Multimodal interactions in insect navigation

Animals travelling through the world receive input from multiple sensory modalities that could be important for the guidance of their journeys. Given the availability of a rich array of cues, from idiothetic information to input from sky compasses and visual information through to olfactory and other cues (e.g. gustatory, magnetic, anemotactic or thermal) it is no surprise to see multimodality in most aspects of navigation. In this review, we present the current knowledge of multimodal cue use during orientation and navigation in insects. Multimodal cue use is adapted to a species’ sensory ecology and shapes navigation behaviour both during the learning of environmental cues and when performing complex foraging journeys. The simultaneous use of multiple cues is beneficial because it provides redundant navigational information, and in general, multimodality increases robustness, accuracy and overall foraging success. We use examples from sensorimotor behaviours in mosquitoes and flies as well as from large scale navigation in ants, bees and insects that migrate seasonally over large distances, asking at each stage how multiple cues are combined behaviourally and what insects gain from using different modalities

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 1: new molecules, metabolism, fate, and transport

With the exponential number of published data on neonicotinoids and fipronil during the last decade, an updated review of literature has been conducted in three parts. The present part focuses on gaps of knowledge that have been addressed after publication of the Worldwide Integrated Assessment (WIA) on systemic insecticides in 2015. More specifically, new data on the mode of action and metabolism of neonicotinoids and fipronil, and their toxicity to invertebrates and vertebrates, were obtained. We included the newly detected synergistic effects and/or interactions of these systemic insecticides with other insecticides, fungicides, herbicides, adjuvants, honeybee viruses, and parasites of honeybees. New studies have also investigated the contamination of all environmental compartments (air and dust, soil, water, sediments, and plants) as well as bees and apicultural products, food and beverages, and the exposure of invertebrates and vertebrates to such contaminants. Finally, we review new publications on remediation of neonicotinoids and fipronil, especially in water systems. Conclusions of the previous WIA in 2015 are reinforced; neonicotinoids and fipronil represent a major threat worldwide for biodiversity, ecosystems, and all the services the latter provide

