Leg Coordination during Walking in Insects

Locomotion depends on constant adaptation to different requirements of the environment. An appropriate temporal and spatial coordination of multiple body parts is necessary to achieve a stable and adapted behavior. Until now it is unclear how the neuronal structures can achieve these meaningful adaptations. The exact role of the nervous system, muscles and mechanical constrains are not known. By using preparations in which special forms of adaptations are considered under experimental conditions that selectively exclude external influences, like mechanical interactions through the ground or differences in body mass, one can draw conclusions about the organization of the respective underlying neuronal structures. In the present thesis, four different publications are presented, giving evidence of mechanisms of temporal or spatial coordination of leg movements in the stick insect Carausius morosus and the fruit fly Drosophila melanogaster during different experimental paradigms. At first, state dependent local coordinating mechanisms are analyzed. Electromyographic measurements of the three major antagonistic leg muscle pairs of the forward and backward walking stick insect are evaluated. It becomes evident that only the motor activity of the most proximal leg joint is changed when walking direction is changed from forward to backward, which demonstrates that the neuronal networks driving movement in each individual leg seem to be organized in a modular structure. In the second part mechanisms that influence movement speed of the individual leg and coordination of speed between the different legs of the stick insect come into focus. Electrophysiological and behavioral experiments with the intact and reduced stick insect were used to examine relationships between the velocity of a stepping front leg and neuronal activity in the mesothoracic segment as well as correlations between the stepping velocities of different legs during walks with constant velocity or with distinct accelerations. It was shown that stepping velocity of single legs were not reflected in motoneuron activity or stepping velocity of another leg. Only when an increase in walking speed was induced, clear correlation in the stepping velocities of the individual legs was found. Subsequently, the analysis of changes in temporal leg coordination during different walking speeds in the fruit fly reveals that the locomotor system of Drosophila can cover a broad range of walking speeds and seems to follow the same rules as the locomotor system of the stick insect. Walking speed is increased by modifying stance duration, whereas swing duration and step amplitude remain largely unchanged. Changes in inter-leg coordination are gradually and systematically with walking speed and can adapt to major biomechanical changes in its walking apparatus. In the final part it was the aim to understand the role of neuronal mechanisms for the orientation and spatial coordination of foot placement in the stick insect. Placement of middle and hind legs with respect to the position of their respective rostrally neighboring leg were analyzed under two different conditions. Segment and state dependent differences in the aiming accuracy of the middle and hind legs could be shown, which indicate differences in the underlying neuronal structures in the different segments and the importance of movement in the target leg for the processing of the position information. Taken together, common principles in inter-leg coordination where found, like similarities between different organisms and segment specific or state dependent modifications in the walking system. They can be interpreted as evidence for a highly adaptive and modular design of the underlying neuronal structures

Organisation of foraging in ants

In social insects, foraging is often cooperative, and so requires considerable organisation. In most ants, organisation is a bottom-up process where decisions taken by individuals result in emergent colony level patterns. Individuals base their decisions on their internal state, their past experience, and their environment. By depositing trail pheromones, for example, ants can alter the environment, and thus affect the behaviour of their nestmates. The development of emergent patterns depends on both how individuals affect the environment, and how they react to changes in the environment. Chapters 4 – 9 investigate the role of trail pheromones and route memory in the ant Lasius niger. Route memories can form rapidly and be followed accurately, and when route memories and trail pheromones contradict each other, ants overwhelmingly follow route memories (chapter 4). Route memories and trail pheromones can also interact synergistically, allowing ants to forage faster without sacrificing accuracy (chapter 5). Home range markings also interact with other information sources to affect ant behaviour (chapter 6). Trail pheromones assist experienced ants when facing complex, difficult-to-learn routes (chapter 7). When facing complicated routes, ants deposit more pheromone to assist in navigation and learning (chapter 7). Deposition of trail pheromones is suppressed by ants leaving a marked path (chapter 5), strong pheromone trails (chapter 7) and trail crowding (chapter 8). Colony level ‘decisions’ can be driven by factors other than trail pheromones, such as overcrowding at a food source (chapter 9). Chapter 10 reviews the many roles of trail pheromones in ants. Chapters 11 – 14 focus on the organisation of cooperative food retrieval. Pheidole oxyops workers arrange themselves non-randomly around items to increase transport speeds (chapter 11). Groups of ants will rotate food items to reduce drag (chapter 12). Chapters 13 and 14 encompass the ecology of cooperative transport, and how it has shaped trail pheromone recruitment in P. oxyops and Paratrechina longicornis. Lastly, chapter 15 provide a comprehensive review of cooperative transport in ants and elsewhere

