Visual guidance fine-tunes probing movements of an insect appendage.

Visually guided reaching, a regular feature of human life, comprises an intricate neural control task. It includes identifying the target's position in 3D space, passing the representation to the motor system that controls the respective appendages, and adjusting ongoing movements using visual and proprioceptive feedback. Given the complexity of the neural control task, invertebrates, with their numerically constrained central nervous systems, are often considered incapable of this level of visuomotor guidance. Here, we provide mechanistic insights into visual appendage guidance in insects by studying the probing movements of the hummingbird hawkmoth's proboscis as they search for a flower's nectary. We show that visually guided proboscis movements fine-tune the coarse control provided by body movements in flight. By impairing the animals' view of their proboscis, we demonstrate that continuous visual feedback is required and actively sought out to guide this appendage. In doing so, we establish an insect model for the study of neural strategies underlying eye-appendage control in a simple nervous system.

A Friend in Need Is a Friend Indeed? Analysis of the Willingness to Share Self-Produced Electricity During a Long-lasting Power Outage.

Will private households owning a photovoltaic system share their electricity during a long-lasting power outage? Prior research has shown that our energy systems need to become more resilient by using dispersed energy sources-a role that could well be performed by these private photovoltaic systems, but only if their owners decide to share the produced electricity, and not consume it themselves. Considering the potential of this approach, it is indispensable to better understand incentives and motives that facilitate such cooperative behaviour. Drawing on theories of social dilemmas as well as prosocial behaviour, we hypothesize that both, structural solutions such as increased rewards as well as individual motives such as empathy-elicited altruism and norms predict cooperation. We test these hypotheses against a dataset of 80 households in Germany which were asked about their sharing behaviour towards four different recipient groups. We show that the effectiveness of motives differs significantly across recipient groups: Individual (intrinsic) motivations such as empathy-elicited altruism and altruistic norms serve as a strong predictor for cooperative behaviour towards related recipients as well as critical infrastructure, whereas higher rewards partially even reduce cooperation depending on the donor's social value orientation. For the recipient groups neighbours and public infrastructure, no significant effect for any of the tested incentives is found. Contributing to literature on social dilemmas and energy resilience, these results demonstrate the relevance of individual rather than structural incentives for electricity sharing during a power outage to render our energy provision more resilient. Practical implications for policymakers are given.

Night skies through animals' eyes-Quantifying night-time visual scenes and light pollution as viewed by animals.

A large proportion of animal species enjoy the benefits of being active at night, and have evolved the corresponding optical and neural adaptations to cope with the challenges of low light intensities. However, over the past century electric lighting has introduced direct and indirect light pollution into the full range of terrestrial habitats, changing nocturnal animals' visual worlds dramatically. To understand how these changes affect nocturnal behavior, we here propose an animal-centered analysis method based on environmental imaging. This approach incorporates the sensitivity and acuity limits of individual species, arriving at predictions of photon catch relative to noise thresholds, contrast distributions, and the orientation cues nocturnal species can extract from visual scenes. This analysis relies on just a limited number of visual system parameters known for each species. By accounting for light-adaptation in our analysis, we are able to make more realistic predictions of the information animals can extract from nocturnal visual scenes under different levels of light pollution. With this analysis method, we aim to provide context for the interpretation of behavioral findings, and to allow researchers to generate specific hypotheses for the behavior of nocturnal animals in observed light-polluted scenes.

Allometric scaling of a superposition eye optimizes sensitivity and acuity in large and small hawkmoths.

Animals vary widely in body size within and across species. This has consequences for the function of organs and body parts in both large and small individuals. How these scale, in relation to body size, reveals evolutionary investment strategies, often resulting in trade-offs between functions. Eyes exemplify these trade-offs, as they are limited by their absolute size in two key performance features: sensitivity and spatial acuity. Due to their size polymorphism, insect compound eyes are ideal models for studying the allometric scaling of eye performance. Previous work on apposition compound eyes revealed that allometric scaling led to poorer spatial resolution and visual sensitivity in small individuals, across a range of insect species. Here, we used X-ray microtomography to investigate allometric scaling in superposition compound eyes-the second most common eye type in insects-for the first time. Our results reveal a novel strategy to cope with the trade-off between sensitivity and spatial acuity, as we show that the eyes of the hummingbird hawkmoth retain an optimal balance between these performance measures across all body sizes.

Connectomics: From form to function in butterfly colour vision.

A recent study has revealed how the connectivity of neurons in the lamina of the Asian swallowtail butterfly forms the basis of this insect's exceptional colour vision through two circuit motifs: colour opponency of photoreceptors and broadband colour integration by lamina neurons.

Spatial tuning of translational optic flow responses in hawkmoths of varying body size.

