Monarch butterflies memorize the spatial location of a food source.

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 and retrieve the spatial location of a food source. We placed several visually identical feeders in a flight cage, with only one feeder providing sucrose solution. Across multiple days, individual butterflies predominantly visited the rewarding feeder. Next, we displaced a salient landmark close to the feeders to test which visual cue the butterflies used to relocate the rewarding feeder. While occasional landmark displacements were ignored by the butterflies and did not affect their decisions, systematic displacement of both the landmark and the rewarding feeder demonstrated that the butterflies associated the salient landmark with the feeder's position. Altogether, we show that butterflies consolidate and retrieve spatial memory in the context of foraging.

Glyphosate impairs aversive learning in bumblebees.

Agrochemicals represent prominent anthropogenic stressors contributing to the ongoing global insect decline. While their impact is generally assessed in terms of mortality rates, non-lethal effects on fitness are equally important to insect conservation. Glyphosate, a commonly used herbicide, is toxic to many animal species, and thought to impact a range of physiological functions. In this study, we investigate the impact of long-term exposure to glyphosate on locomotion, phototaxis and learning abilities in bumblebees, using a fully automated high-throughput assay. We find that glyphosate exposure had a very slight and transient impact on locomotion, while leaving the phototactic drive unaffected. Glyphosate exposure also reduced attraction towards UV light when blue was given as an alternative and, most strikingly, impaired learning of aversive stimuli. Thus, glyphosate had specific actions on sensory and cognitive processes. These non-lethal perceptual and cognitive impairments likely represent a significant obstacle to foraging and predator avoidance for wild bumblebees exposed to glyphosate. Similar effects in other species could contribute to a widespread reduction in foraging efficiency across ecosystems, driven by the large-scale application of this herbicide. The high-throughput paradigm presented in this study can be adapted to investigate sublethal effects of other agrochemicals on bumblebees or other important pollinator species, opening up a critical new avenue for the study of anthropogenic stressors.

Walking bumblebees see faster.

The behavioural state of animals has profound effects on neuronal information processing. Locomotion changes the response properties of visual interneurons in the insect brain, but it is still unknown if it also alters the response properties of photoreceptors. Photoreceptor responses become faster at higher temperatures. It has therefore been suggested that thermoregulation in insects could improve temporal resolution in vision, but direct evidence for this idea has so far been missing. Here, we compared electroretinograms from the compound eyes of tethered bumblebees that were either sitting or walking on an air-supported ball. We found that the visual processing speed strongly increased when the bumblebees were walking. By monitoring the eye temperature during recording, we saw that the increase in response speed was in synchrony with a rise in eye temperature. By artificially heating the head, we show that the walking-induced temperature increase of the visual system is sufficient to explain the rise in processing speed. We also show that walking accelerates the visual system to the equivalent of a 14-fold increase in light intensity. We conclude that the walking-induced rise in temperature accelerates the processing of visual information-an ideal strategy to process the increased information flow during locomotion.

The balbyter ant Camponotus fulvopilosus combines several navigational strategies to support homing when foraging in the close vicinity of its nest.

Many insects rely on path integration to define direct routes back to their nests. When shuttling hundreds of meters back and forth between a profitable foraging site and a nest, navigational errors accumulate unavoidably in this compass- and odometer-based system. In familiar terrain, terrestrial landmarks can be used to compensate for these errors and safely guide the insect back to its nest with pin-point precision. In this study, we investigated the homing strategies employed by Camponotus fulvopilosus ants when repeatedly foraging no more than 1.25 m away from their nest. Our results reveal that the return journeys of the ants, even when setting out from a feeder from which the ants could easily get home using landmark information alone, are initially guided by path integration. After a short run in the direction given by the home vector, the ants then switched strategies and started to steer according to the landmarks surrounding their nest. We conclude that even when foraging in the close vicinity of its nest, an ant still benefits from its path-integrated vector to direct the start of its return journey.

The interplay of directional information provided by unpolarised and polarised light in the heading direction network of the diurnal dung beetle Kheper lamarcki.

