@article {152131, title = {Avenues towards reconciling wild and managed bee proponents.}, journal = {Trends Ecol Evol}, volume = {40}, year = {2025}, month = {2024 Dec 06}, pages = {7-10}, abstract = {

Bees are crucial for food security and biodiversity. However, managed bees are increasingly considered drivers of wild bee declines, leading to stakeholder conflicts and restrictive policies. We propose avenues to reconcile wild and managed bee proponents and point out knowledge gaps that hinder the development of evidence-based policies.

}, issn = {1872-8383}, doi = {10.1016/j.tree.2024.11.009}, author = {Beaurepaire, Alexis L and Hogendoorn, Katja and Kleijn, David and Otis, Gard W and Potts, Simon G and Singer, Theresa L and Boff, Samuel and Pirk, Christian and Settele, Josef and Paxton, Robert J and Raine, Nigel E and Tosi, Simone and Williams, Neal and Klein, Alexandra-Maria and Le Conte, Yves and Campbell, Joshua W and Williams, Geoffrey R and Marini, Lorenzo and Brockmann, Axel and Sgolastra, Fabio and Boyle, Natalie and Neuditschko, Markus and Straub, Lars and Neumann, Peter and Charri{\`e}re, Jean-Daniel and Albrecht, Matthias and Dietemann, Vincent} } @article {140656, title = {Cuticular Hydrocarbon Profiles of Himalayan Bumble Bees (Hymenoptera: Bombus Latreille) are Species-Specific and Show Elevational Variation.}, journal = {J Chem Ecol}, year = {2024}, month = {2024 Mar 12}, abstract = {

Bumble bees are important pollinators in natural environments and agricultural farmlands, and they 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 7,000\ m, shaping a diverse floral and faunal community at the different elevational zones. To identify possible adaptation strategies, we investigated the cuticular hydrocarbon profiles of four bumble bee species occurring at different elevational ranges in Arunachal Pradesh, the northeastern 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; ~ 100\ m - 3,000\ m asl) and two species from higher elevations (B. prshewalskyi and B. mirus; ~ 2,800\ m - 4,500\ m 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 elevation species, and the proportion of saturated hydrocarbons in CHC profiles significantly increased with the elevational range of the bumble bee species. Our results indicate that bumble bees living at high elevations reduce the risk of water loss by adapting their CHC composition on their cuticle, a phenomenon that has also been found in other insects like ants and fruit flies.

}, issn = {1573-1561}, doi = {10.1007/s10886-024-01486-x}, author = {Narah, Jaya and Streinzer, Martin and Chakravorty, Jharna and Megu, Karsing and Spaethe, Johannes and Brockmann, Axel and Schmitt, Thomas} } @article {144794, title = {Tropical and montane Apis cerana show distinct dance-distance calibration curves.}, journal = {J Exp Biol}, year = {2024}, month = {2024 Jun 10}, abstract = {

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 of social bee species 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 populatiInons of both species independently evolved similar adaptations.

}, issn = {1477-9145}, doi = {10.1242/jeb.247510}, author = {A K, Bharath Kumar and George, Ebi Antony and Brockmann, Axel} } @article {129506, title = {Diverse communication strategies in bees as a window into adaptations to an unpredictable world.}, journal = {Proc Natl Acad Sci U S A}, volume = {120}, year = {2023}, month = {2023 Jun 13}, pages = {e2219031120}, abstract = {

Communication is a fundamental feature of animal societies and helps their members to solve the challenges they encounter, from exploiting food sources to fighting enemies or finding a new home. Eusocial bees inhabit a wide range of environments and they have evolved a multitude of communication signals that help them exploit resources in their environment efficiently. We highlight recent advances in our understanding of bee communication strategies and discuss how variation in social biology, such as colony size or nesting habits, and ecological conditions are important drivers of variation in communication strategies. Anthropogenic factors, such as habitat conversion, climate change, or the use of agrochemicals, are changing the world bees inhabit, and it is becoming clear that this affects communication both directly and indirectly, for example by affecting food source availability, social interactions among nestmates, and cognitive functions. Whether and how bees adapt their foraging and communication strategies to these changes represents a new frontier in bee behavioral and conservation research.

}, keywords = {Acclimatization, Animals, Bees, Communication, Ecosystem}, issn = {1091-6490}, doi = {10.1073/pnas.2219031120}, author = {Alves, Denise A and George, Ebi A and Kaur, Rajbir and Brockmann, Axel and Hrncir, Michael and Gr{\"u}ter, Christoph} } @article {137337, title = {Land Cover Mapping of Bengaluru{\textquoteright}s Urban and Surrounding Area with Spatiotemporal Open-source Remote Sensing Data}, journal = {SENSORS AND MATERIALS}, volume = {35}, year = {2023}, month = {12/2023}, pages = {3829-3849}, abstract = {

The rapid urbanization observed in Asian tropics has resulted in extensive landscape transformations, giving rise to novel challenges such as conflicts of interest among citizens and threats to biodiversity. To facilitate informed urban management policies, there is a pressing need for contemporary land use and cover maps that provide precise insights into the evolving landscape. In this paper, we present the city of Bengaluru, India (covering an area of 365,879 ha) as a case study. We introduce an open-source-driven pipeline method capable of generating an updated 11-class land cover map at a high resolution of 10 m, achieving a global F1 score of 0.82. Notably, our proposed pipeline represents a pioneering solution that effectively addresses the persistent issue of cloud cover caused by monsoons, enhancing the utility of such maps for urban management, and planning in rapidly evolving regions.

}, doi = {10.18494/SAM4627}, author = {Grison, Sylvain and Siddaganga, Rajath and Singh, Renu and Hegde, Shrihari and Brockmann, Axel and Krishnan, Smitha and Guo, Wei} } @article {135864, title = {Nutritional properties of giant water bug, a traditional edible insect species of North-East India.}, journal = {Bioengineered}, volume = {14}, year = {2023}, month = {2023 Dec}, pages = {2252669}, abstract = {

Edible insects play an important role in human health and food security. Among those, the Giant water bug, (Lep.\& Ser.) is a widely used edible insect known for its aroma, flavor, and therapeutic purposes. In the present study, we investigated the nutritional profile, natural habitat, and feeding behavior of in aquarium conditions. A comparative analysis of male and female insects{\textquoteright} aroma contents and fatty acid (FA) profiles was also conducted. A dry fried male insect yielded volatile oil of 0.96\%/2 g body weight, whereas a dry fried female yielded 0.48\%/5.36 g of body weight. In terms of lipids, fresh male insects had 0.15\%/5.42 g of body weight and fresh female insects had 0.28\%/9.48 g of body weight. There are 24 volatile compounds specific to males, 37 specific to females, and 13 commons to both were identified. 2-Hexen-1-ol, acetate, (Z)- which smells like banana, was prevalently found in males while 4-Octene, 2,6-dimethyl-, [S-(Z)] was prevalently found in female insects. Fatty acids profile analysis detected 32 FA with 12 unique FA from males whereas 22 FA and 3 unique FA were identified from female insects. The SFA percentage present in males and females was 77.44\% and 85.21\%. Males had 6.78\% MUFA content while females have 4.75\%. Males have 18\% PUFA content enriched with DHA, and EPA, while females had 10.04\%. This study revealed that with the presence of a banana-like smell of volatile compound and more MUFA and PUFA in males, the native people of North-East India preferred male over female insects for entomophagy.