Impacts des polluants métalliques sur l'abeille : de la colonie au cerveau

Les abeilles sont des pollinisateurs essentiels. Une pléthore de facteurs de stress environnementaux, tels que les produits agrochimiques, a été identifiée comme contribuant à leur déclin mondial. En particulier, ces facteurs de stress altèrent les processus cognitifs impliqués dans les comportements fondamentaux. Jusqu'à présent, cependant, on ne sait pratiquement rien de l'impact de l'exposition à des métaux lourds, dont la toxicité est avérée chez de nombreux organismes. Pourtant, leurs émissions mondiales résultant des activités humaines ont élevé leurs concentrations bien au-dessus des niveaux naturels dans l'air, le sol, l'eau et la flore, exposant ainsi les abeilles à tous les stades de leur vie. Le but de ma thèse était d'examiner les effets de la pollution métallique sur l'abeille domestique en utilisant une approche multi-échelle, du cerveau à la colonie, en laboratoire et sur le terrain. J'ai d'abord observé que les abeilles exposées à une gamme de concentrations de trois métaux communs (arsenic, plomb et zinc) en laboratoire étaient incapables de percevoir et éviter des concentrations usuelles, néanmoins nocives, de ces métaux dans leur nourriture. J'ai ensuite exposé de façon chronique des colonies à des concentrations réalistes de plomb dans la nourriture et démontré que la consommation de ce métal altérait la cognition et le développement morphologique des abeilles. Comme les polluants métalliques se trouvent souvent dans des mélanges complexes dans l'environnement, j'ai exploré l'effet des cocktails de métaux, montrant que l'exposition au plomb, à l'arsenic ou au cuivre seul était suffisante pour ralentir l'apprentissage et perturber le rappel de la mémoire, et que les combinaisons de ces métaux induisaient des effets négatifs additifs sur ces deux processus cognitifs. J'ai finalement étudié l'impact de l'exposition naturelle aux polluants métalliques dans un environnement contaminé, en collectant des abeilles à proximité d'une ancienne mine d'or, et montré que les individus des populations les plus exposées aux métaux présentaient des capacités d'apprentissage et de mémoire plus faibles, et des altérations de leur développement conduisant à une réduction de la taille de leur cerveau. Une analyse plus systématique des abeilles non exposées a révélé une relation entre la taille de la tête, la morphométrie du cerveau et les performances d'apprentissage dans différentes tâches comportementales, suggérant que l'exposition aux polluants métalliques amplifie ces variations naturelles. Ainsi, mes résultats suggèrent que les abeilles domestiques sont incapables d'éviter l'exposition à des concentrations réalistes de métaux qui sont préjudiciables au développement et aux fonctions cognitives, et appellent à une révision des niveaux environnementaux considérés comme "sûrs". Ma thèse est la première analyse intégrée de l'impact de plusieurs polluants métalliques sur la cognition, la morphologie et l'organisation cérébrale chez l'abeille, et vise à encourager de nouvelles études sur la contribution de la pollution métallique dans le déclin signalé des abeilles, et plus généralement, des insectes.Honey bees are crucial pollinators. A plethora of environmental stressors, such as agrochemicals, have been identified as contributors to their global decline. Especially, these stressors impair cognitive processes involved in fundamental behaviours. So far however, virtually nothing is known about the impact of metal pollutants, despite their known toxicity to many organisms. Their worldwide emissions resulting from human activities have elevated their concentrations far above natural baselines in the air, soil, water and flora, exposing bees at all life stages. The aim of my thesis was to examine the effects of metallic pollution on honey bees using a multiscale approach, from brain to colonies, in laboratory and field conditions. I first observed that bees exposed to a range of concentrations of three common metals (arsenic, lead and zinc) in the laboratory were unable to perceive and avoid, low, yet harmful, field-realistic concentrations of those metals in their food. I then chronically exposed colonies to field-realistic concentrations of lead in food and demonstrated that consumption of this metal impaired bee cognition and morphological development, leading to smaller adult bees. As metal pollutants are often found in complex mixtures in the environment, I explored the effect of cocktails of metals, showing that exposure to lead, arsenic or copper alone was sufficient to slow down learning and disrupt memory retrieval, and that combinations of these metals induced additive negative effects on both cognitive processes. I finally investigated the impact of natural exposure to metal pollutants in a contaminated environment, by collecting bees in the vicinity of a former gold mine, and showed that individuals from populations most exposed to metals exhibited lower learning and memory abilities, and development impairments conducing to reduced brain size. A more systematic analysis of unexposed bees revealed a relationship between head size, brain morphometrics and learning performances in different behavioural tasks, suggesting that exposure to metal pollutants magnifies these natural variations. Hence, altogether, my results suggest that honey bees are unable to avoid exposure to field-realistic concentrations of metals that are detrimental to development and cognitive functions; and call for a revision of the environmental levels considered as 'safe'. My thesis is the first integrated analysis of the impact of several metal pollutants on bee cognition, morphology and brain structure, and should encourage further studies on the contribution of metal pollution in the reported decline of honey bees, and more generally, of insects

Social Integrating Robots Suggest Mitigation Strategies for Ecosystem Decay

We develop here a novel hypothesis that may generate a general research framework of how autonomous robots may act as a future contingency to counteract the ongoing ecological mass extinction process. We showcase several research projects that have undertaken first steps to generate the required prerequisites for such a technology-based conservation biology approach. Our main idea is to stabilise and support broken ecosystems by introducing artificial members, robots, that are able to blend into the ecosystem's regulatory feedback loops and can modulate natural organisms' local densities through participation in those feedback loops. These robots are able to inject information that can be gathered using technology and to help the system in processing available information with technology. In order to understand the key principles of how these robots are capable of modulating the behaviour of large populations of living organisms based on interacting with just a few individuals, we develop novel mathematical models that focus on important behavioural feedback loops. These loops produce relevant group-level effects, allowing for robotic modulation of collective decision making in social organisms. A general understanding of such systems through mathematical models is necessary for designing future organism-interacting robots in an informed and structured way, which maximises the desired output from a minimum of intervention. Such models also help to unveil the commonalities and specificities of the individual implementations and allow predicting the outcomes of microscopic behavioural mechanisms on the ultimate macroscopic-level effects. We found that very similar models of interaction can be successfully used in multiple very different organism groups and behaviour types (honeybee aggregation, fish shoaling, and plant growth). Here we also report experimental data from biohybrid systems of robots and living organisms. Our mathematical models serve as building blocks for a deep understanding of these biohybrid systems. Only if the effects of autonomous robots onto the environment can be sufficiently well predicted can such robotic systems leave the safe space of the lab and can be applied in the wild to be able to unfold their ecosystem-stabilising potential

