Geosmin suppresses defensive behaviour and elicits unusual neural responses in honey bees

Geosmin is an odorant produced by bacteria in moist soil. It has been found to be extraordinarily relevant to some insects, but the reasons for this are not yet fully understood. Here we report the first tests of the effect of geosmin on honey bees. A stinging assay showed that the defensive behaviour elicited by the bee's alarm pheromone component isoamyl acetate (IAA) is strongly suppressed by geosmin. Surprisingly, the suppression is, however, only present at very low geosmin concentrations, and disappears at higher concentrations. We investigated the underlying mechanisms at the level of the olfactory receptor neurons by means of electroantennography, finding the responses to mixtures of geosmin and IAA to be lower than to pure IAA, suggesting an interaction of both compounds at the olfactory receptor level. Calcium imaging of the antennal lobe (AL) revealed that neuronal responses to geosmin decreased with increasing concentration, correlating well with the observed behaviour. Computational modelling of odour transduction and coding in the AL suggests that a broader activation of olfactory receptor types by geosmin in combination with lateral inhibition could lead to the observed non-monotonic increasing-decreasing responses to geosmin and thus underlie the specificity of the behavioural response to low geosmin concentrations

Experience-dependent plasticity in brain structure and olfactory learning capacities in honey bees (Apis mellifera)

Les expériences vécues par un individu, vont moduler ses capacités d'apprentissage et induire des modifications structurales dans les régions cérébrales impliquées. Chez l'abeille, de la plasticité dépendante de l'expérience a été observée dans des centres cérébraux impliqués dans l'apprentissage et la mémoire : les corps pédonculés (CPs). Pourtant, les conséquences d'une telle plasticité sur les performances d'apprentissage sont inconnues. L'objectif de ma thèse était d'examiner les relations existantes entre expérience, capacités d'apprentissage et structure des CPs. La division du travail étant basée sur l'âge chez l'abeille, j'ai étudié la plasticité dépendante de l'expérience chez des abeilles jeunes, travaillant dans la ruche, mais aussi chez des abeilles plus âgées qui butinent à l'extérieur. J'ai d'abord observé que des abeilles exposées à un environnement appauvri en stimulations sensorielles et sociales pendant les premiers jours de vie adulte présentent un nombre élevé de boutons synaptiques dans les CPs, et une performance altérée dans un apprentissage dépendant des CPs, l'inversion de consigne. Cela suggère l'existence d'un élagage synaptique dépendant de l'expérience acquise dans la ruche, qui serait bénéfique pour les capacités d'apprentissage. J'ai observé un effet similaire de l'enrichissement environnemental lorsque les abeilles commencent à butiner. Le début du butinage s'est en effet accompagné d'une diminution du nombre de boutons synaptiques dans les CPs et d'une amélioration des performances en inversion de consigne. Une activité prolongée de butinage a eu les effets inverses, en particulier chez des abeilles qui, suite à un stress appliqué à la colonie, butinent avant l'âge normal. J'ai ainsi mis en évidence une relation négative entre le nombre de boutons synaptiques dans les CPs et les performances en inversion de consigne. Par la suite, j'ai utilisé un autre apprentissage dépendant des CPs, le patterning positif, afin de pouvoir conclure sur un déclin généralisé des capacités cognitives dépendantes des CPs chez les butineuses. J'ai montré l'implication du système cholinergique dans le déclin cognitif lié à l'expérience de butinage. Cette thèse réunit les premiers travaux analysant la plasticité dépendante de l'expérience à la fois dans la structure cérébrale, mais aussi dans les capacités cognitives. Elle devrait permettre de comprendre les mécanismes reliant connectivité synaptique et apprentissage, et encourager des études sur l'impact des agents stressants environnementaux sur le déclin cognitif lié au butinage.Learning capacities, and the structure of the brain centres supporting them, vary greatly between individuals, partly due to different life experiences. In honey bees, experience-dependent plasticity has been reported in brain centres involved in learning and memory: the mushroom bodies (MBs). The consequences of such plasticity on learning performances are still unknown. The aim of my thesis was to examine the relationships between experience, learning capacities and MB organization in honey bees. The age-related division of labour in honey bees gave me the opportunity to study experience-dependent plasticity both in young bees working inside the hive, and in older bees foraging outdoors. I first observed that bees exposed to a sensory-impoverished environment for the first days of adulthood had a higher number of synaptic boutons in the MBs, and a reduced performance in a MB-dependent learning task; reversal learning. This suggests the occurrence of experience-dependent synaptic pruning in the natural environment, which improves learning capacities. I observed similar effects of environmental enrichment when the bees started foraging. Foraging onset was accompanied by a decrease in the number of synaptic boutons in the MBs, as well as by an improvement in reversal learning performance. Prolonged foraging activity, however, had the opposite effects, especially when a stress applied to the colony induced bees to forage earlier. Therefore, I highlighted a negative relationship between the number of synaptic boutons in the MBs and performance in reversal learning. I then confirmed the negative impact of foraging activity on learning capacities using a different MB-dependent task; positive patterning. I revealed the involvement of the cholinergic signalling pathway in this experience-dependent cognitive decline. This thesis presents the first integrated analyses of experience-dependent plasticity in both brain structure and cognitive capacities in honey bees. It helps to understand the mechanisms linking synaptic connectivity to learning performances, and will encourage further studies on the role of environmental stressors in the reported cognitive decline in foragers

