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Biology subjects

Brockmann, A.

Publications and source records attributed to Brockmann, A..

At least 19 recordsLinked to original sources

Unraveling Honey Bee's Waggle Dances in Natural Conditions with Video-Based Deep Learning

O_LIWild and managed honey bees, crucial pollinators for both agriculture and natural ecosystems, face challenges due to industrial agriculture and urbanization. Understanding how bee colonies utilize the landscape for foraging is essential for managing human-bee conflicts and protecting these pollinators to sustain their vital pollination services. To understand how the bees utilize their surroundings, researchers often decode bee waggle dances, which honey bee workers use to communicate navigational information of desirable food and nesting sites to their nest mates. This process is carried out manually, which is time-consuming, prone to human error and requires specialized skills. C_LIO_LIWe address this problem by introducing a novel deep learning-based pipeline that automatically detects and measures waggle runs, the core movement of the waggle dance, under natural recording conditions for the first time. We combined the capabilities of the action detector YOWOv2 and the DeepSORT tracking method, with the Principal Component Analysis to extract dancing bee bounding boxes and the angles and durations within waggle runs. C_LIO_LIThe presented pipeline works fully automatically with videos taken from wild Apis dorsata colonies in its natural environment, and can be used for any honey bee species. Comparison of our pipeline with analyses made by human experts revealed that our procedure was able to detect 93% of waggle runs on the testing dataset, with a run duration Root Mean Squared Error (RMSE) of less than a second, and a run angle RMSE of 0.14 radians. We also assessed the generalizability of our pipeline to previously unseen recording conditions, successfully detecting 50% of waggle runs performed by Apis mellifera bees from a colony managed in Tokyo, Japan. In parallel, we discovered the most appropriate values of the models hyperparameters for this task. C_LIO_LIOur study demonstrates that a deep learning-based pipeline can successfully and automatically analyze the waggle runs of Apis dorsata in natural conditions and generalize to other bee species. This approach enables precise measurement of direction and duration, enabling the study of bee foraging behavior on an unprecedented scale compared to traditional manual methods contributing to preserving biodiversity and ecosystem services. C_LI

ecology↗

Symbiont loss and gain, rather than co-diversification shapes honeybee gut microbiota diversity and function

Studying gut microbiota evolution across animals is crucial for understanding symbiotic interactions but is hampered by the lack of high-resolution genomic data. Honeybees, with their specialized gut microbiota and well-known ecology, offer an ideal system to study this evolution. Using shotgun metagenomics on 200 worker bees from five honeybee species, we recover thousands of metagenome-assembled genomes and identify several novel bacterial species. While microbial communities were mostly host-specific, we found both specialists and generalists, even among closely related bacterial species, with notable variation between honeybee hosts. Some bacterial generalists emerged host-specific only at the strain level, suggesting recent host switches. While we found some signal of co-diversification between hosts and symbionts, this was not more than expected by chance and was much less pronounced than what has been observed for gut bacteria of hominids and small mammals. Instead, symbiont gains, losses, and replacements emerged as the predominant process for honeybees. This highly dynamic evolution of the specialized honey bee gut microbiota has led to taxonomic and functional differences across hosts, such as the ability to degrade pollen-derived pectin. Our results provide new insights into the evolutionary processes govern gut microbiota diversity across closely related hosts and uncover the functional potential of the previously underexplored gut microbiota of these important pollinators.

microbiology↗

Taxonomic Revision and Identification Keys for the Giant Honey Bees

The taxonomy and phylogeny of the giant honey bees (Apis; subgenus Megapis) are still controversial and unresolved. The species boundaries within the subgenus are unclear and some species that are recognized on the basis of genetic differences lack supporting morphological characters. Two species are now well accepted: Apis dorsata F. of tropical regions of Asia and Apis laboriosa Smith that inhabits the foothills of Himalaya and neighboring mountain ranges. In addition, researchers have suggested that the two allopatric populations of giant honey bees that inhabit Sulawesi, Indonesia (A. binghami Cockerell) and the oceanic Philippine islands (A. breviligula Maa) as well as the South Indian form also deserve species status. We conducted a taxonomic study based on morphological characters of Megapis from throughout Asia. Our study confirms that Apis laboriosa is a distinct species based on numerous morphological characters. Moreover, A. dorsata of mainland Asia differs from the two island taxa based on coloration, ocellus size, and the spacing of compound eyes and ocelli. We found no evidence that breviligula of the Philippines has a distinctively short tongue, and report only one minor character (the shape of sternum 5) that differed statistically between bees from Sulawesi and the Philippines. We conclude that the bees from these islands represent a single morphological species, A. binghami, with two subspecies, A. b. binghami and A. b. breviligula. Apis dorsata from the Andaman Islands are smaller than but conspecific with those of mainland Asia. We found no morphological autapomorphies in the giant honey bees of southern India known to differ in mtDNA from A. dorsata from elsewhere in mainland Asia. We provide a taxonomic keys to workers and drones within the subgenus Megapis.