To safely navigate their environment, flying insects rely on visual cues, such as optic flow. Which cues insects can extract from their environment depends closely on the spatial and temporal response properties of their visual system. These in turn can vary between individuals that differ in body size. How optic flow-based flight control depends on the spatial structure of visual cues, and how this relationship scales with body size, has previously been investigated in insects with apposition compound eyes. Here, we characterised the visual flight control response limits and their relationship to body size in an insect with superposition compound eyes: the hummingbird hawkmoth Macroglossum stellatarum. We used the hawkmoths' centring response in a flight tunnel as a readout for their reception of translational optic flow stimuli of different spatial frequencies. We show that their responses cut off at different spatial frequencies when translational optic flow was presented on either one, or both tunnel walls. Combined with differences in flight speed, this suggests that their flight control was primarily limited by their temporal rather than spatial resolution. We also observed strong individual differences in flight performance, but no correlation between the spatial response cutoffs and body or eye size.

Natural image statistics in the dorsal and ventral visual field match a switch in flight behaviour of a hawkmoth.

Many animals use visual cues to navigate their environment. To encode the large input ranges of natural signals optimally, their sensory systems have adapted to the stimulus statistics experienced in their natural habitats1. A striking example, shared across animal phyla, is the retinal tuning to the relative abundance of blue light from the sky, and green light from the ground, evident in the frequency of each photoreceptor type in the two retinal hemispheres2. By adhering only to specific regions of the visual field that contain the relevant information, as for the high-acuity dorsal regions in the eyes of male flies chasing females3, the neural investment can be further reduced. Regionalisation can even lead to activation of the appropriate visual pathway by target location, rather than by stimulus features. This has been shown in fruit flies, which increase their landing attempts when an expanding disc is presented in their frontal visual field, while lateral presentation increases obstacle avoidance responses4. We here report a similar switch in behavioural responses for extended visual scenes. Using a free-flight paradigm, we show that the hummingbird hawkmoth (Macroglossum stellatarum) responds with flight-control adjustments to translational optic-flow cues exclusively in their ventral and lateral visual fields, while identical stimuli presented dorsally elicit a novel directional flight response. This response split is predicted by our quantitative imaging data from natural visual scenes in a variety of habitats, which demonstrate higher magnitudes of translational optic flow in the ventral hemisphere, and the opposite distribution for contrast edges containing directional information.

Wing damage affects flight kinematics but not flower tracking performance in hummingbird hawkmoths.

Wing integrity is crucial to the many insect species that spend distinct portions of their life in flight. How insects cope with the consequences of wing damage is therefore a central question when studying how robust flight performance is possible with such fragile chitinous wings. It has been shown in a variety of insect species that the loss in lift-force production resulting from wing damage is generally compensated by an increase in wing beat frequency rather than amplitude. The consequences of wing damage for flight performance, however, are less well understood, and vary considerably between species and behavioural tasks. One hypothesis reconciling the varying results is that wing damage might affect fast flight manoeuvres with high acceleration, but not slower ones. To test this hypothesis, we investigated the effect of wing damage on the manoeuvrability of hummingbird hawkmoths (Macroglossum stellatarum) tracking a motorised flower. This assay allowed us to sample a range of movements at different temporal frequencies, and thus assess whether wing damage affected faster or slower flight manoeuvres. We show that hummingbird hawkmoths compensate for the loss in lift force mainly by increasing wing beat amplitude, yet with a significant contribution of wing beat frequency. We did not observe any effects of wing damage on flight manoeuvrability at either high or low temporal frequencies.

A new innovative real-time tracking method for flying insects applicable under natural conditions.

BACKGROUND: Sixty percent of all species are insects, yet despite global efforts to monitor animal movement patterns, insects are continuously underrepresented. This striking difference between species richness and the number of species monitored is not due to a lack of interest but rather to the lack of technical solutions. Often the accuracy and speed of established tracking methods is not high enough to record behavior and react to it experimentally in real-time, which applies in particular to small flying animals. RESULTS: Our new method of real-time tracking relates to frequencies of solar radiation which are almost completely absorbed by traveling through the atmosphere. For tracking, photoluminescent tags with a peak emission (1400 nm), which lays in such a region of strong absorption through the atmosphere, were attached to the animals. The photoluminescent properties of passivated lead sulphide quantum dots were responsible for the emission of light by the tags and provide a superb signal-to noise ratio. We developed prototype markers with a weight of 12.5 mg and a diameter of 5 mm. Furthermore, we developed a short wave infrared detection system which can record and determine the position of an animal in a heterogeneous environment with a delay smaller than 10 ms. With this method we were able to track tagged bumblebees as well as hawk moths in a flight arena that was placed outside on a natural meadow. CONCLUSION: Our new method eliminates the necessity of a constant or predictable environment for many experimental setups. Furthermore, we postulate that the developed matrix-detector mounted to a multicopter will enable tracking of small flying insects, over medium range distances (>1000 m) in the near future because: a) the matrix-detector equipped with an 70 mm interchangeable lens weighs less than 380 g, b) it evaluates the position of an animal in real-time and c) it can directly control and communicate with electronic devices.

