23 results found
Rother L, Kraft N, Smith DB, et al., 2021, A micro-CT-based standard brain atlas of the bumblebee, Cell and Tissue Research, ISSN: 0302-766X
<jats:title>Abstract</jats:title><jats:p>In recent years, bumblebees have become a prominent insect model organism for a variety of biological disciplines, particularly to investigate learning behaviors as well as visual performance. Understanding these behaviors and their underlying neurobiological principles requires a clear understanding of brain anatomy. Furthermore, to be able to compare neuronal branching patterns across individuals, a common framework is required, which has led to the development of 3D standard brain atlases in most of the neurobiological insect model species. Yet, no bumblebee 3D standard brain atlas has been generated. Here we present a brain atlas for the buff-tailed bumblebee <jats:italic>Bombus terrestris</jats:italic> using micro-computed tomography (micro-CT) scans as a source for the raw data sets, rather than traditional confocal microscopy, to produce the first ever micro-CT-based insect brain atlas. We illustrate the advantages of the micro-CT technique, namely, identical native resolution in the three cardinal planes and 3D structure being better preserved. Our <jats:italic>Bombus terrestris</jats:italic> brain atlas consists of 30 neuropils reconstructed from ten individual worker bees, with micro-CT allowing us to segment neuropils completely intact, including the lamina, which is a tissue structure often damaged when dissecting for immunolabeling. Our brain atlas can serve as a platform to facilitate future neuroscience studies in bumblebees and illustrates the advantages of micro-CT for specific applications in insect neuroanatomy.</jats:p>
Colgan TJ, Arce AN, Gill RJ, et al., 2021, Genomic signatures of recent adaptation in a wild bumblebee
<jats:title>Abstract</jats:title><jats:p>Behavioral experiments and analyses of observation records have shown that environmental changes threaten insect pollinators, creating risks for agriculture and ecosystem stability. Despite their importance, we know little about how wild insects or other animals can adapt in response to environmental pressures. To understand the genomic bases of adaptation in an ecologically important pollinator, we analyzed genomes of <jats:italic>Bombus terrestris</jats:italic> bumblebees collected across Great Britain. We reveal extensive genetic diversity within this population, and strong signatures of recent adaptation throughout the genome. More specifically, we find that selection recently affected key processes underpinning environmental interactions, including neurobiology, wing development, and response to xenobiotics. We also discover unusual features of the genome, including a 53-gene region that lacks genetic diversity in many bee species, and a horizontal gene transfer from a <jats:italic>Wolbachia</jats:italic> bacteria. The genetic diversity and gene flow we observe for this species could support its resilience to ongoing and future challenges. Overall, we provide important insight on the genetic health of an ecologically and economically important pollinator and reveal mechanisms by which it has recently adapted. The approach we used could help to understand how species differ in their adaptive potential, and to develop conservation strategies for those most at risk.</jats:p>
Watrobska CM, Rodrigues AR, Arce AN, et al., 2020, Pollen source richness may be a poor predictor of bumblebee colony growth
<jats:title>ABSTRACT</jats:title><jats:p><jats:list list-type="order"><jats:list-item><jats:p>Agricultural intensification has drastically altered foraging landscapes for bees, with large-scale crop monocultures associated with floral diversity loss.</jats:p></jats:list-item><jats:list-item><jats:p>Research on bumblebees and honeybees has shown individuals feeding on pollen from a low richness of floral sources can experience negative impacts on health and longevity relative to higher pollen source richness of similar protein concentrations. Florally rich landscapes are thus generally assumed to better support social bees. Yet, little is known about whether the effects of reduced pollen source richness can be mitigated by feeding on pollen with higher crude protein concentration, and importantly how variation in diet affects whole colony growth, rearing decisions and sexual production.</jats:p></jats:list-item><jats:list-item><jats:p>Studying queen-right bumblebee (<jats:italic>Bombus terrestris</jats:italic>) colonies, we monitored colony development under polyfloral pollen diet or monofloral pollen diet with 1.5-1.8 times higher crude protein concentration.</jats:p></jats:list-item><jats:list-item><jats:p>Over six weeks, we found monofloral colonies performed better for all measures, with no apparent long-term effects on colony mass or worker production, and a higher number of pupae in monofloral colonies at the end of the experiment. Unexpectedly, polyfloral colonies showed higher mortality, and little evidence of any strategy to counteract the effects of reduced protein; with fewer and lower mass workers being reared, and males showing a similar trend.</jats:p></jats:list-item><jats:list-item><jats:p>Our findings i) provide well-needed daily growth dynamics of queenright colonies under varied diets, and ii) sup
Samuelson A, Gill R, Leadbeater E, 2020, Urbanisation is associated with reduced Nosema sp. infection, higher colony strength and higher richness of foraged pollen in honeybees, Apidologie, Vol: 51, Pages: 746-762, ISSN: 0044-8435
Bees are vital pollinators, but are faced with numerous threats that include loss of floral resources and emerging parasites amongst others. Urbanisation is a rapidly expanding driver of land-use change that may interact with these two major threats to bees. Here we investigated effects of urbanisation on food store quality and colony health in honeybees (Apis mellifera) by sampling 51 hives in four different land-use categories: urban, suburban, rural open and rural wooded during two seasons (spring and autumn). We found positive effects of urban land use on colony strength and richness of stored pollen morphotypes, alongside lower late-season Nosema sp. infection in urban and suburban colonies. Our results reveal that honeybees exhibit lower colony performance in strength in rural areas, adding to the growing evidence that modern agricultural landscapes can constitute poor habitat for insect pollinators.
