Migratory animals can detect and use the Earth's magnetic field for orientation and navigation, sometimes over distances spanning thousands of kilometers. How they do so remains, however, one of the greatest mysteries in all sensory biology. Here, the author reviews the progress made to understand the molecular bases of the animal magnetic sense focusing on insect species, the only species in which genetic studies have so far been possible. The central hypothesis in the field posits that magnetically sensitive radical pairs formed by photoexcitation of cryptochrome proteins are key to animal magnetoreception. The author provides an overview of our current state of knowledge for the involvement of insect light-sensitive type I and light-insensitive type II cryptochromes in this enigmatic sense, and highlights some of the unanswered questions to gain a comprehensive understanding of magnetoreception at the organismal level.
The representation and integration of internal and external cues is crucial for any organism to execute appropriate behaviors. In insects, a highly conserved region of the brain, the central complex (CX), functions in the representation of spatial information and behavioral states, as well as the transformation of this information into desired navigational commands. How does this relatively invariant structure enable the incorporation of information from the diversity of anatomical, behavioral, and ecological niches occupied by insects? Here, we examine the input channels to the CX in the context of their development and evolution. Insect brains develop from ~ 100 neuroblasts per hemisphere that divide systematically to form "lineages" of sister neurons, that project to their target neuropils along anatomically characteristic tracts. Overlaying this developmental tract information onto the recently generated Drosophila "hemibrain" connectome and integrating this information with the anatomical and physiological recording of neurons in other species, we observe neuropil and lineage-specific innervation, connectivity, and activity profiles in CX input channels. We posit that the proliferative potential of neuroblasts and the lineage-based architecture of information channels enable the modification of neural networks across existing, novel, and deprecated modalities in a species-specific manner, thus forming the substrate for the evolution and diversification of insect navigational circuits.
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 simulate an insect's sensory perception of compass cues during navigation. In nature, an insect flight is characterized by abrupt changes in moving direction as well as constant changes in velocity. The influence of such varying cue dynamics on compass coding remains unclear. We performed long-term tetrode recordings from the brain of monarch butterflies to study how central complex neurons respond to different stimulus velocities and directions. As these butterflies derive directional information from the sun during migration, we measured the neural response to a virtual sun. The virtual sun was either presented as a spot that appeared at random angular positions or was rotated around the butterfly at different angular velocities and directions. By specifically manipulating the stimulus velocity and trajectory, we dissociated the influence of angular velocity and direction on compass coding. While the angular velocity substantially affected the tuning directedness, the stimulus trajectory influenced the shape of the angular tuning curve. Taken together, our results suggest that the central complex flexibly adjusts its directional coding to the current stimulus dynamics ensuring a precise compass even under highly demanding conditions such as during rapid flight maneuvers.
The optic flow, i.e., the displacement of retinal images of objects in the environment induced by self-motion, is an important source of spatial information, especially for fast-flying insects. Spatial information over a wide range of distances, from the animal's immediate surroundings over several hundred metres to kilometres, is necessary for mediating behaviours, such as landing manoeuvres, collision avoidance in spatially complex environments, learning environmental object constellations and path integration in spatial navigation. To facilitate the processing of spatial information, the complexity of the optic flow is often reduced by active vision strategies. These result in translations and rotations being largely separated by a saccadic flight and gaze mode. Only the translational components of the optic flow contain spatial information. In the first step of optic flow processing, an array of local motion detectors provides a retinotopic spatial proximity map of the environment. This local motion information is then processed in parallel neural pathways in a task-specific manner and used to control the different components of spatial behaviour. A particular challenge here is that the distance information extracted from the optic flow does not represent the distances unambiguously, but these are scaled by the animal's speed of locomotion. Possible ways of coping with this ambiguity are discussed.
The sensing of chemical cues is essential for several aspects of bivalve biology, such as the detection of food and pheromones. However, little is known about chemical communication systems in bivalves or the possible role of the osphradium as a chemosensory organ. To address this, we adapted an electrophysiological technique extensively used in vertebrates—the electro-olfactogram—to record from the osphradium in the Pacific oyster, Magallana gigas. This technique was validated using amino acids as stimulants. The osphradium proved to be sensitive to most proteinogenic l-amino acids tested, evoking tonic, negative, concentration-dependent ‘electro-osphradiogram’ (EOsG) voltage responses, with thresholds of detection in the range of 10− 6 to 10− 5 M. Conversely, it was insensitive to l-arginine and l-glutamic acid. The current study supports the hypothesis that the osphradium is, indeed, a chemosensory organ. The ‘electro-osphradiogram’ may prove to be a powerful tool in the isolation and characterization of pheromones and other important chemical cues in bivalve biology.