Hawkmoth lamina monopolar cells act as dynamic spatial filters to optimize vision at different light levels.

How neural form and function are connected is a central question of neuroscience. One prominent functional hypothesis, from the beginnings of neuroanatomical study, states that laterally extending dendrites of insect lamina monopolar cells (LMCs) spatially integrate visual information. We provide the first direct functional evidence for this hypothesis using intracellular recordings from type II LMCs in the hawkmoth Macroglossum stellatarum. We show that their spatial receptive fields broaden with decreasing light intensities, thus trading spatial resolution for higher sensitivity. These dynamic changes in LMC spatial properties can be explained by the density and lateral extent of their dendritic arborizations. Our results thus provide the first physiological evidence for a century-old hypothesis, directly correlating physiological response properties with distinctive dendritic morphology.

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.

The role of lateral optic flow cues in hawkmoth flight control.

Flying animals require sensory feedback on changes of their body position, as well as on their distance from nearby objects. The apparent image motion, or optic flow, which is generated as animals move through the air, can provide this information. Flight tunnel experiments have been crucial for our understanding of how insects use optic flow for flight control in confined spaces. However, previous work mainly focused on species from two insect orders: Hymenoptera and Diptera. We therefore set out to investigate whether the previously described control strategies to navigate enclosed environments are also used by insects with a different optical system, flight kinematics and phylogenetic background. We tested the role of lateral visual cues for forward flight control in the hummingbird hawkmoth Macroglossum stellatarum (Sphingidae, Lepidoptera), which possesses superposition compound eyes, and has the ability to hover in addition to its capacity for fast forward flight. Our results show that hawkmoths use a similar strategy for lateral position control to bees and flies in balancing the magnitude of translational optic flow perceived in both eyes. However, the influence of lateral optic flow on flight speed in hawkmoths differed from that in bees and flies. Moreover, hawkmoths showed individually attributable differences in position and speed control when the presented optic flow was unbalanced.

Fuelling on the wing: sensory ecology of hawkmoth foraging.

Hawkmoths (Lepidoptera, Sphingidae) comprise around 1500 species, most of which forage on nectar from flowers in their adult stage, usually while hovering in front of the flower. The majority of species have a nocturnal lifestyle and are important nocturnal pollinators, but some species have turned to a diurnal lifestyle. Hawkmoths use visual and olfactory cues including CO2 and humidity to detect and recognise rewarding flowers; they find the nectary in the flowers by means of mechanoreceptors on the proboscis and vision, evaluate it with gustatory receptors on the proboscis, and control their hovering flight position using antennal mechanoreception and vision. Here, we review what is presently known about the sensory organs and sensory-guided behaviour that control feeding behaviour of this fascinating pollinator taxon. We also suggest that more experiments on hawkmoth behaviour in natural settings are needed to fully appreciate their sensory capabilities.

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.

Resolving the Trade-off Between Visual Sensitivity and Spatial Acuity-Lessons from Hawkmoths.

The visual systems of many animals, particularly those active during the day, are optimized for high spatial acuity. However, at night, when photons are sparse and the visual signal competes with increased noise levels, fine spatial resolution cannot be sustained and is traded-off for the greater sensitivity required to see in dim light. High spatial acuity demands detectors and successive visual processing units whose receptive fields each cover only a small area of visual space, in order to reassemble a finely sampled and well resolved image. However, the smaller the sampled area, the fewer the photons that can be collected, and thus the worse the visual sensitivity becomes-leading to the classical trade-off between sensitivity and resolution. Nocturnal animals usually resolve this trade-off in favour of sensitivity, and thus have lower spatial acuity than their diurnal counterparts. Here we review results highlighting how hawkmoths, a highly visual group of insects with species active at different light intensities, resolve the trade-off between sensitivity and spatial resolution. We compare adaptations both in the optics and retina, as well as at higher levels of neural processing in a nocturnal and a diurnal hawkmoth species, and also give a perspective on the behavioral consequences. We broaden the scope of our review by drawing comparisons with the adaptive strategies used by other nocturnal and diurnal insects.

Comparative system identification of flower tracking performance in three hawkmoth species reveals adaptations for dim light vision.

