Insect Navigation Research Articles

A motion compensation treadmill for untethered wood ants (Formica rufa): evidence for transfer of orientation memories from free-walking training.

ABSTRACTThe natural scale of insect navigation during foraging makes it challenging to study under controlled conditions. Virtual reality and trackball setups have offered experimental control over visual environments while studying tethered insects, but potential limitations and confounds introduced by tethering motivates the development of alternative untethered solutions. In this paper, we validate the use of a motion compensator (or ‘treadmill’) to study visually driven behaviour of freely moving wood ants (Formica rufa). We show how this setup allows naturalistic walking behaviour and preserves foraging motivation over long time frames. Furthermore, we show that ants are able to transfer associative and navigational memories from classical maze and arena contexts to our treadmill. Thus, we demonstrate the possibility to study navigational behaviour over ecologically relevant durations (and virtual distances) in precisely controlled environments, bridging the gap between natural and highly controlled laboratory experiments.

An overview of anthropogenic electromagnetic radiations as risk to pollinators and pollination

Pollinators play a key functional role in most terrestrial ecosystems and provide important ecosystem service to maintain wild plant communities and agricultural productivity. The decline in pollinators has been related to anthropogenic disturbances such as habitat loss, alterations in land use, and climate change. The surge in mobile telephony has led to a marked increase in electromagnetic fields in the atmosphere, which may affect pollinator and pollination. Several laboratory studies have reported negative effects of electromagnetic radiation on reproduction, development, and navigation in insects. The abundance of insects such as the beetle, wasp, and hoverfly, decreased with electromagnetic radiation(EMR), whereas the abundance of underground-nesting wild bees and bee fly unexpectedly increased with EMR. Potential risks for pollinators and biodiversity are anthropogenic radiofrequency electromagnetic radiation (AREMR) (light, radiofrequency). Artificial light at night (ALAN) can alter the function and abundance of pollinator. Evidence of impacts of AREMR is not adequate due to a lack of high quality, field-realistic studies. Whether pollinators experiencing a threat of ALAN or AREMR, while major knowledge gap exists. In this review, the effects of EMR on wild pollinator groups such as wild bees, hoverflies, bee flies, beetles, butterflies, and wasps etc. have been highlighted. Researchers are also recommended for further study on the effects of EMR on insects. This study will be significant to conserve pollinators and other important insects.

Towards a multi-level understanding in insect navigation.

To understand the brain is to understand behaviour. However, understanding behaviour itself requires consideration of sensory information, body movements and the animal's ecology. Therefore, understanding the link between neurons and behaviour is a multi-level problem, which can be achieved when considering Marr's three levels of understanding: behaviour, computation, and neural implementation. Rather than establishing direct links between neurons and behaviour, the matter boils down to understanding two transitions: the link between neurons and brain computation on one hand, and the link between brain computations and behaviour on the other hand. The field of insect navigation illustrates well the power of such two-sided endeavour. We provide here examples revealing that each transition requires its own approach with its own intrinsic difficulties, and show how modelling can help us reach the desired multi-level understanding.

Using virtual worlds to understand insect navigation for bio-inspired systems.

Insects perform a wide array of intricate behaviors over large spatial and temporal scales in complex natural environments. A mechanistic understanding of insect cognition has direct implications on how brains integrate multimodal information and can inspire bio-based solutions for autonomous robots. Virtual Reality (VR) offers an opportunity assess insect neuroethology while presenting complex, yet controlled, stimuli. Here, we discuss the use of insects as inspiration for artificial systems, recent advances in different VR technologies, current knowledge gaps, and the potential for application of insect VR research to bio-inspired robots. Finally, we advocate the need to diversify our model organisms, behavioral paradigms, and embrace the complexity of the natural world. This will help us to uncover the proximate and ultimate basis of brain and behavior and extract general principles for common challenging problems.

What makes neurophysiology meaningful? Semantic content ascriptions in insect navigation research

In the course of investigating the living world, biologists regularly attribute semantic content to the phenomena they study. In this paper, I examine the case of a contemporary research program studying the navigation behaviors of ants and develop an account of the norms governing researchers’ ascriptions of semantic content in their research practices. The account holds that researchers assign semantic content to behaviors that reliably achieve a difficult goal-directed function, and it also suggests a productive role for attributions of semantic content in the process of animal behavior research.

