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March 2022 - March 2025
March 2017 - February 2022
January 2015 - February 2017
Publications
Publications (89)
Every autumn, monarch butterflies migrate from North America to their overwintering sites in Central Mexico. To maintain their southward direction, these butterflies rely on celestial cues as orientation references. The position of the sun combined with additional skylight cues are integrated in the central complex, a region in the butterfly's brai...
For navigation, animals use a robust internal compass. Compass navigation is crucial for long-distance migrating animals like monarch butterflies, which use the sun to navigate over 4,000 km to their overwintering sites every fall. Sun-compass neurons of the central complex have only been recorded in immobile butterflies, and experimental evidence...
Neural processing of a desired moving direction requires the continuous comparison between the current heading and the goal direction. While the neural basis underlying the current heading is well-studied, the coding of the goal direction remains unclear in insects. Here, we used tetrode recordings in tethered flying monarch butterflies to unravel...
Insects are well-known for their ability to keep track of their heading direction based on a combination of skylight cues and visual landmarks. This allows them to navigate back to their nest, disperse throughout unfamiliar environments, as well as migrate over large distances between their breeding and non-breeding habitats. The monarch butterfly...
Significance
We show that South African dung beetles use a multimodal orientation compass based on celestial cues and wind cues to steer across the savanna. The cue preference between these 2 modalities is set in a flexible manner: at low sun elevations, the beetles use a celestially driven compass, but switch to a wind-dominated compass at high su...
Neural circuits have evolved to produce cognitive processes that facilitate a species variable behavioural repertoire. Underlying this variation are evolutionary forces, such as selection, that operate on changes to circuitry against a background of constraints. The interplay between selection and potentially limiting constraints determine how circ...
Butterflies can use reflected linearly polarized light from the wing surface of a conspecific to track down a mating partner or from the surface of leaves to find specific plants while foraging or ovipositing. During all these behavioural tasks, linearly polarized light is detected by the abundant polarization-sensitive photoreceptors in the butter...
Ball-rolling dung beetles orient in some of the most visually challenging habitats on Earth: dark savannahs, forests, and cities. This remarkable ability is guided in part by the directional information extracted from the celestial pattern of linearly polarized light. In this chapter, we first summarize our current understanding of the behavioural...
Spatial memory helps animals to navigate familiar environments. In insects, spatial memory has extensively been studied in central place foragers such as ants and bees. However, if butterflies memorize a spatial location remains unclear. Here, we conducted behavioural experiments to test whether monarch butterflies (Danaus plexippus) can remember a...
Monarch butterflies (Danaus plexippus) have become a superb model system to unravel how the tiny insect brain controls an impressive navigation behavior, such as long-distance migration. Moreover, the ability to compare the neural substrate between migratory and non-migratory Monarch butterflies provides us with an attractive model to specifically...
The central complex is a brain region in the insect brain that houses a neural network specialized to encode directional information. Directional coding has traditionally been investigated with compass cues that revolve in full rotations and at constant angular velocities around the insect’s head. However, these stimulus conditions do not fully sim...
Ants perform oscillating scans of the environment during homing. A new study has shown that this scanning behaviour in ants is controlled by an intrinsic neuronal oscillator, which is modulated by both innate, and learnt visual cues.
Neural processing of a navigational goal requires the continuous comparison between the current heading and the intended goal direction. While the neural basis underlying the current heading is well-studied in insects, the coding of the goal direction is completely unexplored. Here, we identify for the first time neurons that encode goal direction...
Ball rolling dung beetles use a wide range of cues to steer themselves along a fixed bearing, including the spectral gradient of scattered skylight that spans the sky. Here, we define the spectral sensitivity of the diurnal dung beetle Kheper lamarcki and use the information to explore the orientation performance under a range of spectral light com...
Monarch butterflies rely on external cues for orientation during their annual long-distance migration from Northern US and Canada to Central Mexico. These external cues can be celestial cues, such as the sun or polarized light, which are processed in a brain region termed the central complex (CX). Previous research typically focused on how individu...
Multisensory integration plays a central role in perception, as all behaviors usually require the input of different sensory signals. For instance, for a foraging honeybee the association of a food source includes the combination of olfactory and visual cues to be categorized as a flower. Moreover, homing after successful foraging using celestial c...
Monarch butterflies rely on external cues for orientation during their annual long-distance migration from Northern US and Canada to Central Mexico. These external cues can be celestial cues, such as the sun or polarized light, which are processed in the internal compass of the brain, termed the central complex (CX). Previous research typically foc...