zoology↗

Multiple molecular links between the circadian clock and memory centers in honey bees

Time and memory are intimately linked: the capability to learn and recall varies over the day and humans and many animals can associate important events with the time of day. However, how the circadian clock and memory centers are connected is not well understood. We time-trained honey bee foragers and used RNA-sequencing and RNAscope imaging to analyze gene expression changes in focal populations of mushroom body neurons. Thus, we identified three candidate functional modules of time-memory: synchronized peak-level expression of memory-related genes during training time, anticipatory activation of transcription in pdfr-expressing neurons, and cry2 and per co-expressing neurons that might represent local clocks. The complex interactions between the clock and memory centers, which appear to be more similar to mammals than other insects, might have been facilitated to optimize social foraging in honey bees.

neuroscience↗

Tropical and montane A. cerana show distinct dance-distance calibration curves

Social bees have evolved sophisticated communication systems to recruit nestmates to newly found food sources. As foraging ranges can vary from a few hundred meters to several kilometers depending on the environment or season, populations living in different climate zones likely show specific adaptations in their recruitment communication. Accordingly, studies in the western honey bee, Apis mellifera, demonstrated that temperate populations exhibit shallower dance-calibration curves compared to tropical populations. Here we report the first comparison of calibration curves for three Indian A. cerana lineages: the tropical A. indica, and the two montane Himalayan populations A. c. cerana (Himachal Pradesh) and A. c. kashmirensis (Jammu and Kashmir). We found that the colonies of the two montane A. cerana populations show dance-distance calibration curves with significantly shallower slopes than the tropical A. indica. Next, we transferred A. c. cerana colonies to Bangalore ([~] 2600 km away) to obtain calibration curves in the same location as A. indica. The common garden experiment confirmed this difference in slopes, implying that the lineages exhibit genetically fixed differences in dance-distance coding. However, the slopes of the calibration curves of the transferred A. c. cerana colonies were also significantly higher than those tested in Himachal Pradesh indicating an important effect of the environment. The differences in dance-distance coding between temperate and tropical A. cerana lineages resemble those described for A. mellifera suggesting that populations of both species independently evolved similar adaptations.

animal behavior and cognition↗

Cuticular hydrocarbon profiles of Himalayan bumble bees (Hymenoptera: Bombus Latreille) are species-specific and show local and elevation related variation

Bumble bees are important pollinators in natural environments and agricultural farmlands and are in particular adapted to harsh environments like high mountain habitats. In these environments, animals are exposed to low temperature and face the risk of desiccation. The Eastern Himalayas are one of the recognized biodiversity hotspots worldwide. The area covers subtropical rainforest with warm temperature and high precipitation as well as high mountain ranges with peaks reaching up to 6000 m, shaping a diverse floral and faunal community at the different altitudinal zones. We investigated the cuticular hydrocarbon profiles of four bumble bee species occurring at different elevational ranges in Arunachal Pradesh, the northeast most state in India. At 17 locations along an elevational gradient we collected workers of two species from lower elevations (B. albopleuralis and B. breviceps; [~] 100m - 3000m asl) and two species from higher elevations (B. prshewalskyi and B. mirus; [~] 2800m - 4,500m asl). The CHC profiles of all four species showed a significant degree of variation in the composition of hydrocarbons, indicating species specificity. We also found clear correlation with elevation. The weighted mean chain length of the hydrocarbons significantly differed between the low and high altitudinal species, and the proportion of saturated hydrocarbons in CHC profiles significantly increased with the elevational range of the bumble bee species. Thus, these four species of bumble bees in the eastern Himalayas seem to adapt their CHC composition to elevation by decreasing water permeability of their cuticle, similar to insects living in dry mountains or deserts habitats.

ecology↗

Temporal effects of sugar intake on fly local search and honey bee dance behaviour