}, keywords = {Animals, Body Weight, Edible Insects, Feeding Behavior, Female, India, Male, Nutritive Value}, issn = {2165-5987}, doi = {10.1080/21655979.2023.2252669}, author = {Devi, Mutum R and Ummalyma, Sabeela B and Brockmann, Axel and Raina, Vishakha and Rajashekar, Yallappa} } @article {137336, title = {Opportunities and challenges in Asian bee research and conservation}, journal = {BIOLOGICAL CONSERVATION }, volume = {285}, year = {2023}, month = {09/23}, pages = {110173}, abstract = {

The challenges of bee research in Asia are unique and severe, reflecting different cultures, landscapes, and faunas. Strategies and frameworks developed in North America or Europe may not prove applicable. Virtually none of these species have been assessed by the IUCN and there is a paucity of public data on even the basics of bee distribution. If we do not know the species present, their distribution and threats, we cannot protect them, but our knowledge base is vanishingly small in Asia compared to the rest of the world. To better understand and meet these challenges, this perspective conveys the ideas accumulated over hundreds of years of cumulative study of Asian bees by the authors, including academic, governmental, and other researchers from 13 Asian countries and beyond. We outline the special circumstances of Asian bee research and the current state of affairs, highlight the importance of highly social species as flagships for the lesser-known solitary bees, the dire need for further research for food security, and identify target research areas in need of further study. Finally, we outline a framework via which we will catalyze future research in the region, especially via governmental and other partnerships necessary to effectively conserve species.

}, doi = {10.1016/j.biocon.2023.110173}, author = {Warrit, Natapot and Ascher, John and Basu, Parthib and Belavadi, Vasuki and Brockmann, Axel and et al} } @article {133183, title = {Temporal effects of sugar intake on fly local search and honey bee dance behaviour.}, journal = {J Comp Physiol A Neuroethol Sens Neural Behav Physiol}, year = {2023}, month = {2023 Aug 25}, abstract = {

Honey bees communicate flight navigational information of profitable food to nestmates via their dance, a small-scale walking pattern, inside the nest. Hungry flies and honey bee foragers exhibit a sugar-elicited search involving path integration that bears a resemblance to dance behaviour. This study aimed to investigate the temporal dynamics of the initiation of sugar-elicited search and dance behaviour, using a comparative approach. Passive displacement experiments showed that feeding and the initiation of search could be spatially and temporally dissociated. Sugar intake increased the probability of initiating a search but the actual onset of walking triggers the path integration system to guide the search. When prevented from walking after feeding, flies and bees maintained their motivation for a path integration-based search for a duration of 3\ min. In flies, turning and associated characters were significantly reduced during this period but remained higher than in flies without sugar stimulus. These results suggest that sugar elicits two independent behavioural responses: path integration and increased turning, with the initiation and duration of path integration system being temporally restricted. Honey bee dance experiments demonstrated that the motivation of foragers to initiate dance persisted for 15\ min, while the number of circuits declined after 3\ min following sugar ingestion. Based on these findings, we propose that food intake during foraging increases the probability to initiate locomotor behaviours involving the path integration system in both flies and honey bees, and this ancestral connection might have been co-opted and elaborated during the evolution of dance communication by honey bees.

}, issn = {1432-1351}, doi = {10.1007/s00359-023-01670-6}, author = {Shakeel, Manal and Brockmann, Axel} } @article {137339, title = {Tracking Sugar-Elicited Local Searching Behavior in Drosophila.}, journal = {J Vis Exp}, year = {2023}, month = {2023 Nov 17}, abstract = {

Foraging behavior is essential for the survival of organisms as it enables them to locate and acquire essential food resources. In Drosophila, hunger triggers a distinct search behavior following the consumption of small quantities of a sugar solution. This report presents a simple experimental setup to study sugar-elicited search behavior with the aim of uncovering the underlying mechanisms. Minute quantities of concentrated sugar solution elicit sustained searching behavior in flies. The involvement of path integration in this behavior has been established, as flies utilize their trajectory to return to the sugar location. The most recent findings provide evidence of temporal modulation in the initiation and intensity of the search behavior after sugar intake. We have also used this setup for artificial activation of specific taste-receptor neurons in the pharynx, which elicits the search behavior. The Drosophila neurogenetic toolkit offers a diverse array of tools and techniques that can be combined with the sugar-elicited search behavior paradigm to study the neural and genetic mechanisms underlying foraging. Understanding the neural basis of hunger-driven searching behavior in flies contributes to the field of neurobiology as a whole, offering insights into the regulatory mechanisms that govern feeding behaviors not only in other organisms but also in humans.

}, keywords = {Animals, Appetitive Behavior, Carbohydrates, Drosophila, Drosophila melanogaster, Drosophila Proteins, Feeding Behavior, Humans, Sugars}, issn = {1940-087X}, doi = {10.3791/65955}, author = {Shakeel, Manal and Kaushik, Shivam and Tanimura, Teiichi and Brockmann, Axel and Kain, Pinky} } @article {115811, title = {Apis laboriosa confirmed by morphometric and genetic analyses of giant honey bees (Hymenoptera, Apidae) from sites of sympatry in Arunachal Pradesh, North East India}, journal = {APIDOLOGIE}, volume = {53}, year = {2022}, month = {08/2022}, pages = {47}, abstract = {

Two potentially different species of giant honey bees (subgenus Megapis) are endemic to India: Apis dorsata, the widespread low elevation form, and Apis laboriosa of the Pan-Himalayan region. Although they differ morphologically, behaviorally, and genetically, the species status of A. laboriosa remains unresolved. We sampled bees in three widely separated regions of Arunachal Pradesh, North East India, where these two taxa occurred sympatrically. We measured morphological characters of worker bees and conducted principal component analyses of two data sets (size-independent traits and the full set of characters excluding ratios). We also sequenced approximately 500 bp of the mtDNA cytochrome c oxidase subunit I (COI) and generated a phylogenetic tree. In all analyses, A. dorsata and A. laboriosa separated into well-defined groups, and with no bees showing traits suggestive of hybridization, regardless of where the species were collected. The a priori identifications of all specimens based on thoracic hair and abdominal color were verified by the analyses. Our results confirm that A. laboriosa is a valid species.