The sun is the most prominent source of directional information in the heading direction network of the diurnal, ball-rolling dung beetle Kheper lamarcki. If this celestial body is occluded from the beetle's field of view, the distribution of the relative weight between the directional cues that remain shifts in favour of the celestial pattern of polarised light. In this study, we continue to explore the interplay of the sun and polarisation pattern as directional cues in the heading direction network of K. lamarcki. By systematically altering the intensity and degree of the two cues, we effectively change the relative reliability as they appear to the dung beetle. The response of the beetle to these modifications allows us to closely examine how the weighting relationship of these two sources of directional information is influenced and altered in the heading direction network of the beetle. We conclude that the process by which K. lamarcki relies on directional information is very likely done based on Bayesian reasoning, where directional information conveying the highest certainty at a particular moment is afforded the greatest weight.

Light pollution forces a change in dung beetle orientation behavior.

Increasing global light pollution1,2 threatens the night-time darkness to which most animals are adapted. Light pollution can have detrimental effects on behavior,3-5 including by disrupting the journeys of migratory birds,5,6 sand hoppers,7-9 and moths.10 This is particularly concerning, since many night-active species rely on compass information in the sky, including the moon,11,12 the skylight polarization pattern,13,14 and the stars,15 to hold their course. Even animals not directly exposed to streetlights and illuminated buildings may still experience indirect light pollution in the form of skyglow,3,4 which can extend far beyond urban areas.1,2 While some recent research used simulated light pollution to estimate how skyglow may affect orientation behavior,7-9 the consequences of authentic light pollution for celestial orientation have so far been neglected. Here, we present the results of behavioral experiments at light-polluted and dark-sky sites paired with photographic measurements of each environment. We find that light pollution obscures natural celestial cues and induces dramatic changes in dung beetle orientation behavior, forcing them to rely on bright earthbound beacons in place of their celestial compass. This change in behavior results in attraction toward artificial lights, thereby increasing inter-individual competition and reducing dispersal efficiency. For the many other species of insect, bird, and mammal that rely on the night sky for orientation and migration, these effects could dramatically hinder their vital night-time journeys.

Sex differences in lower extremity kinematics during overhead and single leg squat tests.

The Overhead Squat (OHS) and Single-Leg Squat (SLS) are two clinical tests used by practitioners to identify high-risk biomechanical movement patterns. Several published studies have reported sex differences in SLS performance; however, few have investigated variations during the OHS and none has measured kinematics with a marker-less motion capture system. Therefore, this study aimed to compare biomechanical movement patterns between male and female collegiate athletes during OHS and SLS testing. Seventy-five females and 58 male athletes completed OHS and SLS . A Microsoft Kinect sensor using Athletic Movement Assessment software (PhysiMax®) was used to measure kinematics. For the OHS, males displayed greater peak knee frontal plane projection angles (FPPA) (M:26°±10°, F:20°±8°; P < 0.05), peak hip flexion (M:-94°±14°, F:-87°±15°; P < 0.05), and peak trunk flexion angles (M:11°±11°, F:6°±9°; P < 0.05). For the SLS (dominant-limb), males displayed greater peak trunk flexion (M:32°±6°, F:27°±7°; P < 0.05). For the non-dominant limb, females displayed greater peak knee FPPA (F:-12°±9°, M:-8°±9°; P < 0.05) whereas males displayed greater peak trunk flexion angles (M:32°±5°, F:27°±7°; P < 0.05). These findings suggest the need for practitioners to develop sex-specific corrective exercise programmes in effort to improve lower extremity kinematics in athletes.

Chicken colour discrimination depends on background colour.

How well can a bird discriminate between two red berries on a green background? The absolute threshold of colour discrimination is set by photoreceptor noise, but animals do not perform at this threshold; their performance can depend on additional factors. In humans and zebra finches, discrimination thresholds for colour stimuli depend on background colour, and thus the adaptive state of the visual system. We have tested how well chickens can discriminate shades of orange or green presented on orange or green backgrounds. Chickens discriminated slightly smaller colour differences between two stimuli presented on a similarly coloured background, compared with a background of very different colour. The slope of the psychometric function was steeper when stimulus and background colours were similar but shallower when they differed markedly, indicating that background colour affects the certainty with which the animals discriminate the colours. The effect we find for chickens is smaller than that shown for zebra finches. We modelled the response to stimuli using Bayesian and maximum likelihood estimation and implemented the psychometric function to estimate the effect size. We found that the result is independent of the psychophysical method used to evaluate the effect of experimental conditions on choice performance.