The Neurophysiological Bases of the Impact of Neonicotinoid Pesticides on the Behaviour of Honeybees

Acetylcholine is the main excitatory neurotransmitter in the honeybee brain and controls a wide range of behaviours that ensure the survival of the individuals and of the entire colony. Neonicotinoid pesticides target this neurotransmission pathway and can thereby affect the behaviours under its control, even at doses far below the toxicity limit. These sublethal effects of neonicotinoids on honeybee behaviours were suggested to be partly responsible for the decline in honeybee populations. However, the neural mechanisms by which neonicotinoids influence single behaviours are still unclear. This is mainly due to the heterogeneity of the exposure pathways, doses and durations between studies. Here, we provide a review of the state of the science in this field and highlight knowledge gaps that need to be closed. We describe the agonistic effects of neonicotinoids on neurons expressing the different nicotinic acetylcholine receptors and the resulting brain structural and functional changes, which are likely responsible for the behavioural alterations reported in bees exposed to neonicotinoids

Les abeilles sont-elles aussi victimes de leur intelligence

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Considering variation in bee responses to stressors can reveal potential for resilience

Environmental stressors frequently have sublethal consequences for animals, often affecting the mean of phenotypic traits in populations. However, effects on inter‐individual variability are poorly understood. Since phenotypic variability is the basis for adaptation, any change due to stressors may have important implications for population resilience. Here, we explored this possibility in bees by analysing raw datasets from 23 studies (5618 bees) in which individuals were first exposed to stressors and then tested for cognitive tasks. While all types of stressors decreased the mean cognitive performance of bees, they increased cognitive variability. Focusing on 14 pesticide studies, we found that the mode of exposure to stressors and the dose were critical. Mean cognitive performance was more affected by a chronic exposure than by an acute exposure. Yet, cognitive variability increased with increasing doses following both exposure durations. Policy implications. Current guidelines for the authorization of plant protection products on the European market prioritize acute over chronic toxicity assessments on non‐target organisms. By overlooking the consequences of a chronic exposure, regulatory authorities may register new products or doses that are harmful to bee populations. Our findings call for more research on stress‐induced phenotypic variation and its incorporation into policy guidelines to help identify levels and modes of exposure animals can cope with.Les facteurs de stress environnementaux ont des effets néfastes sur la santé animale, modifiant souvent la moyenne de traits phénotypiques chez les populations touchées. Les conséquences de ces stress sur la variabilité inter‐individuelle sont cependant peu connues. La variabilité étant la base de l'adaptation, tout changement dû aux facteurs environnementaux pourrait avoir des impacts importants sur la résilience de la population. Nous avons exploré cette possibilité en analysant 23 ensembles de données publiés (5618 individus) dans lesquels des abeilles ont été exposées à divers facteurs de stress préalablement à une évaluation de leurs capacités cognitives. Tous les stress étudiés ont diminué la moyenne des performances cognitives individuelles mais ont également augmenté la variabilité entre les abeilles. Les 14 études basées sur une exposition aux pesticides indiquent que la dose et le mode d'exposition sont déterminants. La performance moyenne est plus affectée par une exposition chronique que par une exposition aiguë. Pourtant, la variabilité inter‐individuelle augmente avec la dose utilisée quel que soit le mode d'exposition. Implications . Les recommandations actuelles concernant l'autorisation de nouveaux produits phytosanitaires sur les marchés européens priorisent l’évaluation sur les organismes non ciblés des effets aigus de ces produits plutôt que les effets chroniques. En négligeant les conséquences des effets chroniques, les autorités pourraient autoriser de nouveaux produits ou doses délétères pour les abeilles. Nos travaux incitent à davantage de recherches sur la variabilité phénotypique induite par les facteurs de stress et à l'incorporation de son analyse dans les recommandations officielles. Ceci devrait aider à identifier les niveaux et modes d'exposition que les animaux peuvent supporter