}, doi = {10.1007/s13592-022-00956-z}, author = {Kitnya, Nyaton and Otis, Gard W. and Chakravorty, Jharna and Smith, Deborah R. and Brockmann, Axel} } @article {116184, title = {Environment-dependent benefits of interindividual variation in honey bee recruitment}, journal = {ANIMAL BEHAVIOUR}, volume = {192}, year = {2022}, month = {10/2022}, pages = {9-26}, abstract = {

Interindividual differences in behaviour within the members of a social group can affect the group{\textquoteright}s productivity. In eusocial insects, individual differences between workers in a colony play a central role in 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 also affect these differences. In this study, we first extended a previously published agent-based model on honey bee, Apis mellifera, 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 played a more important role than probability in producing consistent interindividual differences in recruitment behaviour. We then explored the benefits provided by this individual variation in recruitment behaviour to the colony{\textquoteright}s collective foraging effort under different environmental conditions. We found that individual variation led to a greater energy yield per forager, but only when food was 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. (C) 2022 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

}, doi = {10.1016/j.anbehav.2022.07.011}, author = {Rajagopal, Supraja and Brockmann, Axel and George, Ebi Antony} } @article {115044, title = {Increased complexity of worker CHC profiles in Apis dorsata correlates with nesting ecology.}, journal = {PLoS One}, volume = {17}, year = {2022}, month = {2022}, pages = {e0271745}, abstract = {

Cuticular hydrocarbons (CHC) are known to serve as discrimination cues and will trigger defence behaviour in a plethora of eusocial insects. However, little is known how about nestmate recognition ability selects for CHC diversification. In this study we investigate differences in CHC composition of four major honey bee species with respect to the differences in their nesting behavior. In contrast to A. mellifera, A. cerana and A. florea, the giant honey bee A. dorsata prefers to build their nests in aggregations with very small spatial distances between nests, which increases the probability of intrusions. Thus, A. dorsata exhibits a particularly challenging nesting behavior which we hypothesize should be accompanied with an improved nestmate recognition system. Comparative analyses of the worker CHC profiles indicate that A. dorsata workers exhibit a unique and more complex CHC profile than the other three honey bee species. This increased complexity is likely based on a developmental process that retains the capability to synthesize methyl-branched hydrocarbons as adults. Furthermore, two sets of behavioral experiments provide evidence that A. dorsata shows an improved nestmate discrimination ability compared to the phylogenetically ancestral A. florea, which is also open-nesting but does not form nest aggregations. The results of our study suggest that ecological traits like nesting in aggregation might be able to drive CHC profile diversification even in closely related insect species.

}, keywords = {Animals, Bees, Cues, Hydrocarbons, Nesting Behavior}, issn = {1932-6203}, doi = {10.1371/journal.pone.0271745}, author = {Maihoff, Fabienne and Bohlke, Kyte and Brockmann, Axel and Schmitt, Thomas} } @article {91959, title = {Distance estimation by Asian honey bees in two visually different landscapes.}, journal = {J Exp Biol}, year = {2021}, month = {2021 Apr 01}, abstract = {

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 dance-related odometer are based on experiments with foragers trained into small tunnels with black and white patterns which allowed quantifiable changes in the optic flow. In this study, we determined the calibration curves of two Asian honey bee species, and , 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 but not in Our findings suggest that contrast sensitivity of the waggle dance odometer might vary among honey bee species.

}, issn = {1477-9145}, doi = {10.1242/jeb.242404}, author = {George, Ebi Antony and Thulasi, Neethu and Kohl, Patrick L and Suresh, Sachin and Rutschmann, Benjamin and Brockmann, Axel} } @article {101545, title = {A hard day{\textquoteright}s night: Patterns in the diurnal and nocturnal foraging behavior of Apis dorsata across lunar cycles and seasons.}, journal = {PLoS One}, volume = {16}, year = {2021}, month = {2021}, pages = {e0258604}, abstract = {

The giant honey bee Apis dorsata is unusual in being able to forage during both the day and the night. To date, the extent of this unique nocturnal foraging behavior and the environmental factors correlating with it have not been deeply investigated. We conducted the first systematic investigation into the nocturnal behavior of A. dorsata in Southern India by tracking the daily and nightly foraging activity of A. dorsata colonies in an urban environment for 8 months, over multiple seasons and lunar cycles. We found strong evidence that A. dorsata can behave in a manner that is "cathemeral" (active over the entire diel cycle) when environmental illumination is sufficient for nocturnal flight. However, workers were not always active even when the environment should have been bright enough for them to forage, suggesting that their nocturnal foraging behavior was also affected by seasonal changes in resource availability. The foraging activity observed during the day versus twilight versus night differed between seasons; notably, nocturnal activity rates were higher than diurnal activity rates during the winter. We found that at our study site A. dorsata routinely exhibits both diurnal and crepuscular activity, foraging just as intensely during the short twilight hours as during the day. The high foraging activity observed during the twilight and nighttime hours shows that A. dorsata colonies can extend their foraging beyond the daylight hours and reveals that foraging during these dimly lit hours is an integral part of their foraging ecology. This evidence of the importance of nocturnal and crepuscular foraging by A. dorsata paves the way for future studies examining the role of this species in nocturnal pollination networks, the contribution of nocturnal foraging to colony-level nutrition and energy budget, and the evolution of this unusual behavior. Future work comparing nocturnal activity in light polluted urban environments versus unpolluted natural environments is particularly encouraged to determine the generalizability of these findings.

}, issn = {1932-6203}, doi = {10.1371/journal.pone.0258604}, author = {Young, Allison M and Kodabalagi, Sangamesh and Brockmann, Axel and Dyer, Fred C} } @article {92881, title = {Nesting ecology does not explain slow-fast cognitive differences among honeybee species.}, journal = {Anim Cogn}, year = {2021}, month = {2021 Apr 27}, abstract = {

Slow-fast behavioral and life history differences have been tied to slow-fast variation in cognition that is part of the general speed-accuracy tradeoff. While there is growing evidence for such cognitive variation and its association with behavior and life history at the intraspecific level, it is unknown if a similar relationship extends to the interspecific level. Since interspecific differences in cognition have been shown to be a function of ecology and life history, such differences should be reflected in multiple traits that comprise the slow-fast cognitive axis. In this study, by measuring multiple cognitive traits in individuals, we tested for differences in the cognitive phenotype among four honeybee species, which differ in their behavior and life history in a manner that is associated with differences in their nesting ecology. Our results indicate that a set of cognitive traits consistently covary within each species, resulting in slow and fast cognitive phenotypes that largely meet the predictions of the speed-accuracy tradeoff. We also find that the four species group into two distinct clusters on a slow-fast cognitive axis, although their positions do not align with the known differences in their life history and nesting ecology. We instead find that cognitive differences among the four species are correlated with their brain size. We discuss the possible implications of these results for the role of ecology on slow-fast cognitive differences and the evolution of cognition.

}, issn = {1435-9456}, doi = {10.1007/s10071-021-01515-2}, author = {Tait, Catherine and Brockmann, Axel and Naug, Dhruba} } @article {96165, title = {Search Behavior of Individual Foragers Involves Neurotransmitter Systems Characteristic for Social Scouting}, journal = {Front. Insect Sci}, year = {2021}, month = {06/2021}, abstract = {

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.

}, doi = {10.3389/finsc.2021.664978}, author = {Chatterjee, Arumoy and Bais, Deepika and Brockmann, Axel and Ramesh, Divya} } @article {96102, title = {Tyramine 1 Receptor Distribution in the Brain of Corbiculate Bees Points to a Conserved Function.}, journal = {Brain Behav Evol}, year = {2021}, month = {2021 Jul 15}, pages = {1-13}, abstract = {

Sucrose represents an important carbohydrate source for most bee species. In the Western honeybee (Apis mellifera) it was shown that individual sucrose responsiveness correlates with the task performed in the colony, supporting the response threshold theory which states that individuals with the lowest threshold for a task-associated stimuli will perform the associated task. Tyramine was shown to modulate sucrose responsiveness, most likely via the tyramine 1 receptor. This receptor is located in brain areas important for the processing of gustatory stimuli. We asked whether the spatial expression pattern of the tyramine 1 receptor is a unique adaptation of honeybees or if its expression represents a conserved trait. Using a specific tyramine receptor 1 antibody, we compared the spatial expression of this receptor in the brain of different corbiculate bee species, including eusocial honeybees, bumblebees, stingless bees, and the solitary bee Osmia bicornis as an outgroup. We found a similar labeling pattern in the mushroom bodies, the central complex, the dorsal lobe, and the gnathal ganglia, indicating a conserved receptor expression. With respect to sucrose responsiveness this result is of special importance. We assume that the tyramine 1 receptor expression in these neuropiles provides the basis for modulation of sucrose responsiveness. Furthermore, the tyramine 1 receptor expression seems to be independent of size, as labeling is similar in bee species that differ greatly in their body size. However, the situation in the optic lobes appears to be different. Here, the lobula of stingless bees is clearly labeled by the tyramine receptor 1 antibody, whereas this labeling is absent in other species. This indicates that the regulation of this receptor is different in the optic lobes, while its function in this neuropile remains unclear.