Smith D, Arce A, Ana RR, et al., 2020, Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebees, Proceedings of the Royal Society B: Biological Sciences, Vol: 287, ISSN: 0962-8452
For social bees, an understudied step in evaluating pesticide risk is how contaminated food entering colonies affects residing offspring development and maturation. For instance, neurotoxic insecticide compounds in food could affect central nervous system development predisposing individuals to become poorer task performers later-in-life. Studying bumblebee colonies provisioned with neonicotinoid spiked nectar substitute, we measured brain volume and learning behaviour of 3 or 12-day old adults that had experienced in-hive exposure during brood and/or early-stage adult development. Micro-computed tomography (µCT) scanning and segmentation of multiple brain neuropils showed exposure during either developmental stage caused reduced mushroom body calycal growth relative to unexposed workers. Associated with this, was a lower probability of responding to a sucrose reward and lower learning performance in an olfactory conditioning test. Whilst calycal volume of control workers positively correlated with learning score, this relationship was absent for exposed workers indicating neuropil functional impairment. Comparison of 3 and 12-day adults exposed during brood development showed a similar degree of reduced calycal volume and impaired behaviour highlighting lasting and irrecoverable effects from exposure despite no adult exposure. Our findings help explain how the onset of pesticide exposure to whole colonies can lead to lag-effects on growth and resultant dysfunction.
Kenna D, Cooley H, Pretelli I, et al., 2019, Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees, Ecology and Evolution, Vol: 9, Pages: 5637-5650, ISSN: 2045-7758
The emergence of agricultural land use change creates a number of challenges that insect pollinators, such as eusocial bees, must overcome. Resultant fragmentation and loss of suitable foraging habitats, combined with pesticide exposure, may increase demands on foraging, specifically the ability to collect or reach sufficient resources under such stress. Understanding effects that pesticides have on flight performance is therefore vital if we are to assess colony success in these changing landscapes. Neonicotinoids are one of the most widely used classes of pesticide across the globe, and exposure to bees has been associated with reduced foraging efficiency and homing ability. One explanation for these effects could be that elements of flight are being affected, but apart from a couple of studies on the honeybee (Apis mellifera), this has scarcely been tested. Here, we used flight mills to investigate how exposure to a field realistic (10 ppb) acute dose of imidacloprid affected flight performance of a wild insect pollinator—the bumblebee, Bombus terrestris audax. Intriguingly, observations showed exposed workers flew at a significantly higher velocity over the first ¾ km of flight. This apparent hyperactivity, however, may have a cost because exposed workers showed reduced flight distance and duration to around a third of what control workers were capable of achieving. Given that bumblebees are central place foragers, impairment to flight endurance could translate to a decline in potential forage area, decreasing the abundance, diversity, and nutritional quality of available food, while potentially diminishing pollination service capabilities.