Management and drivers of change of pollinating insects and pollination services. National Pollinator Strategy: for bees and other pollinators in England, Evidence statements and Summary of Evidence

These Evidence Statements provide up-to-date information on what is known (and not known) about the status, values, drivers of change, and responses to management of UK insect pollinators (as was September 2018). This document has been produced to inform the development of England pollinator policy, and provide insight into the evidence that underpins policy decision-making. This document sits alongside a more detailed Summary of Evidence (Annex I) document written by pollinator experts. For information on the development of the statements, and confidence ratings assigned to them, please see section ?Generation of the statements? below. Citations for these statements are contained in the Summary of Evidence document

Management and drivers of change of pollinating insects and pollination services. National Pollinator Strategy: for bees and other pollinators in England, Evidence statements and Summary of Evidence

These Evidence Statements provide up-to-date information on what is known (and not known) about the status, values, drivers of change, and responses to management of UK insect pollinators (as was September 2018). This document has been produced to inform the development of England pollinator policy, and provide insight into the evidence that underpins policy decision-making. This document sits alongside a more detailed Summary of Evidence (Annex I) document written by pollinator experts. For information on the development of the statements, and confidence ratings assigned to them, please see section ‘Generation of the statements’ below. Citations for these statements are contained in the Summary of Evidence document

Neural correlates of diverse navigational strategies

Insects have evolved diverse and remarkable strategies for navigating in various ecologies all over the world. In particular, central place foragers, such as bees and ants, have become renowned for their fascinating navigational capabilities. At the heart of insect navigation lies a brain area known as the central complex (CX). Functionally, the CX integrates world-centric sensory information with self-motion cues to generate an internal map of angular position. It plays a role in driving motor commands and has been suggested as the neural substrate for encoding travel direction as well as navigational vectors theorized to be involved during path integration. Interestingly, the CX appears to have been highly anatomically conserved, even across insect species that diverged hundreds of millions of years ago. The conserved nature of the CX stands in juxtaposition to the fascinating diversity of insect behavior. How does a highly conserved brain area give rise to such diverse navigational behavior? Using block-face electron microscopy combined with neuron segmentation and synapse annotation, I analyzed CX circuits in six species of bees and ants: the honeybee, the bumblebee (Paper 1), the sweat bee, the army ant, the desert ant, and the bull ant. Our data suggests that there are core circuits that have been exceptionally well preserved across evolutionary time. Namely, the head direction circuit (Paper 2) which contains neurons that share total numbers, projectivity, and connectivity motifs from flies to bees and ants. In contrast, inputs from sensory areas vary to a much larger degree. Our data suggests that the relative contribution of parallel input pathways depends strongly on the information available in the habitat of a species. Also variable are the circuits that encode self-motion, something which is fundamental for building navigationally relevant internal representations (Paper 3). Altogether, these neuroanatomical maps provide the framework for future functional and modeling studies that seek to understand how sensory information is transformed into behavioral decisions within the context of navigation