Insects are well-known for their ability to keep track of their heading direction based on a combination of skylight cues and visual landmarks. This allows them to navigate back to their nest, disperse throughout unfamiliar environments, as well as migrate over large distances between their breeding and non-breeding habitats. The monarch butterfly...
In recent years, bumblebees have become a prominent insect model organism for a variety of biological disciplines, particularly to investigate learning behaviors as well as visual performance. Understanding these behaviors and their underlying neurobiological principles requires a clear understanding of brain anatomy. Furthermore, to be able to com...
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 enab...
Spatial orientation is essential for all animals that have to successfully change locations during e.g. foraging, homing or migration. Arthropods occupy many different ecological niches and, thus, have evolved a vast number of orientation strategies while moving by air, land, and water. Some of these strategies seem to be rather simple but are perf...
Head direction can be represented in a self-centered egocentric or a viewpoint-invariant allocentric reference frame. Using the most efficient representation is especially crucial for migrating animals, like monarch butterflies ( Danaus plexippus ) that use the sun for orientation. With tetrode recordings from the brain of tethered flying monarch b...
Wind can act as an external cue to control an animal’s heading. A new study reveals the neural mechanisms behind the wind information pathway in the insect brain.
Distant and predictable features in the environment make ideal compass cues to allow movement along a straight path. Ball-rolling dung beetles use a wide range of different signals in the day or night sky to steer themselves along a fixed bearing. These include the sun, the Milky Way, and the polarization pattern generated by the moon. Almost two d...
Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction are findable, accessible and reusable, despite open data mandates by funding bodies. We have therefore developed the InsectBrainDatabase (IBdb), an open platform for depositing, sharing and managing a wide range of insect neuroanatomical and functional...
Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction are findable, accessible and reusable, despite open data mandates by funding bodies. We have therefore developed the InsectBrainDatabase (IBdb), an open platform for depositing, sharing and managing a wide range of insect neuroanatomical and functional...
Neuroscience and ecology are traditionally two very different schools of research. Still today, each discipline is arguably represented by people with directly opposed points of view and daily routines. Anybody can easily picture neuroscientists in white coats dissecting and exploring brain substrate in the lab, or field ecologists in rubber boots...
Unusual amongst dung beetles, Scarabaeus galenus digs a burrow that it provisions by making repeated trips to a nearby dung pile. Even more remarkable is that these beetles return home moving backwards, with a pellet of dung between their hind legs. Here, we explore the strategy that S. galenus uses to find its way home. We find that, like many oth...
A new study shows that mantis shrimp employ path integration, based on celestial and egocentric cues as orientation references, to return to their underwater burrows.
Dragonflies represent an ancient lineage of visual predators, which last shared a common ancestor with insect groups such as dipteran flies in the early Devonian, 406 million years ago [1,2]. Despite their important evolutionary status, and recent interest in them as a model for complex visual physiology and behavior, the most recent detailed descr...
The morphological structure of the nervous system is ultimately the basis of its function. Analyses of the anatomical layout of brain areas, single neuron morphologies, and the synaptic connectivity of neurons are therefore essential for a comprehensive understanding of the computational processes implemented in neuronal networks. Insect brains hav...
Monarch butterflies (Danaus plexippus) are prominent for their annual long-distance migration from North America to their overwintering area in Central Mexico. To find their way on this long journey, they use a sun compass as their main orientation reference but will also adjust their migratory direction with respect to mountain ranges. This indica...
Cataglyphis ants are known for their outstanding navigational abilities. They return to their inconspicuous nest after far‐reaching foraging trips using path integration, and whenever available, learn and memorize visual features of panoramic sceneries. To achieve this, the ants combine directional visual information from celestial cues and panoram...
Cataglyphis ants are known for their outstanding navigational abilities. They return to their inconspicuous nest after far-reaching foraging trips using path integration, and whenever available, learn and memorize visual features of panoramic sceneries. To achieve this, the ants combine directional visual information from celestial cues and panoram...
Monarch butterflies ( Danaus plexippus ) are prominent for their annual long-distance migration from North America to its overwintering area in Central Mexico. To find their way on this long journey, they use a sun compass as their main orientation reference but will also adjust their migratory direction with respect to mountain ranges. This indica...
p>Nasonia, a genus of parasitoid wasps, is a promising model system in the study of developmental and evolutionary genetics, as well as complex traits such as learning. Of these “jewel wasps”, the species Nasonia vitripennis is widely spread and widely studied. To accelerate neuroscientific research in this model species, fundamental knowledge of i...