Colgan TJ, Fletcher IK, Arce AA, et al., 2019, Caste- and pesticide-specific effects of neonicotinoid pesticide exposure on gene expression in bumblebees, Molecular Ecology, Vol: 28, Pages: 1964-1974, ISSN: 0962-1083
Social bees are important insect pollinators of wildflowers and agricultural crops, making their reported declines a global concern. A major factor implicated in these declines is the widespread use of neonicotinoid pesticides. Indeed, recent research has demonstrated that exposure to low doses of these neurotoxic pesticides impairs bee behaviours important for colony function and survival. However, our understanding of the molecular‐genetic pathways that lead to such effects is limited, as is our knowledge of how effects may differ between colony members. To understand what genes and pathways are affected by exposure of bumblebee workers and queens to neonicotinoid pesticides, we implemented a transcriptome‐wide gene expression study. We chronically exposed Bombus terrestriscolonies to either clothianidin or imidacloprid at field‐realistic concentrations while controlling for factors including colony social environment and worker age. We reveal that genes involved in important biological processes including mitochondrial function are differentially expressed in response to neonicotinoid exposure. Additionally, clothianidin exposure had stronger effects on gene expression amplitude and alternative splicing than imidacloprid. Finally, exposure affected workers more strongly than queens. Our work demonstrates how RNA‐Seq transcriptome profiling can provide detailed novel insight on the mechanisms mediating pesticide toxicity to a key insect pollinator.
Arce A, Ramos Rodrigues A, Yu J, et al., 2018, Foraging bumblebees acquire a preference for neonicotinoid treated food with prolonged exposure, Proceedings of the Royal Society B: Biological Sciences, Vol: 285, ISSN: 1471-2954
Social bees represent an important group of pollinating insects that can be exposed to potentially harmful pesticides when foraging on treated or contaminated flowering plants. To investigate if such exposure is detrimental to bees, many studies have exclusively fed individuals with pesticide-spiked food, informing us about the hazard but not necessarily the risk of exposure. While such studies are important to establish the physiological and behavioural effects on individuals, they do not consider the possibility that the risk of exposure may change over time. For example, many pesticide assays exclude potential behavioural adaptations to novel toxins, such as rejection of harmful compounds by choosing to feed on an uncontaminated food source, thus behaviourally lowering the risk of exposure. In this paper, we conducted an experiment over 10 days in which bumblebees could forage on an array of sucrose feeders containing 0, 2 and 11 parts per billion of the neonicotinoid pesticide thiamethoxam. This more closely mimics pesticide exposure in the wild by allowing foraging bees to (i) experience a field realistic range of pesticide concentrations across a chronic exposure period, (ii) have repeated interactions with the pesticide in their environment, and (iii) retain the social cues associated with foraging by using whole colonies. We found that the proportion of visits to pesticide-laced feeders increased over time, resulting in greater consumption of pesticide-laced sucrose relative to untreated sucrose. After changing the spatial position of each feeder, foragers continued to preferentially visit the pesticide-laced feeders which indicates that workers can detect thiamethoxam and alter their behaviour to continue feeding on it. The increasing preference for consuming the neonicotinoid-treated food therefore increases the risk of exposure for the colony during prolonged pesticide exposure. Our results highlight the need to incorporate attractiveness of pesticides to
Samuelson A, Gill RJ, Brown M, et al., 2018, Lower bumblebee colony reproductive success in agricultural compared with urban environments, Proceedings of the Royal Society B: Biological Sciences, Vol: 285, ISSN: 1471-2954
Urbanization represents a rapidly growing driver of land-use change. While it is clear that urbanization impacts species abundance and diversity, direct effects of urban land use on animal reproductive success are rarely documented. Here, we show that urban land use is linked to long-term colony reproductive output in a key pollinator. We reared colonies from wild-caught bumblebee (Bombus terrestris) queens, placed them at sites characterized by varying degrees of urbanization from inner city to rural farmland and monitored the production of sexual offspring across the entire colony cycle. Our land-use cluster analysis identified three site categories, and this categorization was a strong predictor of colony performance. Crucially, colonies in the two clusters characterized by urban development produced more sexual offspring than those in the cluster dominated by agricultural land. These colonies also reached higher peak size, had more food stores, encountered fewer parasite invasions and survived for longer. Our results show a link between urbanization and bumblebee colony reproductive success, supporting the theory that urban areas provide a refuge for pollinator populations in an otherwise barren agricultural landscape.
