Views from 'crabworld': the spatial distribution of light in a tropical mudflat.

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.

Digger wasps Microbembex monodonta SAY (Hymenoptera, Crabronidae) rely exclusively on visual cues when pinpointing their nest entrances.

The ability of insects to navigate and home is crucial to fundamental tasks, such as pollination, parental care, procuring food, and finding mates. Despite recent advances in our understanding of visual homing in insects, it remains unclear exactly how ground-nesting Hymenoptera are able to precisely locate their often inconspicuous or hidden reproductive burrow entrances. Here we show that the ground-nesting wasp Microbembex monodonta locates her hidden burrow entrance with the help of local landmarks, but only if their view of the wider panorama is not blocked. Moreover, the wasps are able to pinpoint the burrow location to within a few centimeters when potential olfactory, tactile and auditory cues are locally masked. We conclude that M. monodonta locate their hidden burrows relying exclusively on local visual cues in the context of the wider panorama. We discuss these results in the light of the older and more recent literature on nest recognition and homing in insects.

Visual navigation: properties, acquisition and use of views.

Panoramic views offer information on heading direction and on location to visually navigating animals. This review covers the properties of panoramic views and the information they provide to navigating animals, irrespective of image representation. Heading direction can be retrieved by alignment matching between memorized and currently experienced views, and a gradient descent in image differences can lead back to the location at which a view was memorized (positional image matching). Central place foraging insects, such as ants, bees and wasps, conduct distinctly choreographed learning walks and learning flights upon first leaving their nest that are likely to be designed to systematically collect scene memories tagged with information provided by path integration on the direction of and the distance to the nest. Equally, traveling along routes, ants have been shown to engage in scanning movements, in particular when routes are unfamiliar, again suggesting a systematic process of acquiring and comparing views. The review discusses what we know and do not know about how view memories are represented in the brain of insects, how they are acquired and how they are subsequently used for traveling along routes and for pinpointing places.

Camera-based automated monitoring of flying insects in the wild (Camfi). II. flight behaviour and long-term population monitoring of migratory Bogong moths in Alpine Australia.

Introduction: The Bogong moth Agrotis infusa is well known for its remarkable annual round-trip migration from its breeding grounds across eastern and southern Australia to its aestivation sites in the Australian Alps, to which it provides an important annual influx of nutrients. Over recent years, we have benefited from a growing understanding of the navigational abilities of the Bogong moth. Meanwhile, the population of Bogong moths has been shrinking. Recently, the ecologically and culturally important Bogong moth was listed as endangered by the IUCN Red List, and the establishment of a program for long-term monitoring of its population has been identified as critical for its conservation. Methods: Here, we present the results of two years of monitoring of the Bogong moth population in the Australian Alps using recently developed methods for automated wildlife-camera monitoring of flying insects, named Camfi. While in the Alps, some moths emerge from the caves in the evening to undertake seemingly random flights, filling the air with densities in the dozens per cubic metre. The purpose of these flights is unknown, but they may serve an important role in Bogong moth navigation. Results: We found that these evening flights occur throughout summer and are modulated by daily weather factors. We present a simple heuristic model of the arrival to and departure from aestivation sites by Bogong moths, and confirm results obtained from fox-scat surveys which found that aestivating Bogong moths occupy higher elevations as the summer progresses. Moreover, by placing cameras along two elevational transects below the summit of Mt. Kosciuszko, we found that evening flights were not random, but were systematically oriented in directions relative to the azimuth of the summit of the mountain. Finally, we present the first recorded observations of the impact of bushfire smoke on aestivating Bogong moths - a dramatic reduction in the size of a cluster of aestivating Bogong moths during the fire, and evidence of a large departure from the fire-affected area the day after the fire. Discussion: Our results highlight the challenges of monitoring Bogong moths in the wild and support the continued use of automated camera-based methods for that purpose.

Camera-based automated monitoring of flying insects (Camfi). I. Field and computational methods.