Beyond contact-based transmission networks:the role of spatial coincidence

Animal societies rely on interactions between group members to effectively communicate and coordinate their actions. To date, the transmission properties of interaction networks formed by direct physical contacts have been extensively studied for many animal societies and in all cases found to inhibit spreading. Such direct interactions do not, however, represent the only viable pathways. When spreading agents can persist in the environment, indirect transmission via 'same-place, different-time' spatial coincidences becomes possible. Previous studies have neglected these indirect pathways and their role in transmission. Here, we use rock ant colonies, a model social species whose flat nest geometry, coupled with individually tagged workers, allowed us to build temporally and spatially explicit interaction networks in which edges represent either direct physical contacts or indirect spatial coincidences. We show how the addition of indirect pathways allows the network to enhance or inhibit the spreading of different types of agent. This dual-functionality arises from an interplay between the interaction-strength distribution generated by the ants' movement and environmental decay characteristics of the spreading agent. These findings offer a general mechanism for understanding how interaction patterns might be tuned in animal societies to control the simultaneous transmission of harmful and beneficial agents

A glass half empty: Assessing the impact of empty flowers on foraging behaviour in three bee species

Flower-visiting insects face the difficult choice of selecting which flowers to visit and which to ignore. Foraging becomes more complicated because flowers can sometimes stop offering nectar, either due to removal by other visitors or because of physiological changes in the plant. In humans, items that are unexpectedly unavailable at the time of choice are called ‘phantom decoys’ and have been shown to influence preference relationships between other items in the choice set. If phantom decoys occur in pollinating insects, then the presence of empty flowers could have community-wide impacts on visitation rates of neighbouring flowers. In my first chapter, we tested if European honeybees Apis mellifera were susceptible to phantom decoy-style empty flowers. We then tested the effects of empty flowers on Bombus impatiens when they were influenced by the choices of their conspecifics. Finally, we tested if stingless bees, Tetragonula carbonaria made use of floral colour generalisations to choose flowers when the best flower in the choice set had its nectar removed. Overall, while we saw minimal impacts on floral choice by empty flowers, we did show that social behaviour is a key driver in allowing bees to make effective foraging decisions in the presence of empty flowers, and empty flowers can result in the abandonment of patches