Gray R, Ewers R, Boyle M, et al., 2018, Effect of tropical forest disturbance on the competitive interactions within a diverse ant community, Scientific Reports, Vol: 8, ISSN: 2045-2322
Understanding how anthropogenic disturbance influences patterns of community composition and the reinforcing interactive processes that structure communities is important to mitigate threats to biodiversity. Competition is considered a primary reinforcing process, yet little is known concerning disturbance effects on competitive interaction networks.We examined how differences in ant community composition between undisturbed and disturbed Bornean rainforest, is potentially reflected by changes in competitive interactions over a food resource. Comparing 10 primary forest sites to 10 in selectively-logged forest, we found higher genus richness and diversity in the primary forest, with 18.5% and 13.0% of genera endemic to primary and logged respectively. From 180 hours of filming bait cards, we assessed ant-ant interactions, finding that despite considered aggression over food sources, the majority of ant interactions were neutral. Proportion of competitive interactions at bait cards did not differ between forest type, however, the rate and per capita number of competitive interactions was significantly lower in logged forest. Furthermore, the majority of genera showed large changes in aggression-score with often inverse relationships to their occupancy rank. This provides evidence of a shuffled competitive network, and these unexpected changes in aggressive relationships could be considered a type of competitive network re-wiring after disturbance.
Samuelson EEW, Chen-Wishart ZP, Gill RJ, et al., 2016, Effect of acute pesticide exposure on bee spatial working memory using an analogue of the radial-arm maze, Scientific Reports, Vol: 6, ISSN: 2045-2322
Pesticides, including neonicotinoids, typically target pest insects by being neurotoxic. Inadvertent exposure to foraging insect pollinators is usually sub-lethal, but may affect cognition. One cognitive trait, spatial working memory, may be important in avoiding previously-visited flowers and other spatial tasks such as navigation. To test this, we investigated the effect of acute thiamethoxam exposure on spatial working memory in the bumblebee Bombus terrestris, using an adaptation of the radial-arm maze (RAM). We first demonstrated that bumblebees use spatial working memory to solve the RAM by showing that untreated bees performed significantly better than would be expected if choices were random or governed by stereotyped visitation rules. We then exposed bees to either a high sub-lethal positive control thiamethoxam dose (2.5ng-1 bee), or one of two low doses (0.377 or 0.091ng-1) based on estimated field-realistic exposure. The high dose caused bees to make more and earlier spatial memory errors and take longer to complete the task than unexposed bees. For the low doses, the negative effects were smaller but statistically significant, and dependent on bee size. The spatial working memory impairment shown here has the potential to harm bees exposed to thiamethoxam, through possible impacts on foraging efficiency or homing.
Arce AN, David TI, Randall E, et al., 2016, Impact of controlled neonicotinoid exposure on bumblebees in a realistic field setting, Journal of Applied Ecology, Vol: 54, Pages: 1199-1208, ISSN: 1365-2664
1. Pesticide exposure has been implicated as a contributor to insect pollinator declines. In social bees, which are crucial pollination service providers, the effect of low-level chronic exposure is typically non-lethal leading researchers to consider whether exposure induces sub-lethal effects on behaviour and whether such impairment can affect colony development. 2. Studies under laboratory conditions can control levels of pesticide exposure and elucidate causative effects, but are often criticised for being unrealistic. In contrast, field studies can monitor bee responses under a more realistic pesticide exposure landscape; yet typically such findings are limited to correlative results, and can lack true controls or sufficient replication. We attempt to bridge this gap by exposing bumblebees to known amounts of pesticides when colonies are placed in the field.3. Using 20 bumblebee colonies, we assess the consequences of exposure to the neonicotinoid clothianidin, provided in sucrose at a concentration of five parts per billion, over five weeks. We monitored foraging patterns and pollen collecting performance from 3282 bouts using either a non-invasive photographic assessment, or by extracting the pollen from returning foragers. We also conducted a full colony census at the beginning and end of the experiment.4. In contrast to studies on other neonicotinoids, showing clear impairment to foraging behaviours, we detected only subtle changes to patterns of foraging activity and pollen foraging during the course of the experiment. However, our colony census measures showed a more pronounced effect of exposure, with fewer adult workers and sexuals in treated colonies after five weeks.5. Synthesis and applications. Pesticide induced impairments on colony development and foraging could impact on the pollination service that bees provide. Therefore our findings, that bees show subtle changes in foraging behaviour and reductions in colony size after exposure to a common pe
Gill RJ, Smith DB, Raine NE, et al., 2016, Exploring miniature insect brains using micro-CT scanning techniques, Scientific Reports, Vol: 6, ISSN: 2045-2322
The capacity to explore soft tissue structures in detail is important in understandinganimal physiology and how this determines features such as movement, behaviour and the impactof trauma on regular function. Here we use advances in micro-computed tomography (micro-CT)technology to explore the brain of an important insect pollinator and model organism, thebumblebee (Bombus terrestris). Here we present a method for accurate imaging and exploration 2of insect brains that keeps brain tissue free from trauma and in its natural stereo-geometry, andshowcase our 3D reconstructions and analyses of 19 individual brains at high resolution.Development of this protocol allows relatively rapid and cost effective brain reconstructions,making it an accessible methodology to the wider scientific community. The protocol describes thenecessary steps for sample preparation, tissue staining, micro-CT scanning and 3D reconstruction,followed by a method for image analysis using the freeware SPIERS. These image analysis methodsdescribe how to virtually extract key composite structures from the insect brain, and wedemonstrate the application and precision of this method by calculating structural volumes andinvestigating the allometric relationships between bumblebee brain structures.