Honey bees communicate navigational information of profitable food to nestmates via dance, a small scale walking pattern. Hungry flies and honey bee foragers initiate a sugar-elicited local search that involves path integration and show similarities with dance behaviour. Using a comparative approach, we explored the temporal dynamics of initiation of local search and dance in flies and honey bees, respectively. Passive displacement experiments showed that feeding and initiation of search can be spatially dissociated in both species. Sugar intake increased the probability to initiate a search but onset of walking starts the path integration system guiding the search. When prevented from walking, the motivation to begin a path integration-based search was sustained for 3 min after sugar intake in flies and bees. In flies, the behavioural parameters of search were significantly reduced for 3 min but were higher than flies that were given no sugar stimulus, indicating some degree of meander. These results suggest that sugar elicits two independent behavioural responses: path integration and increased turning, and initiation and duration of path integration system is temporally more restricted. Honey bee dance experiments demonstrated that the motivation of foragers to initiate dance was sustained for 15 min, whereas the number of circuits declined after 3 min. Based on our findings, we propose that the food-intake during foraging has the capability to activate the path integration system in flies and honey bees, and this interaction might have been elaborated during evolution to guide the walking pattern of the honey bee dance.

animal behavior and cognition↗

Environment dependent benefits of individual differences in the recruitment behaviour of honey bees

Inter-individual differences in behaviour within the members of a social group can affect the groups productivity. In eusocial insects, individual differences amongst workers in a colony play a central role division of labour and task allocation. Extensive empirical and theoretical work has highlighted variation in response thresholds as a proximate mechanism underlying individual behavioural differences and hence division of labour. However, other response parameters, like response probability and intensity, can affect these differences. In this study, we first extended a previously published agent-based model on honey bee foraging to understand the relative importance of response (dance) probability and response (dance) intensity in the task of recruitment. Comparing variation obtained from the simulations with previously published empirical data, we found that response intensity plays a more important role than probability in producing consistent inter-individual differences in recruitment behaviour. We then explored the benefits provided by this individual variation in recruitment behaviour to the colonys collective foraging effort under different environmental conditions. Our results revealed that individual variation leads to a greater energetic yield per forager, but only when food is abundant. Our study highlights the need to consider all response parameters while studying division of labour and adds to the growing body of evidence linking individual variation in behavioural responses to the success of social groups.

animal behavior and cognition↗

Conserved hormonal and molecular mechanisms underlying behavioural maturation in open- and cavity-nesting honey bees

Division of labour in honey bees is based on a process of behavioural development where the worker bee successively performs different tasks at different ages. Workers start with tasks related to brood care and nest maintenance and move on to become foragers. This process of worker behavioural maturation is well studied in Apis mellifera. Juvenile hormone is one of the major drivers of this behavioural maturation, which is also accompanied by changes in brain physiology and anatomy including changes in neuronal gene expression and connections of neurons. Recent studies have identified whole networks of genes associated with specific tasks like nursing, guarding and foraging. Based on this detailed knowledge in A. mellifera, we ask whether major characteristics of the behavioural maturation process and the underlying hormonal and molecular changes are similar or different in two other honey bee species, the phylogenetically ancestral open-nesting A. florea and the more derived cavity-nesting A. cerana. Our behavioural studies show that workers of A. florea exhibit a slower pace of behavioural maturation and on average start foraging at a later age. However, the basic hormonal and molecular changes associated with onset of foraging are similar between both species. Based on our findings, we propose that evolution of accelerated behavioural maturation in cavity-nesting species is likely attributed to changes in the temporal dynamics of juvenile hormone titres.

molecular biology↗

Search behavior of individual foragers involves neurotransmitter systems characteristic for social scouting

In honey bees search behavior occurs as social and solitary behavior. In the context of foraging, searching for food sources is performed by behavioral specialized foragers, the scouts. When the scouts have found a new food source, they recruit other foragers (recruits). These recruits never search for a new food source on their own. However, when the food source is experimentally removed, they start searching for that food source. Our study provides a detailed description of this solitary search behavior and the variation of this behavior among individual foragers. Furthermore, mass spectrometric measurement showed that the initiation and performance of this solitary search behavior is associated with changes in glutamate, GABA, histamine, aspartate and the catecholaminergic system in the optic lobes and central brain area. These findings strikingly correspond with the results of an earlier study that showed that scouts and recruits differ in the expression of glutamate and GABA receptors. Together, the results of both studies provide first clear support for the hypothesis that behavioral specialization in honey bees is based on adjusting modulatory systems involved in solitary behavior to increase the probability or frequency of that behavior.

animal behavior and cognition↗

Do honey bee species differ in the odometer used for the waggle dance?