Spatial orientation based on multiple visual cues in non-migratory monarch butterflies.

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 indicates that the migratory butterflies also attend to the panorama to guide their travels. Although the compass has been studied in detail in migrating butterflies, little is known about the orientation abilities of non-migrating butterflies. Here, we investigated whether non-migrating butterflies - which stay in a more restricted area to feed and breed - also use a similar compass system to guide their flights. Performing behavioral experiments on tethered flying butterflies in an indoor LED flight simulator, we found that the monarchs fly along straight tracks with respect to a simulated sun. When a panoramic skyline was presented as the only orientation cue, the butterflies maintained their flight direction only during short sequences, suggesting that they potentially use it for flight stabilization. We further found that when we presented the two cues together, the butterflies incorporate both cues in their compass. Taken together, we show here that non-migrating monarch butterflies can combine multiple visual cues for robust orientation, an ability that may also aid them during their migration.

Multimodal cue integration in the dung beetle compass.

South African ball-rolling dung beetles exhibit a unique orientation behavior to avoid competition for food: after forming a piece of dung into a ball, they efficiently escape with it from the dung pile along a straight-line path. To keep track of their heading, these animals use celestial cues, such as the sun, as an orientation reference. Here we show that wind can also be used as a guiding cue for the ball-rolling beetles. We demonstrate that this mechanosensory compass cue is only used when skylight cues are difficult to read, i.e., when the sun is close to the zenith. This raises the question of how the beetles combine multimodal orientation input to obtain a robust heading estimate. To study this, we performed behavioral experiments in a tightly controlled indoor arena. This revealed that the beetles register directional information provided by the sun and the wind and can use them in a weighted manner. Moreover, the directional information can be transferred between these 2 sensory modalities, suggesting that they are combined in the spatial memory network in the beetle's brain. This flexible use of compass cue preferences relative to the prevailing visual and mechanosensory scenery provides a simple, yet effective, mechanism for enabling precise compass orientation at any time of the day.

Orienting to polarized light at night - matching lunar skylight to performance in a nocturnal beetle.

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 reference to the range of degrees of polarization measured in the night sky. An effect of lunar phase on the degree of polarization of skylight was found, with smaller illuminated fractions of the moon's surface corresponding to lower degrees of polarization in the night sky. We found that the South African dung beetle Escarabaeus satyrus can orient to polarized light for a range of degrees of polarization similar to that observed in diurnal insects, reaching a lower threshold between 0.04 and 0.32, possibly as low as 0.11. For degrees of polarization lower than 0.23, as measured on a crescent moon night, orientation performance was considerably weaker than that observed for completely linearly polarized stimuli, but was nonetheless stronger than in the absence of polarized light.

The roles of vision and antennal mechanoreception in hawkmoth flight control.

Flying animals need continual sensory feedback about their body position and orientation for flight control. The visual system provides essential but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter timescales. How the contributions from these two senses are integrated remains an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here, we have investigated the visual-mechanosensory integration in the hawkmoth Macroglossum stellatarum. They represent a large group of insects that use Johnston's organs in their antennae to provide mechanosensory feedback on perturbations in body position. Our experiments show that antennal mechanosensory feedback specifically mediates fast flight manoeuvres, but not slow ones. Moreover, we did not observe compensatory interactions between antennal and visual feedback.

Hermit crabs (Pagurus bernhardus) use visual contrast in self-assessment of camouflage.

Animals can make use of camouflage to reduce the likelihood of visual detection or recognition and thus improve their chances of survival. Background matching, where body colouration is closely matched to the surrounding substrate, is one form of camouflage. Hermit crabs have the opportunity to choose their camouflage independently of body colouration as they inhabit empty gastropod shells, making them ideal to study their choice of camouflage. We used 3D-printed artificial shells of varying contrasts against a grey substrate to test whether hermit crabs prefer shells that they perceive as less conspicuous. Contrast-minimising shells were chosen for Weber contrasts stronger than -0.5. However, in looming experiments, animals responded to contrasts as weak as -0.2, indicating that while they can detect differences between shells and the background, they are only motivated to move into those shells when the alternatives contrast strongly. This suggests a trade-off between camouflage and vulnerability introduced by switching shells.

