting that the control of landing in these insects is visually mediated. Nevertheless, the effect of light intensity was small and the landings were still we...
The Journal of comparative neurology, Jan 11, 2017
To avoid the fierce competition for food, South African ball-rolling dung beetles carve a piece o... more To avoid the fierce competition for food, South African ball-rolling dung beetles carve a piece of dung off a dung-pile, shape it into a ball and roll it away along a straight line path. For this unidirectional exit from the busy dung pile, at night and day, the beetles use a wide repertoire of celestial compass cues. This robust and relatively easily measurable orientation behavior has made ball-rolling dung beetles an attractive model organism for the study of the neuroethology behind insect orientation and sensory ecology. Although there is already some knowledge emerging concerning how celestial cues are processed in the dung beetle brain, little is known about its general neural layout. Mapping the neuropils of the dung beetle brain is thus a prerequisite to understand the neuronal network that underlies celestial compass orientation. Here, we describe and compare the brains of a day-active and a night-active dung beetle species based on immunostainings against synapsin and ser...
Feces is an abundant, rich source of energy, utilized by a myriad of organisms, not least by memb... more Feces is an abundant, rich source of energy, utilized by a myriad of organisms, not least by members of the order Diptera, i.e., flies. How Drosophila melanogaster reacts to fecal matter remains unclear. Here, we examined oviposition behavior toward a range of fecal samples from mammals native to the putative Southeast African homeland of the fly. We show that D. melanogaster display a strong oviposition aversion toward feces from carnivorous mammals but indifference or even attraction toward herbivore dung. We identify a set of four predictor volatiles, which can be used to differentiate fecal from non-fecal matter, as well as separate carnivore from herbivore feces. Of these volatiles, phenol-indicative of carnivore feces-confers egg-laying aversion and is detected by a single class of sensory neurons expressing Or46a. The Or46a-expressing neurons are necessary and sufficient for oviposition site aversion. We further demonstrate that carnivore feces-unlike herbivore dung-contain a...
Proceedings of the Royal Society B: Biological Sciences, 2016
The ability to move safely between obstacles is critical for animals that fly rapidly through clu... more The ability to move safely between obstacles is critical for animals that fly rapidly through cluttered environments but surprisingly little is known about how they achieve this. Do they reactively avoid obstacles or do they instead fly towards the gaps between them? If they aim towards gaps, what information do they use to detect and fly through them? Here, we aim to answer these questions by presenting orchid bees with different apertures. When negotiating gaps, orchid bees locate and fly close to the point that gives them greatest clearance from the edges. The cue that they use to pinpoint this spot is the brightness gradient formed across the aperture. Furthermore, we find that orchid bees also rely on brightness cues to locate gaps that are sufficiently large to negotiate safely. The advantage of using brightness for locating and negotiating gaps in a cluttered environment is that it provides information about the safest path through obstacles, at least in a forest environment....
In order to protect their food from competitors, ball-rolling dung beetles detach a piece of dung... more 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. ...
Proceedings of the National Academy of Sciences, 2015
Significance Many animals use the sun or moon and the polarization pattern for navigation. We com... more 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.
We describe here the detection of polarized light by the simple eyes of spiders. Using behavioura... more We describe here the detection of polarized light by the simple eyes of spiders. Using behavioural, morphological, electrophysiological and optical studies, we show that spiders have evolved two different mechanisms to resolve the e-vector of light. Wolf spiders (Lycosidae), are able to turn in response to rotation of a polarized pattern at the zenith of their visual fields, and we also describe a strip in the ventral retina of the principal (anterio-median) eyes that views this location and has receptors tiered into two layers. This provides each pair of receptors with a similar optical solution to that provided by the 'dorsal rim area' of the insect compound eye. In contrast, gnaphosid spiders have evolved a pair of lensless secondary eyes for the detection of polarized light. These two eyes, each sensitive to orthogonal directions of polarization, are perfectly designed to integrate signals from the larger part of the sky and cooperate to analyse the polarization of light...
Simple Summary To escape competition for food at the dung pat, ball-rolling dung beetles shape a ... more Simple Summary To escape competition for food at the dung pat, ball-rolling dung beetles shape a piece of dung into a sphere and roll it away. To maintain their bearing, these beetles integrate directional information from a range of celestial cues. For the majority of diurnal dung beetles living in open habitats, the most dominant of these cues is the sun. It has recently been demonstrated that beetles living in closed habitats, with closely spaced trees and tall grass, rely predominantly on directional information provided by polarised skylight rather than the sun. Taken together, these findings suggests that the orientation strategy of the beetle is influenced by the animal’s visual ecology. To further investigate the relative weighting of cues in the orientation system of beetles, and its relation to their visual ecology, we investigated the orientation strategy of ball-rollers from three different dung beetle tribes, all present within the same savanna biome. We find that speci...
Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction... more Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction are findable, accessible and reusable. To promote an open data culture, we have therefore developed the InsectBrainDatabase (IBdb), a free online platform for insect neuroanatomical and functional data. The IBdb facilitates biological insight by enabling effective cross-species comparisons, by linking neural structure with function, and by serving as general information hub for insect neuroscience. The IBdb allows users to not only effectively locate and visualize data, but to make them widely available for easy, automated reuse via an application programming interface. A unique private mode of the database expands the IBdb functionality beyond public data deposition, additionally providing the means for managing, visualizing, and sharing of unpublished data. This dual function creates an incentive for data contribution early in data management workflows and eliminates the additional ef...