The ability to measure flying insect activity and abundance is important for ecologists, conservationists and agronomists alike. However, existing methods are laborious and produce data with low temporal resolution (e.g. trapping and direct observation), or are expensive, technically complex, and require vehicle access to field sites (e.g. radar and lidar entomology). We propose a method called "Camfi" for long-term non-invasive population monitoring and high-throughput behavioural observation of low-flying insects using images and videos obtained from wildlife cameras, which are inexpensive and simple to operate. To facilitate very large monitoring programs, we have developed and implemented a tool for automatic detection and annotation of flying insect targets in still images or video clips based on the popular Mask R-CNN framework. This tool can be trained to detect and annotate insects in a few hours, taking advantage of transfer learning. Our method will prove invaluable for ongoing efforts to understand the behaviour and ecology of declining insect populations and could also be applied to agronomy. The method is particularly suited to studies of low-flying insects in remote areas, and is suitable for very large-scale monitoring programs, or programs with relatively low budgets.

Anesthesia disrupts distance, but not direction, of path integration memory.

Solitary foraging insects, such as ants, maintain an estimate of the direction and distance to their starting location as they move away from it, in a process known as path integration. This estimate, commonly known as the "home vector," is updated continuously as the ant moves1-4 and is reset as soon as it enters its nest,5 yet ants prevented from returning to their nest can still use their home vector when released several hours later.6,7 This conjunction of fast update and long persistence of the home vector memory does not directly map to existing accounts of short-, mid-, and long-term memory;2,8-12 hence, the substrate of this memory remains unknown. Chill-coma anesthesia13-15 has previously been shown to affect associative memory retention in fruit flies14,16 and honeybees.9,17,18 We investigate the nature of path integration memory by anesthetizing ants after they have accumulated home vector information and testing if the memory persists on recovery. We show that after anesthesia the memory of the distance ants have traveled is degraded, but the memory of the direction is retained. We also show that this is consistent with models of path integration that maintain the memory in a redundant Cartesian coordinate system and with the hypothesis that chill-coma produces a proportional reduction of the memory, rather than a subtractive reduction or increase of noise. The observed effect is not compatible with a memory based on recurrent circuit activity and points toward an activity-dependent molecular process as the basis of path integration memory.

The Antarium: A Reconstructed Visual Reality Device for Ant Navigation Research.

We constructed a large projection device (the Antarium) with 20,000 UV-Blue-Green LEDs that allows us to present tethered ants with views of their natural foraging environment. The ants walk on an air-cushioned trackball, their movements are registered and can be fed back to the visual panorama. Views are generated in a 3D model of the ants' environment so that they experience the changing visual world in the same way as they do when foraging naturally. The Antarium is a biscribed pentakis dodecahedron with 55 facets of identical isosceles triangles. The length of the base of the triangles is 368 mm resulting in a device that is roughly 1 m in diameter. Each triangle contains 361 blue/green LEDs and nine UV LEDs. The 55 triangles of the Antarium have 19,855 Green and Blue pixels and 495 UV pixels, covering 360° azimuth and elevation from -50° below the horizon to +90° above the horizon. The angular resolution is 1.5° for Green and Blue LEDs and 6.7° for UV LEDs, offering 65,536 intensity levels at a flicker frequency of more than 9,000 Hz and a framerate of 190 fps. Also, the direction and degree of polarisation of the UV LEDs can be adjusted through polarisers mounted on the axles of rotary actuators. We build 3D models of the natural foraging environment of ants using purely camera-based methods. We reconstruct panoramic scenes at any point within these models, by projecting panoramic images onto six virtual cameras which capture a cube-map of images to be projected by the LEDs of the Antarium. The Antarium is a unique instrument to investigate visual navigation in ants. In an open loop, it allows us to provide ants with familiar and unfamiliar views, with completely featureless visual scenes, or with scenes that are altered in spatial or spectral composition. In closed-loop, we can study the behavior of ants that are virtually displaced within their natural foraging environment. In the future, the Antarium can also be used to investigate the dynamics of navigational guidance and the neurophysiological basis of ant navigation in natural visual environments.