Each fall, millions of monarch butterflies migrate from North America to their overwintering habitat in Central Mexico (a). These butterflies use celestial cues, such as the sun or polarized light to maintain their southerly direction (b). A neuronal network processes these celestial cues in the butterfly brain, with a brain area, termed the centra...
For many insects, celestial compass cues play an important role in keeping track of their directional headings. One well-investigated group of celestial orientating insects are the African ball-rolling dung beetles. After finding a dung pile, these insects detach a piece, form it into a ball and roll it away along a straight path while facing backw...
Insect migrations are spectacular natural events and resemble a remarkable relocation of biomass between two locations in space. Unlike the well-known migrations of daytime flying butterflies, such as the painted lady (Vanessa cardui) or the monarch butterfly (Danaus plexippus), much less widely known are the migrations of nocturnal moths. These mi...
For polarized light to inform behaviour, the typical range of degrees of polarization observable in the animal's natural environment must be above the threshold for detection and interpretation. Here, we present the first investigation of the degree of linear polarization threshold for orientation behaviour in a nocturnal species, with specific ref...
The modulation of an animal's behavior through external sensory stimuli, previous experience and its internal state is crucial to survive in a constantly changing environment. In most insects, octopamine (OA) and its precursor tyramine (TA) modulate a variety of physiological processes and behaviors by shifting the organism from a relaxed or dorman...
A new study demonstrates that fruit flies can use a sun compass, which is encoded in specific neurons in the fly's brain, to maintain a fixed heading direction for up to six hours.
What do a burly rower, a backstroke swimmer and a hard-working South African dung beetle all have in common? The answer is: they all benefit from moving along a straight path, and do so moving backwards. This, however, is where the similarity ends. While the rower has solved this navigational challenge by handing the task of steering to the coxswai...
Despite their tiny brains, insects show impressive abilities when navigating over short distances during path integration or during migration over thousands of kilometers across entire continents. Celestial compass cues often play an important role as references during navigation. In contrast to many other insects, South African dung beetles rely e...
The modulation of an animal′s behavior through external sensory stimuli, previous experience and its internal state is crucial to survive in a constantly changing environment. In mammals, the adrenergic system modulates a variety of physiological processes and behaviors by shifting the organism from a relaxed or dormant condition to a responsive, e...
For polarized light to inform behaviour, the typical range of degrees of polarization observable in the animal’s natural environment must be above the threshold for detection and interpretation. Here we present the first investigation of the degree of linear polarization threshold for orientation behaviour in a nocturnal species, with specific refe...
A new study provides evidence that fruit flies use path integration to maintain proximity to a food source during their local searches.
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 beetl...
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 eas...
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 unkn...
Nervous tissue is one of the most metabolically expensive animal tissues, thus evolutionary investments that result in enlarged brain regions should also result in improved behavioural performance. Indeed, large-scale comparative studies in vertebrates and invertebrates have successfully linked differences in brain anatomy to differences in ecology...
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 possib...
During the day, a non-uniform distribution of long and shortwavelength light generates a colour gradient across the sky. This gradient could be used as a compass cue, particularly by animals such as dung beetles that rely primarily on celestial cues for orientation. Here,we tested if dung beetles can use spectral cues for orientation by presenting...
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 enco...
Migrating desert locusts, Schistocerca gregaria, are able to use the skylight polarization pattern for navigation. They detect polarized-light with a specialized dorsal rim area in their compound eye. After multistage processing, polarization signals are transferred to the central complex, a midline spanning brain area involved in locomotor control...
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 an their efficient escape from the dung pile, the beetles rely on a celestial compass to move along a straight paths. Here, we analyzed the reliability of different skylight cues for this compass and found that dung beet...
Animals relying on a celestial compass for spatial orientation may use the position of the sun, the chromatic or intensity gradient of the sky, the polarization pattern of the sky, or a combination of these cues as compass signals. Behavioral experiments in bees and ants, indeed, showed that direct sunlight and sky polarization play a role in sky c...
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 doub...
Electromagnetic radiation perceived as light has three properties: it can differ in spectral composition, perceived as colour, intensity, perceived as brightness, and in the plane of oscillation, termed polarization. While most visual systems exploit differences in brightness and colour for visual discrimination, the third attribute, the plane of o...
On hotter soil, beetles occasionally stop, climb onto their ball and perform a particular preening behaviour during which the front legs are repeatedly brought into contact with the beetles’ mouth-parts.
Infrared thermography shows that during each rolling phase, the surface temperature of the beetles’ front legs (protibia) increases by as much as 10°C and then decreases again when the beetle is on the ball.