Flight control in insects is heavily dependent on vision. Thus, in dim light, the decreased reliability of visual signal detection also prompts consequences for insect flight. We have an emerging understanding of the neural mechanisms that different species employ to adapt the visual system to low light. However, much less explored are comparative analyses of how low light affects the flight behaviour of insect species, and the corresponding links between physiological adaptations and behaviour. We investigated whether the flower tracking behaviour of three hawkmoth species with different diel activity patterns revealed luminance-dependent adaptations, using a system identification approach. We found clear luminance-dependent differences in flower tracking in all three species, which were explained by a simple luminance-dependent delay model, which generalized across species. We discuss physiological and anatomical explanations for the variance in tracking responses, which could not be explained by such simple models. Differences between species could not be explained by the simple delay model. However, in several cases, they could be explained through the addition on a second model parameter, a simple scaling term, that captures the responsiveness of each species to flower movements. Thus, we demonstrate here that much of the variance in the luminance-dependent flower tracking responses of hawkmoths with different diel activity patterns can be captured by simple models of neural processing.This article is part of the themed issue 'Vision in dim light'.

Differential investment in visual and olfactory brain areas reflects behavioural choices in hawk moths.

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 and behaviour, but their precision can be limited by the detail of the anatomical measurements, or by only measuring behaviour indirectly. Therefore, detailed case studies are valuable complements to these investigations, and have provided important evidence linking brain structure to function in a range of higher-order behavioural traits, such as foraging experience or aggressive behaviour. Here, we show that differences in the size of both lower and higher-order sensory brain areas reflect differences in the relative importance of these senses in the foraging choices of hawk moths, as suggested by previous anatomical work in Lepidopterans. To this end we combined anatomical and behavioural quantifications of the relative importance of vision and olfaction in two closely related hawk moth species. We conclude that differences in sensory brain volume in these hawk moths can indeed be interpreted as differences in the importance of these senses for the animal's behaviour.

Neural Summation in the Hawkmoth Visual System Extends the Limits of Vision in Dim Light.

Most of the world's animals are active in dim light and depend on good vision for the tasks of daily life. Many have evolved visual adaptations that permit a performance superior to that of manmade imaging devices [1]. In insects, a major model visual system, nocturnal species show impressive visual abilities ranging from flight control [2, 3], to color discrimination [4, 5], to navigation using visual landmarks [6-8] or dim celestial compass cues [9, 10]. In addition to optical adaptations that improve their sensitivity in dim light [11], neural summation of light in space and time-which enhances the coarser and slower features of the scene at the expense of noisier finer and faster features-has been suggested to improve sensitivity in theoretical [12-14], anatomical [15-17], and behavioral [18-20] studies. How these summation strategies function neurally is, however, presently unknown. Here, we quantified spatial and temporal summation in the motion vision pathway of a nocturnal hawkmoth. We show that spatial and temporal summation combine supralinearly to substantially increase contrast sensitivity and visual information rate over four decades of light intensity, enabling hawkmoths to see at light levels 100 times dimmer than without summation. Our results reveal how visual motion is calculated neurally in dim light and how spatial and temporal summation improve sensitivity while simultaneously maximizing spatial and temporal resolution, thus extending models of insect motion vision derived predominantly from diurnal flies. Moreover, the summation strategies we have revealed may benefit manmade vision systems optimized for variable light levels [21].

Adaptations for nocturnal and diurnal vision in the hawkmoth lamina.

Animals use vision over a wide range of light intensities, from dim starlight to bright sunshine. For animals active in very dim light the visual system is challenged by several sources of visual noise. Adaptations in the eyes, as well as in the neural circuitry, have evolved to suppress the noise and enhance the visual signal, thereby improving vision in dim light. Among neural adaptations, spatial summation of visual signals from neighboring processing units is suggested to increase the reliability of signal detection and thus visual sensitivity. In insects, the likely neural candidates for carrying out spatial summation are the lamina monopolar cells (LMCs) of the first visual processing area of the insect brain (the lamina). We have classified LMCs in three species of hawkmoths with considerably different activity periods but very similar ecology-the diurnal Macroglossum stellatarum, the nocturnal Deilephila elpenor and the crepuscular-nocturnal Manduca sexta. Using this classification, we investigated the anatomical adaptations of hawkmoth LMCs suited for spatial summation. We found that specific types of LMCs have dendrites extending to significantly more neighboring cartridges in the two nocturnal and crepuscular species than in the diurnal species, making these LMC types strong candidates for spatial summation. Moreover, while the absolute number of cartridges visited by the LMCs differed between the two dim-light species, their dendritic extents were very similar in terms of visual angle, possibly indicating a limiting spatial acuity. The overall size of the lamina neuropil did not correlate with the size of its LMCs.