Honey bees estimate distances to food sources using image motion experienced on the flight path and they use this measure to tune the waggle phase duration in their dance communication. Most studies on the relationship between experienced optic flow and the dance-related odometer are based on experiments with Apis mellifera foragers trained into a small tunnel with black and white patterns which allowed quantifiable changes in the optic flow. In this study we determined the calibration curves for foragers of the two Asian honey bee species, A. florea and A. cerana, in two different natural environments with clear differences in the vegetation conditions and hence visual contrast. We found that the dense vegetation condition (with higher contrast) elicited a more rapid increase in the waggle phase duration with distance than the sparse vegetation in A. florea but not in A. cerana. Visual contrast did not affect the perception of the food reward, measured as the number of dance circuits produced per distance, in both species. Our findings suggest that contrast sensitivity of the waggle dance odometer, or other aspects of flight behaviour, might vary among honey bee species.

animal behavior and cognition↗

Cryo-EM structural studies of the agonist complexed human TRPV4 ion-channel reveals novel structural rearrangements resulting in an open-conformation

The human transient receptor potential vanilloid 4 (hTRPV4) ion channel plays a critical role in a variety of biological processes. Whilst the activation of hTRPV4 gating properties has been reported for a broad spectrum of stimuli, including synthetic 4-phorbols, the molecular basis of the activation is poorly understood. Here we report the novel cryo-EM structure of the hTRPV4 determined in the presence of the archetypical phorbol acid agonist, 4-PDD. Complementary mutagenesis experiments support the EM-identified binding site as well as allowing rationalization of disruptive mutants located outside of the 4-PDD binding site. This work represents the first structural information of hTRPV4 in a ligand-induced open conformation. Together, our data reveal the underlying molecular mechanisms resulting in the opening of the central pore and ion-channel activation and provide a structural template for designing inhibitors targeting the open-state conformation of hTRPV4.

molecular biology↗

Similarities in the behaviour of dance followers among honey bee species suggests a conserved mechanism of dance communication

Group living organisms rely on intra-group communication to adjust individual and collective behavioural decisions. Complex communication systems are predominantly multimodal and combine modulatory and information bearing signals. The honey bee waggle dance, one of the most elaborate forms of communication in invertebrates, stimulates nestmates to search for food and communicates symbolic information about the location of the food source. Previous studies on the dance behaviour in diverse honey bee species demonstrated distinct differences in the combination of visual, auditory, olfactory, and tactile signals produced by the dancer. We now studied the behaviour of the receivers of the dance signals, the dance followers, to explore the significance of the different signals in the communication process. In particular, we ask whether there are differences in the behaviour of dance followers between the 3 major Asian honey bee species, A. florea, A. dorsata and A. cerana, and whether these might correlate with the differences in the signals produced by the dancing foragers. Our comparison demonstrates that the behaviour of the dance followers is highly conserved across all 3 species despite the differences in the dance signals. The highest number of followers was present lateral to the dancer throughout the waggle run, and the mean body orientation of the dance followers with respect to the waggle dancer was close to 90{degrees} throughout the run for all 3 species. These findings suggest that dance communication might be more conserved than implied by the differences in the signals produced by the dancer. Along with studies in A. mellifera, our results indicate that all honey bee species rely on tactile contacts between the dancer and follower to communicate spatial information. The cues and signals that differ between the species may be involved in attracting the followers towards the dancer in the different nest environments.

animal behavior and cognition↗

Sex-specific molecular specialization and activity rhythm dependent gene expression changes in honey bee antennae

Eusocial insects, like honey bees, which show an elaborate division of labor involving morphologically and physiologically specialized phenotypes provide a unique toolkit to study molecular underpinnings of behavior as well as neural processing. In this study, we performed an extensive RNA-seq based comparison of gene expression levels in the antennae of honey bee drones and foragers collected at different time of days and activity states to identify molecules involved in peripheral olfactory processing and provide insights into distinct strategies in sensory processing. First, honey bee drone and worker antennae differ in the number of olfactory receptor genes (ORs) showing a biased expression pattern. Only 19 Ors were higher expressed in drone antennae, whereas 54 Ors were higher expressed in workers. Second, drone antennae showed predominant higher expression of genes involved in energy metabolism, and worker antennae showed a higher expression of genes involved in neuronal communication. Third, drones and afternoon-trained foragers showed similar daily changes in the expression of major clock genes, per and cry2. Most of the other genes showing changes with the onset of daily activity were specific to drones and foragers suggesting sex-specific circadian changes in antennae. Drone antennae are specialized to detect small amounts of queens pheromone and quickly respond to changes in pheromone concentration involving energetically costly action potentials, whereas forager antennae are predominantly involved in behavioral context dependent detection and discrimination of complex odor mixtures which requires mechanisms of sensory filtering and neural plasticity.