Kinematics of cricket phonotaxis

Male crickets produce a species specific song to attract females which in response move towards the sound source. This behaviour, termed phonotaxis, has been the subject of many morphological, neurophysiological and behavioural studies making it one of the most well studied examples of acoustic communication in the animal kingdom. Despite this fact, the precise leg movements during this behaviour is unknown. This is of specific interest as the cricket’s ears are located on their front legs, meaning that the perception of the sound input might change as the insect moves. This dissertation describes a methodology and an analysis that fills this knowledge gap. I developed a semi-automated tracking system for insect motion based on commercially available high-speed video cameras and freely available software. I used it to collect detailed three dimensional kinematic information from female crickets performing free walking phonotaxis towards a calling song stimulus. I marked the insect’s joints with small dots of paint and recorded the movements from underneath with a pair of cameras following the insect as it walks on the transparent floor of an arena. Tracking is done offline, utilizing a kinematic model to constrain the processing. I obtained, for the first time, the positions and angles of all joints of all legs and six additional body joints, synchronised with stance-swing transitions and the sound pattern, at a 300 Hz frame rate. I then analysed this data based on four categories: The single leg motion analysis revealed the importance of the thoraco-coxal (ThC) and body joints in the movement of the insect. Furthermore the inside middle leg’s tibio-tarsal (TiTa) joint was the centre of the rotation during turning. Certain joints appear to be the most crucial ones for the transition from straight walking to turning. The leg coordination analysis revealed the patterns followed during straight walking and turning. Furthermore, some leg combinations cannot be explained by current coordination rules. The angles relative to the active speaker revealed the deviation of the crickets as they followed a meandering course towards it. The estimation of ears’ input revealed the differences between the two sides as the insect performed phonotaxis by using a simple algorithm. In general, the results reveal both similarities and differences with other cricket studies and other insects such as cockroaches and stick insects. The work presented herein advances the current knowledge on cricket phonotactic behaviour and will be used in the further development of models of neural control of phonotaxis

The interaction of path integration and terrestrial visual cues in navigating desert ants: what can we learn from path characteristics?

Ant foragers make use of multiple navigational cues to navigate through the world and the combination of innate navigational strategies and the learning of environmental information is the secret of their navigational success. We present here detailed information about the paths of Cataglyphis fortis desert ants navigating by an innate strategy, namely path integration. Firstly, we observe that the ants’ walking speed decreases significantly along their homing paths, such that they slow down just before reaching the goal, and maintain a slower speed during subsequent search paths. Interestingly, this drop in walking speed is independent of absolute home-vector length and depends on the proportion of the home vector that was completed. Secondly, we find that ants are influenced more strongly by novel or altered visual cues the further along their homing path they are. These results suggest that path integration modulates speed along the homing path in a way that might help ants search for, utilise or learn environmental information at important locations. Ants walk more slowly and sinuously when encountering novel or altered visual cues and occasionally stop and scan the world, this might indicate the re-learning of visual information

A unified neural model explaining optimal multi-guidance coordination in insect navigation

The robust navigation of insects arises from the coordinated action of concurrently functioning and interacting guidance systems. Computational models of specific brain regions can account for isolated behaviours such as path integration or route following, but the neural mechanisms by which their outputs are coordinated remains unknown. In this work, a functional modelling approach was taken to identify and model the elemental guidance subsystems required by homing insects. Then we produced realistic adaptive behaviours by integrating different guidance's outputs in a biologically constrained unified model mapped onto identified neural circuits. Homing paths are quantitatively and qualitatively compared with real ant data in a series of simulation studies replicating key infield experiments. Our analysis reveals that insects require independent visual homing and route following capabilities which we show can be realised by encoding panoramic skylines in the frequency domain, using image processing circuits in the optic lobe and learning pathways through the Mushroom Bodies (MB) and Anterior Optic Tubercle (AOTU) to Bulb (BU) respectively before converging in the Central Complex (CX) steering circuit. Further, we demonstrate that a ring attractor network inspired by firing patterns recorded in the CX can optimally integrate the outputs of path integration and visual homing systems guiding simulated ants back to their familiar route, and a simple non-linear weighting function driven by the output of the MB provides a context-dependent switch allowing route following strategies to dominate and the learned route retraced back to the nest when familiar terrain is encountered. 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. These results forward the case for a distributed architecture of the insect navigational toolkit. This unified model then be further validated by modelling the olfactory navigation of flies and ants. With simple adaptions of the sensory inputs, this model reproduces the main characteristics of the observed behavioural data, further demonstrating the useful role played by sensory-processing to CX to motor pathway in generating context-dependent coordination behaviours. In addition, this model help to complete the unified model of insect navigation by adding the olfactory cues that is one of the most crucial cues for insects