}, issn = {1421-9743}, doi = {10.1159/000517014}, author = {Thamm, Markus and Wagler, Katharina and Brockmann, Axel and Scheiner, Ricarda} } @article {74446, title = {Adaptive evolution of honeybee dance dialects.}, journal = {Proc Biol Sci}, volume = {287}, year = {2020}, month = {2020 Mar 11}, pages = {20200190}, abstract = {

Efficient communication is highly important for the evolutionary success of social animals. Honeybees (genus ) are unique in that they communicate the spatial information of resources using a symbolic {\textquoteright}language{\textquoteright}, the waggle dance. Different honeybee species differ in foraging ecology but it remains unknown whether this shaped variation in the dance. We studied distance dialects-interspecific differences in how waggle duration relates to flight distance-and tested the hypothesis that these evolved to maximize communication precision over the bees{\textquoteright} foraging ranges. We performed feeder experiments with , and in India and found that had the steepest dialect, i.e. a rapid increase in waggle duration with increasing feeder distance, had an intermediate, and had the lowest dialect. By decoding dances for natural food sites, we inferred that the foraging range was smallest in , intermediate in and largest in . The inverse correlation between foraging range and dialect was corroborated when comparing six (sub)species across the geographical range of the genus including previously published data. We conclude that dance dialects constitute adaptations resulting from a trade-off between the spatial range and the spatial accuracy of communication.

}, issn = {1471-2954}, doi = {10.1098/rspb.2020.0190}, author = {Kohl, Patrick L and Thulasi, Neethu and Rutschmann, Benjamin and George, Ebi A and Steffan-Dewenter, Ingolf and Brockmann, Axel} } @article {86474, title = {Downregulation of the tyrosine degradation pathway extends lifespan.}, journal = {Elife}, volume = {9}, year = {2020}, month = {2020 Dec 15}, abstract = {

Aging is characterized by extensive metabolic reprogramming. To identify metabolic pathways associated with aging, we analyzed age-dependent changes in the metabolomes of long-lived . Among the metabolites that changed, levels of tyrosine were increased with age in long-lived flies. We demonstrate that the levels of enzymes in the tyrosine degradation pathway increase with age in wild-type flies. Whole-body and neuronal-specific downregulation of enzymes in the tyrosine degradation pathway significantly extends lifespan, causes alterations of metabolites associated with increased lifespan, and upregulates the levels of tyrosine-derived neuromediators. Moreover, feeding wild-type flies with tyrosine increased their lifespan. Mechanistically, we show that suppression of ETC complex I drives the upregulation of enzymes in the tyrosine degradation pathway, an effect that can be rescued by tigecycline, an FDA-approved drug that specifically suppresses mitochondrial translation. In addition, tyrosine supplementation partially rescued lifespan of flies with ETC complex I suppression. Altogether, our study highlights the tyrosine degradation pathway as a regulator of longevity.

}, issn = {2050-084X}, doi = {10.7554/eLife.58053}, author = {Parkhitko, Andrey A and Ramesh, Divya and Wang, Lin and Leshchiner, Dmitry and Filine, Elizabeth and Binari, Richard and Olsen, Abby L and Asara, John M and Cracan, Valentin and Rabinowitz, Joshua D and Brockmann, Axel and Perrimon, Norbert} } @article {80780, title = {A field-based quantitative analysis of sublethal effects of air pollution on pollinators.}, journal = {Proc Natl Acad Sci U S A}, year = {2020}, month = {2020 Aug 10}, abstract = {

While the impact of air pollution on human health is well studied, mechanistic impacts of air pollution on wild systems, including those providing essential ecosystem services, are largely unknown, but directly impact our health and well-being. India is the world{\textquoteright}s largest fruit producer, second most populous country, and contains 9 of the world{\textquoteright}s 10 most polluted cities. Here, we sampled Giant Asian honey bees, , at locations with varying air pollution levels in Bangalore, India. We observed significant correlations between increased respirable suspended particulate matter (RSPM) deposition and changes in bee survival, flower visitation, heart rate, hemocyte levels, and expression of genes related to lipid metabolism, stress, and immunity. Lab-reared exposed to these same sites also exhibited similar molecular and physiological differences. Our study offers a quantitative analysis on the current impacts of air pollution on insects, and indicates the urgency for more nonhuman studies to accurately assess the effects of pollution on our natural world.

}, issn = {1091-6490}, doi = {10.1073/pnas.2009074117}, author = {Thimmegowda, Geetha G and Mullen, Susan and Sottilare, Katie and Sharma, Ankit and Mohanta, Saptashi Soham and Brockmann, Axel and Dhandapany, Perundurai S and Olsson, Shannon B} } @article {80779, title = {Geographical distribution of the giant honey bee Smith, 1871 (Hymenoptera, Apidae).}, journal = {Zookeys}, volume = {951}, year = {2020}, month = {2020}, pages = {67-81}, abstract = {

Worldwide pollinator declines have dramatically increased our need to survey and monitor pollinator distributions and abundances. The giant honey bee, , is one of the important pollinators at higher altitudes of the Himalayas. This species has a restricted distribution along the Himalayas and neighbouring mountain ranges of Asia. Previous assessments of its distribution, published more than 20 years ago, were based on museum specimens. Since then, 244 additional localities have been revealed through field trips by the authors, publications, and websites. We present a revised distribution for that better defines its range and extends it eastward to the mountains of northern Vietnam, southward along the Arakan Mountains to west-central Myanmar, into the Shillong Hills of Meghalaya, India, and northwestward in Uttarakhand, India. This species is generally found at elevations between 1000-3000 m a.s.l.. In northeastern India colonies occur during summer at sites as low as 850 m a.s.l. and some lower elevation colonies maintain their nests throughout the winter. Finally, we report three regions in Arunachal Pradesh, India, and nine locations in northern Vietnam, where we observed workers of and foraging sympatrically; their co-occurrence supports the species status of .