animal behavior and cognition↗

Species composition and altitudinal distribution of bumble bees (Hymenoptera: Apidae: Bombus) in the East Himalaya, Arunachal Pradesh, India

The East Himalaya is one of the worlds most biodiverse ecosystems. Yet, very little is known about the abundance and distribution of many plant and animal taxa in this region. Bumble bees are a group of cold-adapted and high altitude insects that fulfill an important ecological and economical function as pollinators of wild and agricultural flowering plants and crops. The Himalayan mountain range provides ample suitable habitats for bumble bees. Himalayan bumble bees have been studied systematically for a few decades now, with the main focus on the western region, while the eastern part of the mountain range received little attention and only a few species are genuinely reported. During a three-year survey, we collected more than 700 bumble bee specimens of 21 species in Arunachal Pradesh, the largest of the north-eastern states of India. We collected a range of species that were previously known from a very limited number of collected specimens, which highlights the unique character of the East Himalayan ecosystem. Our results are an important first step towards a future assessment of species distribution, threat and conservation. We observed clear altitudinal patterns of species diversity, which open important questions about the functional adaptations that allow bumble bees to thrive in this particularly moist region in the East Himalaya.

zoology↗

Making honey bees lie: experimental dissociation of flight experience and dance communication.

Honey bees use their dance to communicate flight distance and direction of a food source to their nest mates in the hive. How bees transpose flight information to generate a corresponding walking (dance) behavior is still unknown. We now present a detailed study of the changes in dance duration of individual bees after shifting feeder distance. Our experiments indicated that most bees needed two or more foraging trips to the new position before showing an updated dance duration. In addition, only a few bees significantly changed dance duration immediately, whereas most bees first produced intermediary durations. Double shift experiments showed that under certain conditions bees do not update dance duration but continued to perform dance duration for the previously visited feeder position. We propose that generation of dance information involves two memory contents one for newly acquired and one for previously stored distance information.\n\nOne Sentence SummaryGeneration of dance information is temporally separated from immediate flight experience and involves two different memory contents.

animal behavior and cognition↗

Investigating the viral ecology of global bee communities with high-throughput metagenomics

Bee viral ecology is a fascinating emerging area of research: viruses exert a range of effects on their hosts, exacerbate the impacts of other environmental stressors, and, importantly, are readily shared across multiple bee species in a community. However, our understanding of bee viral communities is limited, as it is primarily derived from studies of North American and European Apis mellifera populations. Here, we examined viruses in populations of A. mellifera and 11 other bee species from 9 countries, across 5 continents and Oceania. We developed a novel pipeline to rapidly, inexpensively, and robustly screen for bee viruses. This pipeline includes purification of encapsulated RNA/DNA viruses, sequence-independent amplification, high throughput sequencing, integrated assembly of contigs, and filtering to identify contigs specifically corresponding to viral sequences. We identified sequences corresponding to (+)ssRNA, (-)ssRNA, dsRNA, and ssDNA viruses. Overall, we found 127 contigs corresponding to novel viruses (i.e. previously not observed in bees), with 29 represented by >0.1 % of the reads in a given sample. These viruses and viral families were distributed across multiple regions and species. This study provides a robust pipeline for metagenomics analysis of viruses, and greatly expands our understanding of the diversity of viruses found in bee communities.

genomics↗

Time-restricted foraging under natural light/dark condition shifts the molecular clock in the honey bee, Apis mellifera

Honey bees have a remarkable sense of time and individual honey bee foragers are capable to adjust their foraging activity with respect to the time of food availability. Although, there is plenty of experimental evidence that foraging behavior is guided by the circadian clock, nothing is known about the underlying cellular and molecular mechanisms. Here we present a first study exploring whether the time-restricted foraging under natural light-dark condition affects the molecular clock in honey bees. In an enclosed flight chamber (12m x 4m x 4m), food was presented either for 2 hours in the morning or 2 hours in the afternoon for several consecutive days and daily cycling of the two major clock genes, cryptochrome2 (cry2) and period (per), were analyzed in three different tissues involved in feeding-related behaviors: brain, antennae and subesophageal ganglion (SEG). We found that morning and afternoon trained foragers showed significant phase-differences in the cycling of both clock genes in all three tissues. Furthermore, the phase-differences were more pronounced when the feeder was scented with the general plant odor linalool. Our results clearly demonstrate that foraging time functions as a strong circadian Zeitgeber in honey bees. More surprisingly our results suggest that foraging time might have the potential to override the entrainment effect of the light-dark cycle.

neuroscience↗