Apprentissage visuel en réalité virtuelle chez Apis mellifera

Dotées d'un cerveau de moins d'un millimètre cube et contenant environ 950 000 neurones, les abeilles présentent un riche répertoire comportemental, parmi lesquels l'apprentissage appétitif et la mémoire jouent un rôle fondamental dans le contexte des activités de recherche de nourriture. Outre les formes élémentaires d'apprentissage, où les abeilles apprennent une association spécifique entre des événements de leur environnement, les abeilles maîtrisent également différentes formes d'apprentissage non-élémentaire, à la fois dans le domaine visuel et olfactif, y compris la catégorisation, l'apprentissage contextuel et l'abstraction de règles. Ces caractéristiques en font un modèle idéal pour l'étude de l'apprentissage visuel et pour explorer les mécanismes neuronaux qui sous-tendent leurs capacités d'apprentissage. Afin d'accéder au cerveau d'une abeille lors d'une tâche d'apprentissage visuel, l'insecte doit être immobilisé. Par conséquent, des systèmes de réalité virtuelle (VR) ont été développés pour permettre aux abeilles d'agir dans un monde virtuel, tout en restant stationnaires dans le monde réel. Au cours de mon doctorat, j'ai développé un logiciel de réalité virtuelle 3D flexible et open source pour étudier l'apprentissage visuel, et je l'ai utilisé pour améliorer les protocoles de conditionnement existants en VR et pour étudier le mécanisme neuronal de l'apprentissage visuel. En étudiant l'influence du flux optique sur l'apprentissage associatif des couleurs, j'ai découvert que l'augmentation des signaux de mouvement de l'arrière-plan nuisait aux performances des abeilles. Ce qui m'a amené à identifier des problèmes pouvant affecter la prise de décision dans les paysages virtuels, qui nécessitent un contrôle spécifique par les expérimentateurs. Au moyen de la VR, j'ai induit l'apprentissage visuel chez des abeilles et quantifié l'expression immédiate des gènes précoces (IEG) dans des zones spécifiques de leur cerveau pour détecter les régions impliquées dans l'apprentissage visuel. En particulier, je me suis concentré sur kakusei, Hr38 et Egr1, trois IEG liés à la recherche de nourriture et à l'orientation des abeilles et qui peuvent donc également être pertinents pour la formation d'association visuelle appétitive. Cette analyse suggère que les corps pédonculés sont impliqués dans l'apprentissage associatif des couleurs. Enfin, j'ai exploré la possibilité d'utiliser la VR sur d'autres modèles d'insectes et effectué un conditionnement différentiel sur des bourdons. Cette étude a montré que non seulement les bourdons sont capables de résoudre cette tâche cognitive aussi bien que les abeilles, mais aussi qu'ils interagissent davantage avec la réalité virtuelle, ce qui entraîne un ratio plus faible d'individus rejetés de l'expérience par manque de mouvement. Ces résultats indiquent que les protocoles VR que j'ai établis au cours de cette thèse peuvent être appliqués à d'autres insectes, et que le bourdon est un bon candidat pour l'étude de l'apprentissage visuel en VR.Equipped with a brain smaller than one cubic millimeter and containing ~950,000 neurons, honeybees display a rich behavioral repertoire, among which appetitive learning and memory play a fundamental role in the context of foraging activities. Besides elemental forms of learning, where bees learn specific association between environmental features, bees also master different forms of non-elemental learning, including categorization, contextual learning and rule abstraction. These characteristics make them an ideal model for the study of visual learning and its underlying neural mechanisms. In order to access the working brain of a bee during visual learning the insect needs to be immobilized. To do so, virtual reality (VR) setups have been developed to allow bees to behave within a virtual world, while remaining stationary within the real world. During my PhD, I developed a flexible and open source 3D VR software to study visual learning, and used it to improve existing conditioning protocols and to investigate the neural mechanism of visual learning. By developing a true 3D environment, we opened the possibility to add frontal background cues, which were also subjected to 3D updating based on the bee movements. We thus studied if and how the presence of such motion cues affected visual discrimination in our VR landscape. Our results showed that the presence of frontal background motion cues impaired the bees' performance. Whenever these cues were suppressed, color discrimination learning became possible. Our results point towards deficits in attentional processes underlying color discrimination whenever motion cues from the background were frontally available in our VR setup. VR allows to present insects with a tightly controlled visual experience during visual learning. We took advantage of this feature to perform ex-vivo analysis of immediate early gene (IEG) expression in specific brain area, comparing learner and non-learner bees. Using both 3D VR and a lore restrictive 2D version of the same task we tackled two questions, first what are the brain region involved in visual learning? And second, is the pattern of activation of the brain dependent on the modality of learning? Learner bees that solved the task in 3D showed an increased activity of the Mushroom Bodies (MB), which is coherent with the role of the MB in sensory integration and learning. Surprisingly we also found a completely different pattern of IEGs expression in the bees that solved the task in 2D conditions. We observed a neural signature that spanned the optic lobes and MB calyces and was characterized by IEG downregulation, consistent with an inhibitory trace. The study of visual learning's neural mechanisms requires invasive approach to access the brain of the insects, which induces stress in the animals and can thus impair behaviors in itself. To potentially mitigate this effect, bumble bees Bombus terrestris could constitute a good alternative to Apis mellifera as bumble bees are more robust. That's why in the last part of this work we explored the performances of bumblebees in a differential learning task in VR and compared them to those of honey bees. We found that, not only bumble bees are able to solve the task as well as honey bees, but they also engage more with the virtual environment, leading to a lower ratio of discarded individuals. We also found no correlation between the size of bumble bees and their learning performances. This is surprising as larger bumble bees, that assume the role of foragers in the colony, have been shown to be better at learning visual tasks in the literature

Neuronal encoding of object and distance information: a model simulation study on naturalistic optic flow processing

We developed a model of the input circuitry of the FD1 cell, an identified motion-sensitive interneuron in the blowfly's visual system. The model circuit successfully reproduces the FD1 cell's most conspicuous property: its larger responses to objects than to spatially extended patterns. The model circuit also mimics the time-dependent responses of FD1 to dynamically complex naturalistic stimuli, shaped by the blowfly's saccadic flight and gaze strategy: the FD1 responses are enhanced when, as a consequence of self-motion, a nearby object crosses the receptive field during intersaccadic intervals. Moreover, the model predicts that these object-induced responses are superimposed by pronounced pattern-dependent fluctuations during movements on virtual test flights in a three-dimensional environment with systematic modifications of the environmental patterns. Hence, the FD1 cell is predicted to detect not unambiguously objects defined by the spatial layout of the environment, but to be also sensitive to objects distinguished by textural features. These ambiguous detection abilities suggest an encoding of information about objects—irrespective of the features by which the objects are defined—by a population of cells, with the FD1 cell presumably playing a prominent role in such an ensemble