Correction to: Polarisation vision: overcoming challenges of working with a property of light we barely see.

In "Polarisation vision: overcoming challenges of working with a property of light we barely see" (Foster et al. 2018) we provide a basic description of how Stokes parameters can be estimated and used to calculate the angle of polarisation (AoP).

The sea urchin Diadema africanum uses low resolution vision to find shelter and deter enemies.

Many sea urchins can detect light on their body surface and some species are reported to possess image-resolving vision. Here, we measure the spatial resolution of vision in the long-spined sea urchin Diadema africanum, using two different visual responses: a taxis towards dark objects and an alarm response of spine-pointing towards looming stimuli. For the taxis response we used visual stimuli, which were isoluminant to the background, to discriminate spatial vision from phototaxis. Individual animals were placed in the centre of a cylindrical arena under bright down-welling light, with stimuli of varying angular width placed on the arena wall at alternating directions from the centre. We tracked the direction of movement of individual animals in relation to the stimuli to determine whether the animals oriented towards the stimulus. We found that D. africanum responds by taxis towards isoluminant stimuli with a spatial resolution in the range of 29-69 deg. This corresponds to a theoretical acceptance angle of 38-89 deg, assuming a contrast threshold of 10%. The visual acuity of the alarm response of D. africanum was tested by exposing animals to different sized dark looming and appearing stimuli on a monitor. We found that D. africanum displays a spine-pointing response to appearing black circles of 13-25 deg angular width, corresponding to an acceptance angle of 60-116 deg, assuming the same contrast threshold as above.

Polarisation vision: overcoming challenges of working with a property of light we barely see.

In recent years, the study of polarisation vision in animals has seen numerous breakthroughs, not just in terms of what is known about the function of this sensory ability, but also in the experimental methods by which polarisation can be controlled, presented and measured. Once thought to be limited to only a few animal species, polarisation sensitivity is now known to be widespread across many taxonomic groups, and advances in experimental techniques are, in part, responsible for these discoveries. Nevertheless, its study remains challenging, perhaps because of our own poor sensitivity to the polarisation of light, but equally as a result of the slow spread of new practices and methodological innovations within the field. In this review, we introduce the most important steps in designing and calibrating polarised stimuli, within the broader context of areas of current research and the applications of new techniques to key questions. Our aim is to provide a constructive guide to help researchers, particularly those with no background in the physics of polarisation, to design robust experiments that are free from confounding factors.

How animals follow the stars.

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 may aid in the study of stellar orientation, and suggest how field experiments may be used to characterize the mechanisms underlying stellar orientation.

Stellar performance: mechanisms underlying Milky Way orientation in dung beetles.

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 discussed in the context of studies of stellar orientation in migratory birds and itinerant seals.This article is part of the themed issue 'Vision in dim light'.

A Snapshot-Based Mechanism for Celestial Orientation.

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. We also find that the beetles are able to maintain their bearing with respect to the presented cues only if the cues are visible when the snapshot is taken. This happens during the "dance," a behavior in which the beetle climbs on top of its ball and rotates about its vertical axis [11]. This strategy for reading celestial signals is a simple but efficient mechanism for straight-line orientation.

Spectral information as an orientation cue in dung beetles.

During the day, a non-uniform distribution of long and short wavelength 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 them with monochromatic (green and UV) light spots in an indoor arena. Beetles kept their original bearing when presented with a single light cue, green or UV, or when presented with both light cues set 180° apart. When either the UV or the green light was turned off after the beetles had set their bearing in the presence of both cues, they were still able to maintain their original bearing to the remaining light. However, if the beetles were presented with two identical green light spots set 180° apart, their ability to maintain their original bearing was impaired. In summary, our data show that ball-rolling beetles could potentially use the celestial chromatic gradient as a reference for orientation.