Each fall, eastern North American monarch butterflies in their northern range undergo a long-distance migration south to their overwintering grounds in Mexico. Migrants use a time-compensated sun compass to determine directionality during the migration. This compass system uses information extracted from sun-derived skylight cues that is compensate...
Papilio butterflies have sophisticated color vision and are potential pollinators for red flowers. Do they innately prefer red flowers? Is their foraging based solely on color? To answer these questions, we presented newly emerged Papilio with four colored disks (blue, green, yellow and red) on an otherwise black floor of a small cage. We defined t...
The characteristic crawling behavior of Drosophila larvae consists of a series of rhythmic waves of peristalsis and episodes of head swinging and turning. The two biogenic amines octopamine and tyramine have recently been shown to modulate various parameters of locomotion, such as muscle contraction, the time spent in pausing or forward locomotion,...
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 [1]. Ball-rolling dung beetles work under similar thermal con...
Many migrating insects rely on the plane of sky polarization as a cue to detect spatial directions. Desert locusts (Schistocerca gregaria), like other insects, perceive polarized light through specialized photoreceptors in a dorsal eye region. Desert locusts occur in two phases: a gregarious swarming phase, which migrates during the day, and a soli...
Although insect brains are small in comparison to those of vertebrates, some species show astonishing navigational abilities. Desert locusts (Schistocerca gregaria) are well-known for forming huge swarms consisting of millions of animals and their long-range migrations throughout North Africa and the Middle East. Experiments on tethered flying locu...
Movie of the 3D reconstructed TIM2 neuron illustrated in Figure 2E. The medulla is shown in transparent grey.
(AVI)
Short movie of the ramification of the TML1 neuron in the medulla (transparent grey) reconstructed in three-dimensions (same neuron as in
Figure 3A and D
).
(AVI)
Movie presenting a 360° vertical rotation of the three-dimensional reconstruction of the TIM1 neuron shown in Figure 2D. The innerved brain areas are shown in transparent grey.
(AVI)
Movie illustrating the three-dimensionally reconstructed MeMe1 neuron of
Figure 4B
and the medullae of both hemispheres (transparent grey) rotating around the vertical axis.
(AVI)
Movie showing a 3D model of the MeMe2 neuron (same as in Figure 4F). Optic lobe neuropils and brain areas of the central brain are shown in transparent grey. Vertical rotation.
(AVI)
Mass migration of desert locusts is a common phenomenon in North Africa and the Middle East but how these insects navigate is still poorly understood. Laboratory studies suggest that locusts are able to exploit the sky polarization pattern as a navigational cue. Like other insects locusts detect polarized light through a specialized dorsal rim area...
Many animals rely on a sun compass for spatial orientation and long-range navigation. In addition to the Sun, insects also exploit the polarization pattern and chromatic gradient of the sky for estimating navigational directions. Analysis of polarization-vision pathways in locusts and crickets has shed first light on brain areas involved in sky com...
The cockroach Leucophaea maderae is an established model in circadian rhythm research. Its circadian clock is located in the accessory medulla of the brain. Pigment-dispersing factor-immunoreactive (PDF-ir) neurons of the accessory medulla act as circadian pacemakers controlling locomotor activity rhythms. To characterize the neuronal network of th...
For spatial orientation and navigation, many insects derive compass information from the polarization pattern of the blue sky. The desert locust Schistocerca gregaria detects polarized light with a specialized dorsal rim area of its compound eye. In the locust brain, polarized-light signals are passed through the anterior optic tract and tubercle t...
DURING METAMORPHOSIS, THE TRANSITION FROM THE LARVA TO THE ADULT, THE INSECT BRAIN UNDERGOES CONSIDERABLE REMODELING: new neurons are integrated while larval neurons are remodeled or eliminated. One well acknowledged model to study metamorphic brain development is the sphinx moth Manduca sexta. To further understand mechanisms involved in the metam...
The red flour beetle Tribolium castaneum is emerging as a further standard insect model beside Drosophila. Its genome is fully sequenced and it is susceptible for genetic manipulations including RNA-interference. We use this beetle to study adult brain development and plasticity primarily with respect to the olfactory system. In the current study,...
Many insects use the pattern of polarized light in the sky for spatial orientation and navigation. We have investigated the polarization vision system in the desert locust. To create a common platform for anatomical studies on polarization vision pathways, Kurylas et al. (2008) have generated a three-dimensional (3D) standard brain from confocal mi...
Lepidopterans like the giant sphinx moth Manduca sexta are known for their conspicuous sexual dimorphism in the olfactory system, which is especially pronounced in the antennae and in the antennal lobe, the primary integration center of odor information. Even minute scents of female pheromone are detected by male moths, facilitated by a huge array...