}, issn = {1313-2989}, doi = {10.3897/zookeys.951.49855}, author = {Kitnya, Nyaton and Prabhudev, M V and Bhatta, Chet Prasad and Pham, Thai Hong and Nidup, Tshering and Megu, Karsing and Chakravorty, Jharna and Brockmann, Axel and Otis, G W} } @article {59709, title = {Inter-individual variation in honey bee dance intensity correlates with expression of the foraging gene.}, journal = {Genes Brain Behav}, volume = {19}, year = {2020}, month = {19/Jan}, abstract = {

Individual behavioural differences in responding to the same stimuli is an integral part of division of labour in eusocial insect colonies. Among honey bee nectar foragers, individuals strongly differ in their sucrose responsiveness, which correlates with strong differences in behavioural decisions. In this study, we explored whether the mechanisms underlying the regulation of foraging are linked to inter-individual differences in the waggle dance activity of honey bee foragers. We first quantified the variation in dance activity amongst groups of foragers visiting an artificial feeder filled consecutively with different sucrose concentrations. We then determined for these foragers the sucrose responsiveness and the brain expression levels of three genes associated with food search and foraging; the foraging gene Amfor, octopamine receptor gene AmoctαR1 and insulin receptor AmInR-2. As expected, foragers showed large inter-individual differences in their dance activity, irrespective of the reward offered at the feeder. The sucrose responsiveness correlated positively with the intensity of the dance activity at the higher reward condition, with the more responsive foragers having a higher intensity of dancing. Out of the three genes tested, Amfor expression significantly correlated with dance activity, with more active dancers having lower expression levels. Our results show that dance and foraging behaviour in honey bees have similar mechanistic underpinnings and supports the hypothesis that the social communication behaviour of honey bees might have evolved by co-opting behavioural modules involved in food search and foraging in solitary insects.

}, issn = {1601-183X}, doi = {10.1111/gbb.12592}, author = {George, Ebi Antony and Br{\"o}ger, Ann-Kathrin and Thamm, Markus and Brockmann, Axel and Scheiner, Ricarda} } @article {78102, title = {Sex-specific molecular specialization and activity rhythm dependent gene expression in honey bee antennae.}, journal = {J Exp Biol}, year = {2020}, month = {2020 May 11}, abstract = {

We performed an RNA-seq based comparison of gene expression levels in the antennae of honey bee drones and time-trained foragers (workers) collected at different times of the day and different activity states. Interestingly, olfaction-related genes (i.e. odorant receptor (), odorant binding proteins (), carboxyl esterases () etc.) showed stable gene expression differences between drone and worker antennae. Drone antennae showed higher expression of 24 of which 21 belong to the clade X which comprises the receptor for the major queen pheromone compound 9-ODA. This high number of drone-biased suggests that more than previously expected play a role in sex-pheromone communication. In addition, we found higher expression levels for many non-olfaction related genes including (), and the potassium channel In contrast, workers showed higher expression of 67 which belong to different clades that are involved in pheromone communication as well as the perception of cuticular hydrocarbons and floral scents. Further, drone antennae showed higher expression of genes involved in energy metabolism, whereas worker antennae showed higher expression of genes involved in neuronal communication consistent with earlier reports on peripheral olfactory plasticity. Finally, drones that perform mating flight in the afternoon (innate) and foragers that are trained to forage in the afternoon (adapted) showed similar daily changes in the expression of two major clock genes, and Most of the other genes showing changes with time or onset of daily flight activity were specific to drones and foragers.

}, issn = {1477-9145}, doi = {10.1242/jeb.217406}, author = {Jain, Rikesh and Brockmann, Axel} } @article {85849, title = {Similarities in dance follower behaviour across honey bee species suggest a conserved mechanism of dance communication}, journal = {ANIMAL BEHAVIOUR}, volume = {169}, year = {2020}, month = {11/2020}, pages = {139-155}, abstract = {

Social communication systems are predominantly multimodal and can combine modulatory and information-bearing signals. The honey bee waggle dance, one of the most elaborate forms of social communication in animals, activates 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 concurrence of visual, auditory, olfactory and tactile signals produced by the dancer. We studied the behaviour of dance signal receivers, the dance followers, to explore the potential significance of different signals in the communication process. In particular, we asked whether the behaviour of dance followers differs between the three major Asian honey bee species, Apis florea, Apis dorsata and Apis cerana, and whether this might correlate with the differences in the signals produced by the dancing foragers. Our comparison demonstrated that the behaviour of the dance followers is highly similar across all three species. The mean body orientation of the dance followers with respect to the waggle dancer was close to 90 degrees throughout the run, with the majority positioning themselves lateral to the dancer. These findings suggest that the communication of spatial information might be more conserved than implied by the differences in the signals produced by the dancer. Along with studies in Apis mellifera, our results suggest 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 or increasing their motivation to start foraging in the different nest environments. (C) 2020 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

}, doi = {10.1016/j.anbehav.2020.09.011}, author = {George, Ebi Antony and Pimplikar, Smruti and Thulasi, Neethu and Brockmann, Axel} } @article {51229, title = {Apis florea workers show a prolonged period of nursing behavior}, journal = {Apidologie}, year = {2019}, month = {01/2019}, abstract = {

Studies on behavioral maturation and division of labor in open-nesting honey bee species are scarce as the bee curtain inhibits direct examination of intranidal behaviors. We observed and studied nursing behavior in Apis florea by attaching a foreign comb with open brood to a host colony. Several of the workers that explored the attached comb visited the cells with brood more often and spent more time in cells compared to empty cells. Workers seen inspecting and feeding the brood had well-developed hypopharyngeal glands compared to foragers of their own colony indicating that they are nurses performing nursing behavior. Further, introducing marked 1-day-old workers into the host colony and repeatedly attaching combs with open brood allowed us to estimate the age range of nursing behavior. In our experiments, A. florea workers started to perform significant nursing behavior 8 days after eclosion and continued to show nursing behavior until the age of 28 days, the end of our observation period. Thus, nursing behavior in A. florea appears to be substantially extended relative to A. mellifera .

}, doi = {10.1007/s13592-018-0618-7}, author = {Bhagavan, H and Brockmann, Axel} } @article {59721, title = {Honey bees flexibly use two navigational memories when updating dance distance information.}, journal = {J Exp Biol}, volume = {222}, year = {2019}, month = {2019 Jun 13}, abstract = {

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.

}, issn = {1477-9145}, doi = {10.1242/jeb.195099}, author = {Chatterjee, Arumoy and George, Ebi A and M V, Prabhudev and Basu, Pallab and Brockmann, Axel} } @article {45301, title = {Immediate early genes in social insects: a tool to identify brain regions involved in complex behaviors and molecular processes underlying neuroplasticity.}, journal = {Cell Mol Life Sci}, volume = {76}, year = {2019}, month = {2018 Oct 22}, pages = {637-651}, abstract = {

Social insects show complex behaviors and master cognitive tasks. The underlying neuronal mechanisms, however, are in most cases only poorly understood due to challenges in monitoring brain activity in freely moving animals. Immediate early genes (IEGs) that get rapidly and transiently expressed following neuronal stimulation provide a powerful tool for detecting behavior-related neuronal activity in vertebrates. In social insects, like honey bees, and in insects in general, this approach is not yet routinely established, even though these genes are highly conserved. First studies revealed a vast potential of using IEGs as neuronal activity markers to analyze the localization, function, and plasticity of neuronal circuits underlying complex social behaviors. We summarize the current knowledge on IEGs in social insects and provide ideas for future research directions.