The role of attractive and repellent scene memories in ant homing (Myrmecia croslandi).

Solitary foraging ants rely on vision when travelling along routes and when pinpointing their nest. We tethered foragers of Myrmecia croslandi on a trackball and recorded their intended movements when the trackball was located on their normal foraging corridor (on-route), above their nest and at a location several metres away where they have never been before (off-route). We found that at on- and off-route locations, most ants walk in the nest or foraging direction and continue to do so for tens of metres in a straight line. In contrast, above the nest, ants walk in random directions and change walking direction frequently. In addition, the walking direction of ants above the nest oscillates on a fine scale, reflecting search movements that are absent from the paths of ants at the other locations. An agent-based simulation shows that the behaviour of ants at all three locations can be explained by the integration of attractive and repellent views directed towards or away from the nest, respectively. Ants are likely to acquire such views via systematic scanning movements during their learning walks. The model predicts that ants placed in a completely unfamiliar environment should behave as if at the nest, which our subsequent experiments confirmed. We conclude first, that the ants' behaviour at release sites is exclusively driven by what they currently see and not by information on expected outcomes of their behaviour; and second, that navigating ants might continuously integrate attractive and repellent visual memories. We discuss the benefits of such a procedure.

An insect-inspired model for acquiring views for homing.

Wasps and bees perform learning flights when leaving their nest or food locations for the first time during which they acquire visual information that enables them to return successfully. Here we present and test a set of simple control rules underlying the execution of learning flights that closely mimic those performed by ground-nesting wasps. In the simplest model, we assume that the angle between flight direction and the nest direction as seen from the position of the insect is constant and only flips sign when pivoting direction around the nest is changed, resulting in a concatenation of piecewise defined logarithmic spirals. We then added characteristic properties of real learning flights, such as head saccades and the condition that the nest entrance within the visual field is kept nearly constant to describe the development of a learning flight in a head-centered frame of reference, assuming that the retinal position of the nest is known. We finally implemented a closed-loop simulation of learning flights based on a small set of visual control rules. The visual input for this model are rendered views generated from 3D reconstructions of natural wasp nesting sites, and the retinal nest position is controlled by means of simple template-based tracking. We show that naturalistic paths can be generated without knowledge of the absolute distance to the nest or of the flight speed. We demonstrate in addition that nest-tagged views recorded during such simulated learning flights are sufficient for a homing agent to pinpoint the goal, by identifying nest direction when encountering familiar views. We discuss how the information acquired during learning flights close to the nest can be integrated with long-range homing models.

Cyclic nature of the REM sleep-like state in the cuttlefish Sepia officinalis.

Sleep is a state of immobility characterized by three key criteria: an increased threshold of arousal, rapid reversal to an alert state and evidence of homeostatic 'rebound sleep' in which there is an increase in the time spent in this quiescent state following sleep deprivation. Common European cuttlefish, Sepia officinalis, show states of quiescence during which they meet the last two of these three criteria, yet also show spontaneous bursts of arm and eye movements that accompany rapid changes in chromatophore patterns in the skin. Here, we report that this rapid eye movement sleep-like (REMS-like) state is cyclic in nature. Iterations of the REMS-like state last 2.42±0.22 min (mean±s.e.m.) and alternate with 34.01±1.49 min of the quiescent sleep-like state for durations lasting 176.89±36.71 min. We found clear evidence that this REMS-like state (i) occurs in animals younger than previously reported; (ii) follows an ultradian pattern; (iii) includes intermittent dynamic chromatophore patterning, representing fragments of normal patterning seen in the waking state for a wide range of signaling and camouflage; and (iv) shows variability in the intensity of expression of these skin patterns between and within individuals. These data suggest that cephalopods, which are mollusks with an elaborate brain and complex behavior, possess a sleep-like state that resembles behaviorally the vertebrate REM sleep state, although the exact nature and mechanism of this form of sleep may differ from that of vertebrates.

Insect learning flights and walks.