Flying insects like the honeybee experience the world as a metric layout embedded in a compass, the time-compensated sun compass. The focus of the review lies on the properties of the landscape memory as accessible by data from radar tracking and analyses of waggle dance following. The memory formed during exploration and foraging is thought to be composed of multiple elements, the aerial pictures that associate the multitude of sensory inputs with compass directions. Arguments are presented that support retrieval and use of landscape memory not only during navigation but also during waggle dance communication. I argue that bees expect landscape features that they have learned and that are retrieved during dance communication. An intuitive model of the bee’s navigation memory is presented that assumes the picture memories form a network of geographically defined locations, nodes. The intrinsic components of the nodes, particularly their generalization process leads to binding structures, the edges. In my view, the cognitive faculties of landscape memory uncovered by these experiments are best captured by the term cognitive map.
Honeybee comb architecture and the manner of its construction have long been the subject of scientific curiosity. Comb is characterised by an even hexagonal layout and the sharing of cell bases and side walls, which provides maximised storage volume while requiring minimal wax. The efficiency of this structure relies on a regular layout and the correct positioning of cells relative to each other, with each new cell placed at the junction of two previously constructed cells. This task is complicated by the incomplete nature of cells at the edge of comb, where new cells are to be built. We presented bees with wax stimuli comprising shallow depressions and protuberances in simulation of features found within partially formed comb, and demonstrated that construction work by honeybee builders was influenced by these stimuli. The building of new cells was aligned to concave stimuli that simulated the clefts that naturally appear between two partially formed cells, revealing how new cells may be aligned to ensure proper tessellation within comb. We also found that bees built cell walls in response to edges formed by our stimuli, suggesting that cell and wall construction was specifically directed towards the locations necessary for continuation of hexagonal comb.
In this special issue of articles from leading neuroethologists—all of whom gave outstanding presentations within the Presidential Symposium of the 2022 International Congress of Neuroethology held in Lisbon, Portugal—we learn about the role of cryptochrome molecules in the magnetic sense of animals, how honeybees construct their honeycombs, why fish eyes are built the way they are in species from different depths, how archerfish intercept their newly downed prey with a swift muscular curving of the body (known as a C-start) and how birds process optic flow information to control flight. Each contribution showcases how nervous systems have evolved to control behaviour, the raison d’être of neuroethology.
Polarization vision is used by a wide range of animals for navigating, orienting, and detecting objects or areas of interest. Shallow marine and semi-terrestrial crustaceans are particularly well known for their abilities to detect predator-like or conspecific-like objects based on their polarization properties. On land, some terrestrial invertebrates use polarization vision for detecting suitable habitats, oviposition sites or conspecifics, but examples of threat detection in the polarization domain are less well known. To test whether this also applies to crustaceans that have evolved to occupy terrestrial habitats, we determined the sensitivity of two species of land and one species of marine hermit crab to predator-like visual stimuli varying in the degree of polarization. All three species showed an ability to detect these cues based on polarization contrasts alone. One terrestrial species, Coenobita rugosus , showed an increased sensitivity to objects with a higher degree of polarization than the background. This is the inverse of most animals studied to date, suggesting that the ecological drivers for polarization vision may be different in the terrestrial environment.
Representatives of arthropods, the largest animal phylum, occupy terrestrial, aquatic, arboreal, and subterranean niches. Their evolutionary success depends on specific morphological and biomechanical adaptations related to their materials and structures. Biologists and engineers have become increasingly interested in exploring these natural solutions to understand relationships between structures, materials, and their functions in living organisms. The aim of this special issue is to present the state-of-the-art research in this interdisciplinary field using modern methodology, such as imaging techniques, mechanical testing, movement capture, and numerical modeling. It contains nine original research reports covering diverse topics, including flight, locomotion, and attachment of the arthropods. The research achievements are essential not only to understand ecological adaptations, and evolutionary and behavioral traits, but also to drive prominent advances for engineering from exploitation of numerous biomimetic ideas.