Sideways Walking Control of a Cyborg Beetle

Cyborg insect also referred as insect-machine hybrid robot, consists of a living insect platform and an electronic backpack mounted on. The small size and magnificent walking ability of the insect make this hybrid system a potential candidate for search and rescue missions. The great locomotory capability helps the insect to cope with the complex and unpredictable terrains, whereas the tiny dimension allows it to easily enter the debris of post-disaster sites. There is a necessity to establish more controllable mobility for cyborg insects to develop more efficient maneuver plans. Here, this study demonstrates the control of sideways and forward walking in a cyborg beetle by emulating the touch responses of mechanoreceptors on the insect's elytra using the electrical stimulation. The beetle walked sideways leftward when the right elytron was stimulated, and vice versa. The forward control was attained by stimulating both elytra simultaneously. In addition, these elicited motions were found to be graded by tuning the stimulation frequency as increasing the frequency sped up the sideways walking and slowed down the forward velocity. Besides complementing the controllability of the cutting-edge cyborg insects, this graded response is essential for improving the navigation in cyborg insects for search and rescue missions.

A decentralised neural model explaining optimal integration of navigational strategies in insects.

Insect navigation arises from the coordinated action of concurrent guidance systems but the neural mechanisms through which each functions, and are then coordinated, remains unknown. We propose that insects require distinct strategies to retrace familiar routes (route-following) and directly return from novel to familiar terrain (homing) using different aspects of frequency encoded views that are processed in different neural pathways. We also demonstrate how the Central Complex and Mushroom Bodies regions of the insect brain may work in tandem to coordinate the directional output of different guidance cues through a contextually switched ring-attractor inspired by neural recordings. The resultant unified model of insect navigation reproduces behavioural data from a series of cue conflict experiments in realistic animal environments and offers testable hypotheses of where and how insects process visual cues, utilise the different information that they provide and coordinate their outputs to achieve the adaptive behaviours observed in the wild.

How do backward-walking ants (Cataglyphis velox) cope with navigational uncertainty?

Current opinion in insect navigation assumes that animals need to align with the goal direction to recognize familiar views and approach it. Yet, ants sometimes drag heavy food items backwards to the nest and it is still unclear to what extent they rely on visual memories while doing so. In this study displacement experiments and alterations of the visual scenery revealed that ants indeed recognized and used the learnt visual scenery to guide their path towards the nest while walking backwards. In addition, the occurrence of forward-peeking behaviours revealed that backward-walking ants continually estimated their directional uncertainty by integrating multiple cues such as visual familiarity, the state of their path integrator and the time spent backwards. A simple mechanical model based on repulsive and attractive visual memories captured the results and explained how visual navigation can be performed backwards.

Mantis Shrimp Navigate Home Using Celestial and Idiothetic Path Integration.

Path integration is a robust mechanism that many animals employ to return to specific locations, typically their homes, during navigation. This efficient navigational strategy has never been demonstrated in a fully aquatic animal, where sensory cues used for orientation may differ dramatically from those available above the water's surface. Here, we report that the mantis shrimp, Neogonodactylus oerstedii, uses path integration informed by a hierarchical reliance on the sun, overhead polarization patterns, and idiothetic (internal) orientation cues to return home when foraging, making them the first fully aquatic path-integrating animals yet discovered. We show that mantis shrimp rely on navigational strategies closely resembling those used by insect navigators, opening a new avenue for the investigation of the neural basis of navigation behaviors and the evolution of these strategies in arthropods and potentially other animals as well. VIDEO ABSTRACT.

Mantis Shrimp Navigate Home Using Celestial and Idiothetic Path Integration

Path integration is a robust mechanism that many animals employ to return to specific locations, typically their homes, during navigation. This efficient navigational strategy has never been demonstrated in a fully aquatic animal, where sensory cues used for orientation may differ dramatically from those available above the water’s surface. Here we report that the mantis shrimp, Neogonodactylus oerstedii, uses path integration informed by a hierarchical reliance on the sun, overhead polarization patterns, and idiothetic (internal) orientation cues to return home when foraging, making them the first fully aquatic path-integrating animals yet discovered. We show that mantis shrimp rely on navigational strategies closely resembling those used by insect navigators, opening a new avenue for the investigation of the neural basis of navigation behaviors and the evolution of these strategies in arthropods and potentially other animals as well.

Extremely low neonicotinoid doses alter navigation of pest insects along pheromone plumes

The prevailing use of neonicotinoids in pest control has adverse effects on non-target organisms, like honeybees. However, relatively few studies have explored the effect of sublethal neonicotinoid levels on olfactory responses of pest insects, and thus their potential impact on semiochemical surveillance and control methods, such as monitoring or mating disruption. We recently reported that sublethal doses of the neonicotinoid thiacloprid (TIA) had dramatic effects on sex pheromone release in three tortricid moth species. We present now effects of TIA on pheromone detection and, for the first time, navigational responses of pest insects to pheromone sources. TIA delayed and reduced the percentage of males responding in the wind tunnel without analogous alteration of electrophysiological antennal responses. During navigation along an odor plume, treated males exhibited markedly slower flights and, in general, described narrower flight tracks, with an increased susceptibility to wind-induced drift. All these effects increased in a dose-dependent manner starting at LC0.001 - which would kill just 10 out of 106 individuals - and revealed an especially pronounced sensitivity in one of the species, Grapholita molesta. Our results suggest that minimal neonicotinoid quantities alter chemical communication, and thus could affect the efficacy of semiochemical pest management methods.