}, issn = {1420-9071}, doi = {10.1007/s00018-018-2948-z}, author = {Sommerlandt, Frank M J and Brockmann, Axel and R{\"o}ssler, Wolfgang and Spaethe, Johannes} } @article {53188, title = {Learning of monochromatic stimuli in Apis cerana and Apis mellifera by means of PER conditioning.}, journal = {J Insect Physiol}, volume = {114}, year = {2019}, month = {2019 Feb 15}, pages = {30-34}, abstract = {

Honey bees are globally distributed and have received increased attention due to their high economic and ecological value for pollination, their exceptional eusocial lifestyle and complex behavioral repertoire. Interestingly, most research on learning and memory in honey bees has been performed in the Western honey bee, Apis mellifera L., and other honey bee species were largely neglected. In the current study, we thus compared visual learning performance of A. mellifera and the Eastern honey bee, A. cerana Fabr., using the proboscis extension response (PER) paradigm. Workers of A. mellifera and A. cerana were differentially conditioned to two monochromatic light stimuli, with peak maxima at 435 and 528 nm. Both honey bee species were able to form an association between the color stimulus and a sugar reward and significantly distinguished between the two color stimuli in a differential discrimination test. However, besides similar performance levels during visual learning, A. cerana showed a reduced mid-term memory (tested after 2 h) compared to A. mellifera. Finally, performance of the visual PER conditioning in our study reached similar levels as found in olfactory PER conditioning, and we thus recommend the visual PER conditioning approach in addition to olfactory conditioning as a useful tool for studying species-specific learning and memory capabilities in honey bees under controlled laboratory conditions.

}, issn = {1879-1611}, doi = {10.1016/j.jinsphys.2019.02.006}, author = {Lichtenstein, Leonie and Brockmann, Axel and Spaethe, Johannes} } @article {45302, title = {Mass Spectrometric Quantification of Arousal Associated Neurochemical Changes in Single Honey Bee Brains and Brain Regions.}, journal = {ACS Chem Neurosci}, volume = {10}, year = {2019}, month = {2018 Oct 26}, pages = {950-1959}, abstract = {

Honey bee foragers show a strong diurnal rhythm of foraging activity, and such behavioral changes are likely under the control of specific neuromodulators. To identify and quantify neuromodulators involved in regulating rest and arousal in honey bees, we established a mass spectrometric method for quantifying 14 different neurochemicals and precursor molecules. We measured forager type and brain region specific differences in amine levels from individual honey bee brains and brain regions. The observed differences in amine levels between resting and aroused foragers resemble findings in other species indicating a conserved molecular mechanism by glutamate and GABA in regulating arousal. Subesophageal ganglion specific changes in the histaminergic system and global increases in aspartate during arousal suggest a possible role of histamine and aspartate in feeding and arousal, respectively. More aminergic systems were significantly affected due to arousal in nectar foragers than in pollen foragers, implying that forager phenotypes differ not only in their food preference but also in their neuromodulatory signaling systems (brain states). Finally, we found that neurotransmitter precursors were better at distinguishing brain states in the central brain, while their end products correlated with arousal associated changes in sensory regions like the optic and antennal lobes.

}, issn = {1948-7193}, doi = {10.1021/acschemneuro.8b00254}, author = {Ramesh, Divya and Brockmann, Axel} } @article {53617, title = {Social modulation of individual differences in dance communication in honey bees}, journal = {Behavioral Ecology and Sociobiology}, volume = {74}, year = {2019}, month = {04/2019}, chapter = {41}, abstract = {

Group-living animals must constantly integrate and respond to information from other individuals within the group. The degree to which consistent inter-individual behavioural differences are influenced by social cues in such groups is largely unanswered. We used the honey bee waggle dance as an experimental paradigm to explore this question. Honey bee foragers use the waggle dance behaviour to communicate information about food sources in the environment to their nest mates. This recruitment process incorporates information about the food reward, the colony food stores and the environmental food availability and plays a major role in ensuring efficient exploitation of the food sources available to the colony. We first observed individual foragers visiting the same food source and quantified the probability and intensity of their dance activity. We found that there are consistent inter-individual differences in both measures of dance activity within a forager group. Next, we removed foragers and observed that this led to a significant increase in the average dance activity of some foragers. The individuals which increased their dance activity were the ones which were more active before the removal. Finally, we allowed recruits to join the foragers at the food source, which had a strong inhibitory effect on the dance activity of all the individual foragers. Our study shows that a complex interplay between individual behavioural differences and social interactions drives the dance communication needed to effectively organise the colony{\textquoteright}s collective foraging behaviour.

}, doi = {10.1007/s00265-019-2649-0}, author = {George, EA and Brockmann, Axel} } @article {59701, title = {Species composition and elevational distribution of bumble bees (Hymenoptera, Apidae, Latreille) in the East Himalaya, Arunachal Pradesh, India.}, journal = {Zookeys}, volume = {851}, year = {2019}, month = {2019}, pages = {71-89}, abstract = {

The East Himalaya is one of the world{\textquoteright}s most biodiverse ecosystems. However, 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 elevation insects that fulfil 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. Systematic study of Himalayan bumble bees began a few decades ago and the main focus has centred on the western region, while the eastern part of the mountain range has received little attention and only a few species have been verified. During a three-year survey, more than 700 bumble bee specimens of 21 species were collected in Arunachal Pradesh, the largest of the north-eastern states of India. The material included a range of species that were previously known from a 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. Clear elevation patterns of species diversity were observed, which raise important questions about the functional adaptations that allow bumble bees to thrive in this particularly moist region in the East Himalaya.

}, issn = {1313-2989}, doi = {10.3897/zookeys.851.32956}, author = {Streinzer, Martin and Chakravorty, Jharna and Neumayer, Johann and Megu, Karsing and Narah, Jaya and Schmitt, Thomas and Bharti, Himender and Spaethe, Johannes and Brockmann, Axel} } @article {36658, title = {: A Candidate Transcription Factor Involved in Molecular Processes Underlying Time-Memory.}, journal = {Front Psychol}, volume = {9}, year = {2018}, month = {2018}, pages = {865}, abstract = {

In honey bees, continuous foraging is accompanied by a sustained up-regulation of the immediate early gene (early growth response protein-1) and candidate downstream genes involved in learning and memory. Here, we present a series of feeder training experiments indicating that expression is highly correlated with the time and duration of training even in the absence of the food reward. Foragers that were trained to visit a feeder over the whole day and then collected on a day without food presentation showed up-regulation over the whole day with a peak expression around 14:00. When exposed to a time-restricted feeder presentation, either 2 h in the morning or 2 h in the evening, expression in the brain was up-regulated only during the hours of training. Foragers that visited a feeder in the morning as well as in the evening showed two peaks of expression. Finally, when we prevented time-trained foragers from leaving the colony using artificial rain, expression in the brains was still slightly but significantly up-regulated around the time of feeder training. hybridization studies showed that active foraging and time-training induced up-regulation occurred in the same brain areas, preferentially the small Kenyon cells of the mushroom bodies and the antennal and optic lobes. Based on these findings we propose that foraging induced expression can get regulated by the circadian clock after time-training over several days and is a candidate transcription factor involved in molecular processes underlying time-memory.