Why Bees Are So Vulnerable to Environmental Stressors

International audienceBee populations are declining in the industrialized world, raising concerns for the sustainable pollination of crops. Pesticides, pollutants, parasites, diseases, and malnutrition have all been linked to this problem. We consider here neuro-biological, ecological, and evolutionary reasons why bees are particularly vulnerable to these environmental stressors. Central-place foraging on flowers demands advanced capacities of learning, memory, and navigation. However, even at low intensity levels, many stressors damage the bee brain, disrupting key cognitive functions needed for effective foraging, with dramatic consequences for brood development and colony survival. We discuss how understanding the relationships between the actions of stressors on the nervous system, individual cognitive impairments, and colony decline can inform constructive interventions to sustain bee populations. Bees Are Exposed to Multiple Environmental Stressors Bees are ecologically and economically vital pollinators for both wild and cultivated flowers. Presently many populations are in decline [1-4], while demand for pollination[ 2 8 5 _ T D $ D I F F ]-dependent crops continues to rise, generating understandable alarm and debate about the possibility of an emerging 'pollination crisis' [5]. Many causal factors have been identified, including a range of pathogens and parasites [6,7], human-induced stressors such as pesticides [8-10], and other forms of environmental degradation [11]. Very few of these stressors can be considered new, but many have increased in intensity over the past decade in much of the industrialized world. Our objective in this review is to consider why bees are particularly sensitive to these environmental stressors, even at low levels, and why their populations are now declining. Bees, with the exception of parasitic species, raise their brood in a single defensible nest [12]. We argue that, in these insects, central-place foraging on ephemeral, dispersed, and highly variable floral resources places particularly heavy demands on cognitive capacities. Individuals must learn to forage at an energetic profit, locate high-quality feeding sites, efficiently handle flowers, and navigate back to the nest to provision their brood with the right mix of nectar and pollen. The cognitive capacities underpinning these complex behaviors require optimal development and function of central brain structures as well as precisely regulated plasticity of brain circuits necessary for learning, memory, and navigation [13,14]. These brain systems are very easily disrupted, and it is especially problematic that many pesticides found in floral resources directly target key neural pathways [15,16]. Pathogens and nutritional deficits also compromise cognitive functions [17,18]. Even mild damage to the brain can significantly reduce foraging performance, thus rendering bees especially vulnerable to these environmental stressors. In social species, such as honey bees, bumblebees, and stingless bees, efficient division of labor and coordination of tasks across nest mates provide buffering against environmental stressors because individuals share a fortress-factory stocked with stored resources [19]. However, thi

An Analysis of Famous Person Semantic Memory in Aging

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Mushroom body structure of orientating bees and foragers.

<p><b>(A)</b> Frontal confocal image of the right median MB labelled for synapsin (scale bar = 100μm). Borders of the lip (<i>orange</i>) and dense collar (<i>blue</i>) are highlighted. Boxplots showing the characteristics of the dense collar (<i>blue</i>) and lip (<i>orange</i>) of a sample of orientating bees (<i>O</i>, n = 5) and foragers (<i>F</i>, n = 13): <b>(B)</b> neuropil volume, <b>(C)</b> density of synaptic boutons, <b>(D)</b> number of synaptic boutons per neuropil. * p < 0.05, Mann-Whitney U-Test.</p

Correlations between foraging intensity and structural characteristics of the mushroom bodies.

<p>Individual values (n = 13) for the parameters of the lip <b>(A, B, C)</b> and dense collar <b>(D, E, F)</b> are plotted against foraging intensity: neuropilar volume <b>(A, D)</b>, density of synaptic boutons <b>(B, E),</b> total number of synaptic boutons <b>(C, F)</b>. The volume of the lip and collar, as well as the total number of boutons per lip, correlate positively with foraging intensity (Spearman rank correlations).</p