At the start of a journey home or to a foraging site, ants often stop, interrupting their forward movement, turn on the spot a number of times, and fixate in different directions. These scanning bouts are thought to provide visual information for choosing a path to travel. The temporal organization of such scanning bouts has implications about the neural organisation of navigational behaviour. We examined (1) the temporal distribution of the start of such scanning bouts and (2) the dynamics of saccadic body turns and fixations that compose a scanning bout in Australian desert ants, Melophorus bagoti, as they came out of a walled channel onto open field at the start of their homeward journey. Ants were caught when they neared their nest and displaced to different locations to start their journey home again. The observed parameters were mostly similar across familiar and unfamiliar locations. The turning angles of saccadic body turning to the right or left showed some stereotypy, with a peak just under 45°. The direction of such saccades appears to be determined by a slow oscillatory process as described in other insect species. In timing, however, both the distribution of inter-scanning-bout intervals and individual fixation durations showed exponential characteristics, the signature for a random-rate or Poisson process. Neurobiologically, therefore, there must be some process that switches behaviour (starting a scanning bout or ending a fixation) with equal probability at every moment in time. We discuss how chance events in the ant brain that occasionally reach a threshold for triggering such behaviours can generate the results.
The cover images of the 2023 issues of the Journal of Comparative Physiology A, as well as its logo image, are presented at full size and high resolution, together with the stories behind them. These images are testament to the artistic quality of the scientific illustrations published in the Journal of Comparative Physiology A.
Most insects can detect the pattern of polarized light in the sky with the dorsal rim area in their compound eyes and use this visual information to navigate in their environment by means of 'celestial' polarization vision. 'Non-celestial polarization vision', in contrast, refers to the ability of arthropods to analyze polarized light by means of the 'main' retina, excluding the dorsal rim area. The ability of using the main retina for polarization vision has been attracting sporadic, but steady attention during the last decade. This special issue of the Journal of Comparative Physiology A presents recent developments with a collection of seven original research articles, addressing different aspects of non-celestial polarization vision in crustaceans and insects. The contributions cover different sources of linearly polarized light in nature, the underlying retinal and neural mechanisms of object detection using polarization vision and the behavioral responses of arthropods to polarized reflections from water.
Eyes in low-light environments typically must balance sensitivity and spatial resolution. Vertebrate eyes with large "pixels" (e.g., retinal ganglion cells with inputs from many photoreceptors) will be sensitive but provide coarse vision. Small pixels can render finer detail, but each pixel will gather less light, and thus have poor signal relative-to-noise, leading to lower contrast sensitivity. This balance is particularly critical in oceanic species at mesopelagic depths (200–1000 m) because they experience low light and live in a medium that significantly attenuates contrast. Depending on the spatial frequency and inherent contrast of a pattern being viewed, the viewer’s pupil size and temporal resolution, and the ambient light level and water clarity, a visual acuity exists that maximizes the distance at which the pattern can be discerned. We develop a model that predicts this acuity for common conditions in the open ocean, and compare it to visual acuity in marine teleost fishes and elasmobranchs found at various depths in productive and oligotrophic waters. Visual acuity in epipelagic and upper mesopelagic species aligned well with model predictions, but species at lower mesopelagic depths (> 600 m) had far higher measured acuities than predicted. This is consistent with the prediction that animals found at lower mesopelagic depths operate in a visual world consisting primarily of bioluminescent point sources, where high visual acuity helps localize targets of this kind. Overall, the results suggest that visual acuity in oceanic fish and elasmobranchs is under depth-dependent selection for detecting either extended patterns or point sources.
Avian flight is guided by optic flow—the movement across the retina of images of surfaces and edges in the environment due to self-motion. In all vertebrates, there is a short pathway for optic flow information to reach pre-motor areas: retinal-recipient regions in the midbrain encode optic flow, which is then sent to the cerebellum. One well-known role for optic flow pathways to the cerebellum is the control of stabilizing eye movements (the optokinetic response). However, the role of this pathway in controlling locomotion is less well understood. Electrophysiological and tract tracing studies are revealing the functional connectivity of a more elaborate circuit through the avian cerebellum, which integrates optic flow with other sensory signals. Here we review the research supporting this framework and identify the cerebellar output centres, the lateral (CbL) and medial (CbM) cerebellar nuclei, as two key nodes with potentially distinct roles in flight control. The CbM receives bilateral optic flow information and projects to sites in the brainstem that suggest a primary role for flight control over time, such as during forward flight. The CbL receives monocular optic flow and other types of visual information. This site provides feedback to sensory areas throughout the brain and has a strong projection the nucleus ruber, which is known to have a dominant role in forelimb muscle control. This arrangement suggests primary roles for the CbL in the control of wing morphing and for rapid maneuvers.