}, issn = {1664-1078}, doi = {10.3389/fpsyg.2018.00865}, author = {Shah, Aridni and Jain, Rikesh and Brockmann, Axel} } @article {35862, title = {Investigating the viral ecology of global bee communities with high-throughput metagenomics.}, journal = {Sci Rep}, volume = {8}, year = {2018}, month = {2018 Jun 11}, pages = {8879}, abstract = {

Bee viral ecology is a fascinating emerging area of research: viruses exert a range of effects on their hosts, exacerbate 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 4 continents and Oceania. We developed a novel pipeline to rapidly and inexpensively 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 for (+)ssRNA, (-)ssRNA, dsRNA, and ssDNA viruses. Overall, we found 127 contigs corresponding to novel viruses (i.e. previously not observed in bees), with 27 represented by \>0.1\% of the reads in a given sample, and 7 contained an RdRp or replicase sequence which could be used for robust phylogenetic analysis. This study provides a sequence-independent pipeline for viral metagenomics analysis, and greatly expands our understanding of the diversity of viruses found in bee communities.

}, issn = {2045-2322}, doi = {10.1038/s41598-018-27164-z}, author = {Galbraith, David A and Fuller, Zachary L and Ray, Allyson M and Brockmann, Axel and Frazier, Maryann and Gikungu, Mary W and Martinez, J Francisco Iturralde and Kapheim, Karen M and Kerby, Jeffrey T and Kocher, Sarah D and Losyev, Oleksiy and Muli, Elliud and Patch, Harland M and Rosa, Cristina and Sakamoto, Joyce M and Stanley, Scott and Vaudo, Anthony D and Grozinger, Christina M} } @article {48887, title = {Sugar Intake Elicits Intelligent Searching Behavior in Flies and Honey Bees.}, journal = {Front Behav Neurosci}, volume = {12}, year = {2018}, month = {2018}, pages = {280}, abstract = {

We present a comparison of the sugar-elicited search behavior in and . In both species, intake of sugar-water elicits a complex of searching responses. The most obvious response was an increase in turning frequency. However, we also found that flies and honey bees returned to the location of the sugar drop. They even returned to the food location when we prevented them from using visual and chemosensory cues. Analyses of the recorded trajectories indicated that flies and bees use two mechanisms, a locomotor pattern involving an increased turning frequency and path integration to increase the probability to stay close or even return to the sugar drop location. However, evidence for the use of path integration in honey bees was less clear. In general, walking trajectories of honey bees showed a higher degree of curvature and were more spacious; two characters which likely masked evidence for the use of path integration in our experiments. Visual cues, i.e., a black dot, presented underneath the sugar drop made flies and honey bees stay closer to the starting point of the search. In honey bees, vertical black columns close to the sugar drop increased the probability to visit similar cues in the vicinity. An additional one trial learning experiment suggested that the intake of sugar-water likely has the potential to initiate an associative learning process. Together, our experiments indicate that the sugar-elicited local search is more complex than previously assumed. Most importantly, this local search behavior appeared to exhibit major behavioral capabilities of large-scale navigation. Thus, we propose that sugar-elicited search behavior has the potential to become a fruitful behavioral paradigm to identify neural and molecular mechanisms involved in general mechanisms of navigation.

}, issn = {1662-5153}, doi = {10.3389/fnbeh.2018.00280}, author = {Brockmann, Axel and Basu, Pallab and Shakeel, Manal and Murata, Satoshi and Murashima, Naomi and Boyapati, Ravi Kumar and Prabhu, Nikhil G and Herman, Jacob J and Tanimura, Teiichi} } @article {43839, title = {Time-restricted foraging under natural light/dark condition shifts the molecular clock in the honey bee, Apis mellifera.}, journal = {Chronobiol Int}, year = {2018}, month = {2018 Sep 25}, pages = {1-12}, abstract = {

Honey bees have a remarkable sense of time and individual honey bee foragers are capable of adjusting their foraging activity with respect to the time of food availability. Although, there is compelling experimental evidence that foraging behavior is guided by the circadian clock, nothing is known about the underlying molecular mechanisms. Here we present for the first time a study that explores whether time-restricted foraging under natural light-dark (LD) condition affects the molecular clock in honey bees. Food was presented in an enclosed flight chamber (12\ m {\texttimes} 4\ m {\texttimes} 4\ m) 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 for three different parts of the nervous system involved in feeding-related behaviors: brain, subesophageal ganglion (SEG), and the antennae with olfactory sensory neurons. We found that morning and afternoon trained foragers showed significant phase differences in the cycling of both clock genes in all three tissues. In addition, the phase differences were more pronounced when the feeder was scented with the common plant odor, linalool. Together our findings suggest that foraging time may function as a Zeitgeber that might have the capability to modulate the light entrained molecular clock.

}, issn = {1525-6073}, doi = {10.1080/07420528.2018.1509867}, author = {Jain, Rikesh and Brockmann, Axel} } @article {23142, title = {Computational genome-wide survey of odorant receptors from two solitary bees Dufourea novaeangliae (Hymenoptera: Halictidae) and Habropoda laboriosa (Hymenoptera: Apidae).}, journal = {Sci Rep}, volume = {7}, year = {2017}, month = {2017 Sep 07}, pages = {10823}, abstract = {

Olfactory/odorant receptors (ORs) probably govern eusocial behaviour in honey bees through detection of cuticular hydrocarbons (CHCs) and queen mandibular gland pheromones (QMP). CHCs are involved in nest-mate recognition whereas QMP acts as sex pheromone for drones and as retinue pheromone for female workers. Further studies on the effect of eusociality on the evolution of ORs are hindered by the non-availability of comprehensive OR sets of solitary species. We report complete OR repertoires from two solitary bees Dufourea novaeangliae (112 ORs) and Habropoda laboriosa (151 ORs). We classify these ORs into 34 phylogenetic clades/subfamilies. Differences in the OR sets of solitary and eusocial bees are observed in individual subfamilies like subfamily 9-exon (putative CHC receptors) and L (contains putative QMP receptor group). A subfamily (H) including putative floral scent receptors is expanded in the generalist honey bees only, but not in the specialists. On the contrary, subfamily J is expanded in all bees irrespective of their degree of social complexity or food preferences. Finally, we show species-lineage specific and OR-subfamily specific differences in the putative cis-regulatory DNA motifs of the ORs from six hymenopteran species. Out of these, [A/G]CGCAAGCG[C/T] is a candidate master transcription factor binding site for multiple olfactory genes.

}, issn = {2045-2322}, doi = {10.1038/s41598-017-11098-z}, author = {Karpe, Snehal D and Dhingra, Surbhi and Brockmann, Axel and Sowdhamini, R} } @article {26284, title = {Octopamine Drives Endurance Exercise Adaptations in Drosophila.}, journal = {Cell Rep}, volume = {21}, year = {2017}, month = {2017 Nov 14}, pages = {1809-1823}, abstract = {

Endurance exercise is an effective therapeutic intervention with substantial pro-healthspan effects. Male Drosophila respond to a ramped daily program of exercise by inducing conserved physiological responses similar to those seen in mice and humans. Female flies respond to an exercise stimulus but do\ not experience the adaptive training response seen in males. Here, we use female flies as a model\ to demonstrate that differences in exercise response are mediated by differences in neuronal activity. The activity of octopaminergic neurons is specifically required to induce the conserved cellular and physiological changes seen following endurance training. Furthermore, either intermittent, scheduled activation of octopaminergic neurons or octopamine feeding is able to fully substitute for exercise, conferring a suite of pro-healthspan benefits to sedentary Drosophila. These experiments indicate that octopamine is a critical mediator of adaptation to endurance exercise in Drosophila.