Moving along a straight path is a surprisingly difficult task. This is because, with each ensuing... more 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 direction...
Visually-guided behaviour is constrained by the capacity of the visual system to resolve detail. ... more Visually-guided behaviour is constrained by the capacity of the visual system to resolve detail. This is, in turn, limited by the spatial resolution and contrast sensitivity of the underlying visual system. Because these properties are interdependent and vary non-uniformly, it is only possible to fully understand the limits of a specific visually guided behaviour when they are investigated in combination. To understand the visual limits of flight control in bees, which rely heavily on vision to control flight, and to explore whether they vary between species, we tested how changes in spatial resolution and contrast sensitivity affect the speed and position control of the Asian and European honeybees (Apis cerana and A. mellifera). Despite their apparent similarity, we found some interesting and surprising differences between the visual limits of these species. While the effect of spatial frequency and contrast on position control is similar between the species, ground speed is diffe...
Throughout history, the stars have provided humans with ever more information about our world, en... more 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...
Philosophical transactions of the Royal Society of London. Series B, Biological sciences, Jan 5, 2017
Nocturnal dung beetles (Scarabaeus satyrus) are currently the only animals that have been demonst... more 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 discuss...
Despite their tiny eyes and brains, nocturnal insects have evolved a remarkable capacity to visua... more Despite their tiny eyes and brains, nocturnal insects have evolved a remarkable capacity to visually navigate at night. Whereas some use moonlight or the stars as celestial compass cues to maintain a straight-line course, others use visual landmarks to navigate to and from their nest. These impressive abilities rely on highly sensitive compound eyes and specialized visual processing strategies in the brain.
To make a smooth touchdown when landing, an insect must be able to reliably control its approach ... more To make a smooth touchdown when landing, an insect must be able to reliably control its approach speed as well as its body and leg position-behaviors that are thought to be regulated primarily by visual information. Bumblebees forage and land under a broad range of light intensities and while their behavior during the final moments of landing has been described in detail in bright light, little is known about how this is affected by decreasing light intensity. Here, we investigate this by characterizing the performance of bumblebees, B. terrestris, landing on a flat platform at two different orientations (horizontal and vertical) and at four different light intensities (ranging from 600 lx down to 19 lx). As light intensity decreased, the bees modified their body position and the distance at which they extended their legs, suggesting that the control of landing in these insects is visually mediated. Nevertheless, the effect of light intensity was small and the landings were still we...
The Journal of comparative neurology, Jan 11, 2017
To avoid the fierce competition for food, South African ball-rolling dung beetles carve a piece o... more To avoid the fierce competition for food, South African ball-rolling dung beetles carve a piece of dung off a dung-pile, shape it into a ball and roll it away along a straight line path. For this unidirectional exit from the busy dung pile, at night and day, the beetles use a wide repertoire of celestial compass cues. This robust and relatively easily measurable orientation behavior has made ball-rolling dung beetles an attractive model organism for the study of the neuroethology behind insect orientation and sensory ecology. Although there is already some knowledge emerging concerning how celestial cues are processed in the dung beetle brain, little is known about its general neural layout. Mapping the neuropils of the dung beetle brain is thus a prerequisite to understand the neuronal network that underlies celestial compass orientation. Here, we describe and compare the brains of a day-active and a night-active dung beetle species based on immunostainings against synapsin and ser...
Feces is an abundant, rich source of energy, utilized by a myriad of organisms, not least by memb... more Feces is an abundant, rich source of energy, utilized by a myriad of organisms, not least by members of the order Diptera, i.e., flies. How Drosophila melanogaster reacts to fecal matter remains unclear. Here, we examined oviposition behavior toward a range of fecal samples from mammals native to the putative Southeast African homeland of the fly. We show that D. melanogaster display a strong oviposition aversion toward feces from carnivorous mammals but indifference or even attraction toward herbivore dung. We identify a set of four predictor volatiles, which can be used to differentiate fecal from non-fecal matter, as well as separate carnivore from herbivore feces. Of these volatiles, phenol-indicative of carnivore feces-confers egg-laying aversion and is detected by a single class of sensory neurons expressing Or46a. The Or46a-expressing neurons are necessary and sufficient for oviposition site aversion. We further demonstrate that carnivore feces-unlike herbivore dung-contain a...
Proceedings of the Royal Society B: Biological Sciences, 2016
The ability to move safely between obstacles is critical for animals that fly rapidly through clu... more The ability to move safely between obstacles is critical for animals that fly rapidly through cluttered environments but surprisingly little is known about how they achieve this. Do they reactively avoid obstacles or do they instead fly towards the gaps between them? If they aim towards gaps, what information do they use to detect and fly through them? Here, we aim to answer these questions by presenting orchid bees with different apertures. When negotiating gaps, orchid bees locate and fly close to the point that gives them greatest clearance from the edges. The cue that they use to pinpoint this spot is the brightness gradient formed across the aperture. Furthermore, we find that orchid bees also rely on brightness cues to locate gaps that are sufficiently large to negotiate safely. The advantage of using brightness for locating and negotiating gaps in a cluttered environment is that it provides information about the safest path through obstacles, at least in a forest environment....
In order to protect their food from competitors, ball-rolling dung beetles detach a piece of dung... more 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. ...
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