Knowledge of where things are in one's habitual surroundings cannot be encoded genetically and must be acquired in those surroundings. Many ants, bees and wasps forage from a home base and before doing so learn where resources are to be found and how to return with them to their nest. A significant component of this navigational learning seems to be the acquisition of panoramic views that insects record close to their nests and resource sites and along the paths between these places. Behavioural evidence indicates that these views are retinotopic, meaning, for instance, that an insect knows that it faces along a familiar route, if the image on its retina matches a view that it had previously recorded, when facing in that direction during route learning.

The choreography of learning walks in the Australian jack jumper ant Myrmecia croslandi.

We provide a detailed analysis of the learning walks performed by Myrmecia croslandi ants at the nest during which they acquire visual information on its location. Most learning walks of 12 individually marked naïve ants took place in the morning with a narrow time window separating the first two learning walks, which most often occurred on the same day. Naïve ants performed between two and seven walks over up to four consecutive days before heading out to forage. On subsequent walks, naïve ants tend to explore the area around the nest in new compass directions. During learning walks, ants move along arcs around the nest while performing oscillating scanning movements. In a regular temporal sequence, the ants' gaze oscillates between the nest direction and the direction pointing away from the nest. Ants thus experience a sequence of views roughly across the nest and away from the nest from systematically spaced vantage points around the nest. Further, we show that ants leaving the nest for a foraging trip often walk in an arc around the nest on the opposite side to the intended foraging direction, performing a scanning routine indistinguishable from that of a learning walk. These partial learning walks are triggered by disturbance around the nest and may help returning ants with reorienting when overshooting the nest, which they frequently do. We discuss what is known about learning walks in different ant species and their adaptive significance for acquiring robust navigational memories.

Fractal dimension and the navigational information provided by natural scenes.

Recent work on virtual reality navigation in humans has suggested that navigational success is inversely correlated with the fractal dimension (FD) of artificial scenes. Here we investigate the generality of this claim by analysing the relationship between the fractal dimension of natural insect navigation environments and a quantitative measure of the navigational information content of natural scenes. We show that the fractal dimension of natural scenes is in general inversely proportional to the information they provide to navigating agents on heading direction as measured by the rotational image difference function (rotIDF). The rotIDF determines the precision and accuracy with which the orientation of a reference image can be recovered or maintained and the range over which a gradient descent in image differences will find the minimum of the rotIDF, that is the reference orientation. However, scenes with similar fractal dimension can differ significantly in the depth of the rotIDF, because FD does not discriminate between the orientations of edges, while the rotIDF is mainly affected by edge orientation parallel to the axis of rotation. We present a new equation for the rotIDF relating navigational information to quantifiable image properties such as contrast to show (1) that for any given scene the maximum value of the rotIDF (its depth) is proportional to pixel variance and (2) that FD is inversely proportional to pixel variance. This contrast dependence, together with scene differences in orientation statistics, explains why there is no strict relationship between FD and navigational information. Our experimental data and their numerical analysis corroborate these results.

Diversity and common themes in the organization of ocelli in Hymenoptera, Odonata and Diptera.

We show in a comparative analysis that distinct retinal specializations in insect ocelli are much more common than previously realized and that the rhabdom organization of ocellar photoreceptors is extremely diverse. Hymenoptera, Odonata and Diptera show prominent equatorial fovea-like indentations of the ocellar retinae, where distal receptor endings are furthest removed from the lens surface and receptor densities are highest. In contrast, rhabdomere arrangements are very diverse across insect groups: in Hymenoptera, with some exceptions, pairs of ocellar retinular cells form sheet-like rhabdoms that form elongated rectangular shapes in cross-section, with highly aligned microvilli directions perpendicular to the long axis of cross-sections. This arrangement makes most ocellar retinular cells in Hymenoptera sensitive to the direction of polarized light. In dragonflies, triplets of retinular cells form a y-shaped fused rhabdom with microvilli directions oriented at 60° to each other. In Dipteran ocellar retinular cells microvilli directions are randomised, which destroys polarization sensitivity. We suggest that the differences in ocellar organization between insect groups may reflect the different head attitude control systems that have evolved in these insect groups, but possibly also differences in the mode of locomotion and in the need for celestial compass information.