Private information conflict: Lasius niger ants prefer olfactory cues to route memory.

Foraging animals use a variety of information sources to navigate, such as memorised views or odours associated with a goal. Animals frequently use different information sources concurrently, to increase navigation accuracy or reliability. While much research has focussed on conflicts between individually learned (private) information and social information, conflicts between private information sources have been less broadly studied. Here, we investigate such a conflict by pitting route memory against associative odour cue learning in the ant Lasius niger. Ants were alternatingly trained to find a high-quality scented food source on one arm of a Y-maze, and a differently scented low-quality food source on the opposite arm. After training, ants were presented with a Y-maze in which the high- and low-quality-associated scents were presented on opposite arms than during training. The ants showed an extremely strong preferential reliance on the odour cues, with 100% of ants following the high-quality odour and thus moving towards the side associated with low-quality food. Further experiments demonstrated that ants also learn odour associations more rapidly, requiring only one visit to each odour-quality combination to form a reliable association. Side associations in the absence of odours, by contrast, required at least two visits to each side for reliable learning. While much attention has been focussed on visual route learning in insect navigation and decision-making, our results highlight the overwhelming importance of odour cues in insect path choice.

Celestial navigation in Drosophila.

Many casual observers typecast Drosophila melanogaster as a stationary pest that lurks around fruit and wine. However, the omnipresent fruit fly, which thrives even in desert habitats, likely established and maintained its cosmopolitan status via migration over large spatial scales. To perform long-distance dispersal, flies must actively maintain a straight compass heading through the use of external orientation cues, such as those derived from the sky. In this Review, we address how D. melanogaster accomplishes long-distance navigation using celestial cues. We focus on behavioral and physiological studies indicating that fruit flies can navigate both to a pattern of linearly polarized light and to the position of the sun - the same cues utilized by more heralded insect navigators such as monarch butterflies and desert ants. In both cases, fruit flies perform menotaxis, selecting seemingly arbitrary headings that they then maintain over time. We discuss how the fly's nervous system detects and processes this sensory information to direct the steering maneuvers that underlie navigation. In particular, we highlight recent findings that compass neurons in the central complex, a set of midline neuropils, are essential for navigation. Taken together, these results suggest that fruit flies share an ancient, latent capacity for celestial navigation with other insects. Furthermore, they illustrate the potential of D. melanogaster to help us to elucidate both the cellular basis of navigation and mechanisms of directed dispersal on a landscape scale.

Navigation: from animal behaviour to guiding principles

![Figure][1] Tritonia diomedea navigating through a sea pen bed in search of prey or mates. Photo credit: Russell Wyeth and James A. Murray. Whether an animal's world is restricted to a few twigs or the avian highways that traverse the planet, creatures must navigate their surroundings

Honey bees flexibly use two navigational memories when updating dance distance information.

Honey bees can communicate navigational information which makes them unique amongst all prominent insect navigators. Returning foragers recruit nest mates to a food source by communicating flight distance and direction using a small scale walking pattern: the waggle dance. It is still unclear how bees transpose flight information to generate corresponding dance information. In single feeder shift experiments, we monitored for the first time how individual bees update dance duration after a shift of feeder distance. Interestingly, the majority of bees (86%) needed two or more foraging trips to update dance duration. This finding demonstrates that transposing flight navigation information to dance information is not a reflexive behavior. Furthermore, many bees showed intermediate dance durations during the update process, indicating that honey bees highly likely use two memories: (i) a recently acquired navigation experience and (ii) a previously stored flight experience. Double-shift experiments, in which the feeder was moved forward and backward, created an experimental condition in which honey bee foragers did not update dance duration; suggesting the involvement of more complex memory processes. Our behavioral paradigm allows the dissociation of foraging and dance activity and opens the possibility of studying the molecular and neural processes underlying the waggle dance behavior.

Two distance memories in desert ants-Modes of interaction.