}, issn = {2211-1247}, doi = {10.1016/j.celrep.2017.10.065}, author = {Sujkowski, Alyson and Ramesh, Divya and Brockmann, Axel and Wessells, Robert} } @article {20327, title = {Pharyngeal stimulation with sugar triggers local searching behavior in Drosophila.}, journal = {J Exp Biol}, year = {2017}, month = {2017 Jul 06}, abstract = {

Foraging behavior is essential for all organisms to find food containing nutritional chemicals. A hungry fly of Drosophila melanogaster performs local searching behavior after drinking a small amount of sugar solution. Using video tracking we examined how the searching behavior is regulated in D. melanogaster We found that a small amount of highly concentrated sugar solution induced a long-lasting searching behavior. After the intake of sugar solution, a fly moved around in circles and repeatedly returned to the position where the sugar droplet had been placed. The non-nutritious sugar, D-arabinose, but not the non-sweet nutritious sugar, D-sorbitol, was effective in inducing the behavior, indicating that sweet sensation is essential. Furthermore, pox-neuro mutant flies with no external taste bristles showed local searching behavior, suggesting the involvement of the pharyngeal taste organ. Experimental activation of pharyngeal sugar-sensitive gustatory receptor neurons by capsaicin using the Gal4/UAS system induced local searching behavior. In contrast, inhibition of pharyngeal sugar-responsive gustatory receptor neurons abolished the searching behavior. Together our results indicate that in Drosophila the pharyngeal taste-receptor neurons trigger searching behavior immediately after ingestion.

}, issn = {1477-9145}, doi = {10.1242/jeb.161646}, author = {Murata, Satoshi and Brockmann, Axel and Tanimura, Teiichi} } @article {1619, title = {Agatoxin-like peptides in the neuroendocrine system of the honey bee and other insects.}, journal = {J Proteomics}, volume = {132}, year = {2016}, month = {2016 Jan 30}, pages = {77-84}, abstract = {

UNLABELLED: We investigated the peptide inventory of the corpora cardiaca (CC) of the honey bee, Apis mellifera, by direct tissue profiling using MALDI-TOF MS combined with proteomic approaches focusing on cysteine-containing peptides. An agatoxin-like peptide (ALP) was identified as a component of the glandular part of the CC and was associated with the presence of the adipokinetic hormone in mass spectra. Although abundant in the CC, ALP does not belong to the toxins observed in the venom gland of A. mellifera. Homologs of ALP are highly conserved in major groups of arthropods and in line with this we detected ALP in the CC of non-venomous insects such as cockroaches and silverfish. In the American cockroach, Periplaneta americana, ALP was also identified in the CNS and stomatogastric nervous system. This is the first report that establishes the presence of ALPs in the neuroendocrine tissues of insects and further studies are necessary to reveal common functions of these peptides, e.g. as antimicrobial agents, ion channel modulators or classical neuropeptides.

BIOLOGICAL SIGNIFICANCE: Among the messenger molecules of the nervous system, neuropeptides represent the structurally most diverse class and basically participate in the regulation of all physiological processes. The set of neuropeptides, their functions and spatial distribution are particularly well-studied in insects. Until now, however, several potential neuropeptide receptors remained orphan, which indicates the existence of so far unknown ligands. In our study, we used proteomic methods such as cysteine modification, enzymatic digestion and peptide derivatization, combined with direct tissue profiling by MALDI-TOF mass spectrometry, for the discovery of novel putative messenger molecules in the neuroendocrine system. The described presence of agatoxin-like peptides in the nervous system of the honey bee and other insects was overseen so far and is thus a remarkable addition to the very well studied neuropeptidome of insects. It is not yet clear, if these toxin-like peptides act as antimicrobial agents, ion channel modulators or classical neuropeptides.

}, issn = {1876-7737}, doi = {10.1016/j.jprot.2015.11.021}, author = {Sturm, Sebastian and Ramesh, Divya and Brockmann, Axel and Neupert, Susanne and Predel, Reinhard} } @article {1620, title = {Brain regions and molecular pathways responding to food reward type and value in honey bees.}, journal = {Genes Brain Behav}, volume = {15}, year = {2016}, pages = {305-17}, abstract = {

The ability of honey bees to evaluate differences in food type and value is crucial for colony success, but these assessments are made by individuals who bring food to the hive, eating little, if any, of it themselves. We tested the hypothesis that responses to food type (pollen or nectar) and value involve different subsets of brain regions, and genes generally, responsive to food. mRNA in situ hybridization of c-jun revealed that brain regions responsive to differences in food type were mostly different from regions responsive to differences in food value, except those dorsal and lateral to the mushroom body calyces, which responded to all three. Transcriptomic profiles of the mushroom bodies generated by RNA sequencing gave the following results: 1) responses to differences in food type or value included a subset of molecular pathways involved in the response to food reward; 2) genes responsive to food reward, food type and food value were enriched for (the Gene Ontology categories) mitochondrial and endoplasmic reticulum activity; 3) genes responsive to only food and food type were enriched for regulation of transcription and translation; and 4) genes responsive to only food and food value were enriched for regulation of neuronal signaling. These results reveal how activities necessary for colony survival are channeled through the reward system of individual honey bees.

}, issn = {1601-183X}, doi = {10.1111/gbb.12275}, author = {McNeill, Matthew S and Kapheim, Karen M and Brockmann, Axel and McGill, Tara A W and Robinson, Gene E} } @article {16565, title = {Identification of Complete Repertoire of Apis florea Odorant Receptors Reveals Complex Orthologous Relationships with Apis mellifera.}, journal = {Genome Biol Evol}, volume = {8}, year = {2016}, month = {2016 Sep 26}, pages = {2879-2895}, abstract = {

We developed a computational pipeline for homology based identification of the complete repertoire of olfactory receptor (OR) genes in the Asian honey bee species, Apis florea Apis florea is phylogenetically the most basal honey bee species and also the most distant sister species to the Western honey bee Apis mellifera, for which all OR genes had been identified before. Using our pipeline, we identified 180 OR genes in A. florea, which is very similar to the number of ORs identified in A. mellifera (177 ORs). Many characteristics of the ORs including gene structure, synteny of tandemly repeated ORs and basic phylogenetic clustering are highly conserved. The composite phylogenetic tree of A. florea and A. mellifera ORs could be divided into 21 clades which are in harmony with the existing Hymenopteran tree. However, we found a few nonorthologous OR relationships between both species as well as independent pseudogenization of ORs suggesting separate evolutionary changes. Particularly, a subgroup of the OR gene clade XI, which had been hypothesized to code cuticular hydrocarbon receptors showed a high number of species-specific ORs RNAseq analysis detected a total number of 145 OR transcripts in male and 162 in female antennae. Most of the OR genes were highly expressed on the female antennae. However, we detected five distinct male-biased OR genes, out of which three genes (AfOr11, AfOr18, AfOr170P) were shown to be male-biased in A. mellifera, too, thus corroborating a behavioral function in sex-pheromone communication.

}, issn = {1759-6653}, doi = {10.1093/gbe/evw202}, author = {Karpe, Snehal D and Jain, Rikesh and Brockmann, Axel and Sowdhamini, Ramanathan} }