A very quick decision enables hunting archerfish to secure downed prey even when they are heavily outnumbered by competing other surface-feeding fish. Based exclusively on information that is taken briefly after the onset of prey motion, the fish select a rapid C-start that turns them right towards the later point of catch. Moreover, the C-start, and not later fin strokes, already lends the fish the speed needed to arrive at just the right time. The archerfish predictive C-starts are kinematically not distinguishable from escape C-starts made by the same individual and are among the fastest C-starts known in teleost fish. The start decisions allow the fish-for ballistically falling prey-to respond accurately to any combination of the initial variables of prey movement and for any position and orientation of the responding fish. The start decisions do not show a speed-accuracy tradeoff and their accuracy is buffered against substantial changes of environmental parameters. Here, I introduce key aspects of this high-speed decision that combines speed, complexity, and precision in an unusual way.
Many insects detect water bodies by observing the linearly polarised light which is reflected from the water surface. Polarotactic horseflies exhibit acrobatic manoeuvres above the water and are able to plunge on its surface, collect a droplet and fly away. This behaviour is extremely fast and has not yet been analysed. We recorded the flight patterns and kinematics of drinking horseflies using a pair of high-speed cameras. The animals of both sexes are attracted to water puddles where they make short, millisecond pitstops to collect a droplet of water that is then presumably drank "on the wing". Before the collection, the flies perform several low-altitude flybys above the puddle. After a few passes, the fly suddenly reverses its body orientation, decelerates, briefly touches the water surface and immediately flies away, usually with a droplet carried between its front legs. During the approach flight, the horseflies fly low but do not show any angular preference. Thus, they view the reflections from the sky, sun, or vegetation with a wide band of ventral ommatidia. Polarotaxis in drinking horseflies is a very robust visually guided behaviour, which operates at a broad range of intensities and various spectral compositions of reflected light.
Natural scene analysis has been extensively used to understand how the invariant structure of the visual environment may have shaped biological image processing strategies. This paper deals with four crucial, but hitherto largely neglected aspects of natural scenes: (1) the viewpoint of specific animals; (2) the fact that image statistics are not independent of the position within the visual field; (3) the influence of the direction of illumination on luminance, spectral and polarization contrast in a scene; and (4) the biologically relevant information content of natural scenes. To address these issues, I recorded the spatial distribution of light in a tropical mudflat with a spectrographic imager equipped with a polarizing filter in an attempt to describe quantitatively the visual environment of fiddler crabs. The environment viewed by the crabs has a distinct structure. Depending on the position of the sun, the luminance, the spectral composition, and the polarization characteristics of horizontal light distribution are not uniform. This is true for both skylight and for reflections from the mudflat surface. The high-contrast feature of the line of horizon dominates the vertical distribution of light and is a discontinuity in terms of luminance, spectral distribution and of image statistics. On a clear day, skylight intensity increases towards the horizon due to multiple scattering, and its spectral composition increasingly resembles that of sunlight. Sky-substratum contrast is highest at short wavelengths. I discuss the consequences of this extreme example of the topography of vision for extracting biologically relevant information from natural scenes.
Hymenopterans, such as bees and wasps, have long fascinated researchers with their sinuous movements at novel locations. These movements, such as loops, arcs, or zigzags, serve to help insects learn their surroundings at important locations. They also allow the insects to explore and orient themselves in their environment. After they gained experience with their environment, the insects fly along optimized paths guided by several guidance strategies, such as path integration, local homing, and route-following, forming a navigational toolkit. Whereas the experienced insects combine these strategies efficiently, the naive insects need to learn about their surroundings and tune the navigational toolkit. We will see that the structure of the movements performed during the learning flights leverages the robustness of certain strategies within a given scale to tune other strategies which are more efficient at a larger scale. Thus, an insect can explore its environment incrementally without risking not finding back essential locations.