Navigation plays an essential role for many animals leading a mobile mode of life, and for central place foragers in particular. One important prerequisite for navigation is the ability to estimate distances covered during locomotion. It has been shown that Cataglyphis desert ants, well-established model organisms in insect navigation, use two odometer mechanisms, namely, stride and optic flow integration. Although both mechanisms are well established, their mode of interaction to build one odometer output remains enigmatic. We tackle this problem by selectively covering the ventral eye parts in Cataglyphis fortis foragers, the eye regions responsible for optic flow input in odometry. Exclusion of optic flow cues was implemented during different sections of outbound and inbound travel. This demonstrated that the two odometers have separate distance memories that interact in determining homing distance. Possible interpretations posit that the two odometer memories (i) take on different relative weights according to context or (ii) compete in a winner-take-all mode. Explanatory values and implications of such interpretations are discussed. We are able to provide a rough quantitative assessment of odometer cue interaction. An understanding of the interaction of different odometer mechanisms appears valuable not only for animal navigation research but may inform discussions on sensor fusion in both behavioural contexts and potential technical applications.

Interception by two predatory fly species is explained by a proportional navigation feedback controller.

When aiming to capture a fast-moving target, animals can follow it until they catch up, or try to intercept it. In principle, interception is the more complicated strategy, but also more energy efficient. To study whether simple feedback controllers can explain interception behaviours by animals with miniature brains, we have reconstructed and studied the predatory flights of the robber fly Holcocephala fusca and killer fly Coenosia attenuata. Although both species catch other aerial arthropods out of the air, Holcocephala contrasts prey against the open sky, while Coenosia hunts against clutter and at much closer range. Thus, their solutions to this target catching task may differ significantly. We reconstructed in three dimensions the flight trajectories of these two species and those of the presented targets they were attempting to intercept. We then tested their recorded performances against simulations. We found that both species intercept targets on near time-optimal courses. To investigate the guidance laws that could underlie this behaviour, we tested three alternative control systems (pure pursuit, deviated pursuit and proportional navigation). Only proportional navigation explains the timing and magnitude of fly steering responses, but with differing gain constants and delays for each fly species. Holcocephala uses a dimensionless navigational constant of N ≈ 3 with a time delay of ≈28 ms to intercept targets over a comparatively long range. This constant is optimal, as it minimizes the control effort required to hit the target. In contrast, Coenosia uses a constant of N ≈ 1.5 with a time delay of ≈18 ms, this setting may allow Coenosia to cope with the extremely high line-of-sight rotation rates, which are due to close target proximity, and thus prevent overcompensation of steering. This is the first clear evidence of interception supported by proportional navigation in insects. This work also demonstrates how by setting different gains and delays, the same simple feedback controller can yield the necessary performance in two different environments.

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.

The Geomagnetic Field Is a Compass Cue in Cataglyphis Ant Navigation

Desert ants (Cataglyphis) are famous insect navigators. During their foraging lives, the ants leave their underground colonies for long distances and return to their starting point with fair accuracy [1, 2]. Their incessantly running path integrator provides them with a continually updated home vector [3-5]. Directional input to their path integrator is provided by avisual compass based on celestial cues [6, 7]. However, as path integration is prone to cumulative errors, the ants additionally employ landmark guidance routines [8-11]. At the start of their foraging lives, they acquire the necessary landmark information by performing well-structured learning walks [12, 13], including turns about their vertical body axes [14]. When Cataglyphis noda performs these pirouettes, it always gazes at the nest entrance during the longest of several short stopping phases [14]. As the small nest entrance is not visible, the ants can adjust their gaze direction only by reading out their path integrator. However, recent experiments have shown that, for adjusting the goal-centered gaze directions during learning walks, skylight cues are not required [15]. A most promising remaining compass cue is the geomagnetic field, which is used for orientation in one way or the other by a variety of animal species [16-25]. Here, we show that the gaze directions during the look-back-to-the-nest behavior change in a predictable way to alterations of the horizontal component of the magnetic field. This is the first demonstration that, in insects, a geomagnetic compass cue is both necessary and sufficient for accomplishing a well-defined navigational task.

Optimal multiguidance integration in insect navigation

In the last decades, desert ants have become model organisms for the study of insect navigation. In finding their way, they use two major navigational routines: path integration using a celestial compass and landmark guidance based on sets of panoramic views of the terrestrial environment. It has been claimed that this information would enable the insect to acquire and use a centralized cognitive map of its foraging terrain. Here, we present a decentralized architecture, in which the concurrently operating path integration and landmark guidance routines contribute optimally to the directions to be steered, with "optimal" meaning maximizing the certainty (reliability) of the combined information. At any one time during its journey, the animal computes a path integration (global) vector and landmark guidance (local) vector, in which the length of each vector is proportional to the certainty of the individual estimates. Hence, these vectors represent the limited knowledge that the navigator has at any one place about the direction of the goal. The sum of the global and local vectors indicates the navigator's optimal directional estimate. Wherever applied, this decentralized model architecture is sufficient to simulate the results of quite a number of diverse cue-conflict experiments, which have recently been performed in various behavioral contexts by different authors in both desert ants and honeybees. They include even those experiments that have deliberately been designed by former authors to strengthen the evidence for a metric cognitive map in bees.