Quantifying navigational information: The catchment volumes of panoramic snapshots in outdoor scenes.

Panoramic views of natural environments provide visually navigating animals with two kinds of information: they define locations because image differences increase smoothly with distance from a reference location and they provide compass information, because image differences increase smoothly with rotation away from a reference orientation. The range over which a given reference image can provide navigational guidance (its 'catchment area') has to date been quantified from the perspective of walking animals by determining how image differences develop across the ground plane of natural habitats. However, to understand the information available to flying animals there is a need to characterize the 'catchment volumes' within which panoramic snapshots can provide navigational guidance. We used recently developed camera-based methods for constructing 3D models of natural environments and rendered panoramic views at defined locations within these models with the aim of mapping navigational information in three dimensions. We find that in relatively open woodland habitats, catchment volumes are surprisingly large extending for metres depending on the sensitivity of the viewer to image differences. The size and the shape of catchment volumes depend on the distance of visual features in the environment. Catchment volumes are smaller for reference images close to the ground and become larger for reference images at some distance from the ground and in more open environments. Interestingly, catchment volumes become smaller when only above horizon views are used and also when views include a 1 km distant panorama. We discuss the current limitations of mapping navigational information in natural environments and the relevance of our findings for our understanding of visual navigation in animals and autonomous robots.

Sounds of Modified Flight Feathers Reliably Signal Danger in a Pigeon.

In his book on sexual selection, Darwin [1] devoted equal space to non-vocal and vocal communication in birds. Since then, vocal communication has become a model for studies of neurobiology, learning, communication, evolution, and conservation [2, 3]. In contrast, non-vocal "instrumental music," as Darwin called it, has only recently become subject to sustained inquiry [4, 5]. In particular, outstanding work reveals how feathers, often highly modified, produce distinctive sounds [6-9], and suggests that these sounds have evolved at least 70 times, in many orders [10]. It remains to be shown, however, that such sounds are signals used in communication. Here we show that crested pigeons (Ochyphaps lophotes) signal alarm with specially modified wing feathers. We used video and feather-removal experiments to demonstrate that the highly modified 8th primary wing feather (P8) produces a distinct note during each downstroke. The sound changes with wingbeat frequency, so that birds fleeing danger produce wing sounds with a higher tempo. Critically, a playback experiment revealed that only if P8 is present does the sound of escape flight signal danger. Our results therefore indicate, nearly 150 years after Darwin's book, that modified feathers can be used for non-vocal communication, and they reveal an intrinsically reliable alarm signal.

Three-dimensional visualization of ocellar interneurons of the orchid bee Euglossa imperialis using micro X-ray computed tomography.

We used contrast-optimized micro X-ray computed tomography (mCT) to trace the profiles of the full complement of large ocellar L-neurons in the male orchid bee Euglossa imperialis. We find that most L-neurons collect information from either the dorsal or the ventral retinae in both median and lateral ocelli, with only three neurons associated with the median ocellus having dendritic branches in both dorsal and ventral retina. In the median ocellus, we find also L-neurons that either collect information from the left or the right half of the ocellar plexus and two neurons that have a split dendritic tree in both halves. Fourteen large L-neurons collect information from the median ocellus and six to seven L-neurons from each of the lateral ocelli. The only L-neurons that project to the contralateral protocerebrum are those that have their dendritic branches in the ventral plexi of both median and lateral ocelli. The target areas of dorsal L-neurons from the lateral ocelli include a tract of mechanosensory fibers originating in the antennae. We compare our findings with what is known from the ocellar systems of other insects, make a number of functional inferences and discuss the advantages and disadvantages of mCT scans for the purpose of tracing large neuron profiles.

The sensory arrays of the ant, Temnothorax rugatulus.

Individual differences in response thresholds to task-related stimuli may be one mechanism driving task allocation among social insect workers. These differences may arise at various stages in the nervous system. We investigate variability in the peripheral nervous system as a simple mechanism that can introduce inter-individual differences in sensory information. In this study we describe size-dependent variation of the compound eyes and the antennae in the ant Temnothorax rugatulus. Head width in T. rugatulus varies between 0.4 and 0.7 mm (2.6-3.8 mm body length). But despite this limited range of worker sizes we find sensory array variability. We find that the number of ommatidia and of some, but not all, antennal sensilla types vary with head width. The antennal array of T. rugatulus displays the full complement of sensillum types observed in other species of ants, although at much lower quantities than other, larger, studied species. In addition, we describe what we believe to be a new type of sensillum in hymenoptera that occurs on the antennae and on all body segments. T. rugatulus has apposition compound eyes with 45-76 facets per eye, depending on head width, with average lens diameters of 16.5 µm, rhabdom diameters of 5.7 µm and inter-ommatidial angles of 16.8°. The optical system of T. rugatulus ommatidia is severely under focussed, but the absolute sensitivity of the eyes is unusually high. We discuss the functional significance of these findings and the extent to which the variability of sensory arrays may correlate with task allocation.

Regional differences in the preferred e-vector orientation of honeybee ocellar photoreceptors.

In addition to compound eyes, honeybees (Apis mellifera) possess three single-lens eyes called ocelli located on the top of the head. Ocelli are involved in head-attitude control and in some insects have been shown to provide celestial compass information. Anatomical and early electrophysiological studies have suggested that UV and blue-green photoreceptors in ocelli are polarization sensitive. However, their retinal distribution and receptor characteristics have not been documented. Here, we used intracellular electrophysiology to determine the relationship between the spectral and polarization sensitivity of the photoreceptors and their position within the visual field of the ocelli. We first determined a photoreceptor's spectral response through a series of monochromatic flashes (340-600 nm). We found UV and green receptors, with peak sensitivities at 360 and 500 nm, respectively. We subsequently measured polarization sensitivity at the photoreceptor's peak sensitivity wavelength by rotating a polarizer with monochromatic flashes. Polarization sensitivity (PS) values were significantly higher in UV receptors (3.8±1.5, N=61) than in green receptors (2.1±0.6, N=60). Interestingly, most receptors with receptive fields below 35 deg elevation were sensitive to vertically polarized light while the receptors with visual fields above 35 deg were sensitive to a wide range of polarization angles. These results agree well with anatomical measurements showing differences in rhabdom orientations between dorsal and ventral retinae. We discuss the functional significance of the distribution of polarization sensitivities across the visual field of ocelli by highlighting the information the ocelli are able to extract from the bee's visual environment.

How Ants Use Vision When Homing Backward.

Ants can navigate over long distances between their nest and food sites using visual cues [1, 2]. Recent studies show that this capacity is undiminished when walking backward while dragging a heavy food item [3-5]. This challenges the idea that ants use egocentric visual memories of the scene for guidance [1, 2, 6]. Can ants use their visual memories of the terrestrial cues when going backward? Our results suggest that ants do not adjust their direction of travel based on the perceived scene while going backward. Instead, they maintain a straight direction using their celestial compass. This direction can be dictated by their path integrator [5] but can also be set using terrestrial visual cues after a forward peek. If the food item is too heavy to enable body rotations, ants moving backward drop their food on occasion, rotate and walk a few steps forward, return to the food, and drag it backward in a now-corrected direction defined by terrestrial cues. Furthermore, we show that ants can maintain their direction of travel independently of their body orientation. It thus appears that egocentric retinal alignment is required for visual scene recognition, but ants can translate this acquired directional information into a holonomic frame of reference, which enables them to decouple their travel direction from their body orientation and hence navigate backward. This reveals substantial flexibility and communication between different types of navigational information: from terrestrial to celestial cues and from egocentric to holonomic directional memories. VIDEO ABSTRACT.