Gill RJ, Baldock KCR, Brown MJF, et al., 2016, Protecting an Ecosystem Service: Approaches to Understanding and Mitigating Threats to Wild Insect Pollinators, Advances in Ecological Research, Vol: 54, Pages: 135-206, ISSN: 0065-2504
Insect pollination constitutes an ecosystem service of global importance, providing significant economic and aesthetic benefits as well as cultural value to human society, alongside vital ecological processes in terrestrial ecosystems. It is therefore important to understand how insect pollinator populations and communities respond to rapidly changing environments if we are to maintain healthy and effective pollinator services. This chapter considers the importance of conserving pollinator diversity to maintain a suite of functional traits and provide a diverse set of pollinator services. We explore how we can better understand and mitigate the factors that threaten insect pollinator richness, placing our discussion within the context of populations in predominantly agricultural landscapes in addition to urban environments. We highlight a selection of important evidence gaps, with a number of complementary research steps that can be taken to better understand: (i) the stability of pollinator communities in different landscapes in order to provide diverse pollinator services; (ii) how we can study the drivers of population change to mitigate the effects and support stable sources of pollinator services and (iii) how we can manage habitats in complex landscapes to support insect pollinators and provide sustainable pollinator services for the future. We advocate a collaborative effort to gain higher quality abundance data to understand the stability of pollinator populations and predict future trends. In addition, for effective mitigation strategies to be adopted, researchers need to conduct rigorous field testing of outcomes under different landscape settings, acknowledge the needs of end-users when developing research proposals and consider effective methods of knowledge transfer to ensure effective uptake of actions.
Gill RJ, Woodward G, 2016, Networking our way to better ecosystem service provision, Trends in Ecology & Evolution, Vol: 31, Pages: 105-115, ISSN: 0169-5347
The ecosystem services (EcoS) concept is being used increasingly to attach values to natural systems and the multiple benefits they provide to human societies. Ecosystem processes or functions only become EcoS if they are shown to have social and/or economic value. This should assure an explicit connection between the natural and social sciences, but EcoS approaches have been criticized for retaining little natural science. Preserving the natural, ecological science context within EcoS research is challenging because the multiple disciplines involved have very different traditions and vocabularies (common-language challenge) and span many organizational levels and temporal and spatial scales (scale challenge) that define the relevant interacting entities (interaction challenge). We propose a network-based approach to transcend these discipline challenges and place the natural science context at the heart of EcoS research.
Raine NE, Gill RJ, 2015, ECOLOGY Tasteless pesticides affect bees in the field, NATURE, Vol: 521, Pages: 38-40, ISSN: 0028-0836
Gill RJ, Raine NE, 2014, Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure, Functional Ecology, Vol: 28, Pages: 1459-1471, ISSN: 0269-8463
Insect pollination is a vital ecosystem service that maintains biodiversity and sustains agricultural crop yields. Social bees are essential insect pollinators, so it is concerning that their populations are in global decline.Although pesticide exposure has been implicated as a possible cause for bee declines, we currently have a limited understanding of the risk these chemicals pose. Whilst environmental exposure to pesticides typically has non‐lethal effects on individual bees, recent reports suggest that sublethal exposure can affect important behavioural traits such as foraging. However, at present, we know comparatively little about how natural foraging behaviour is impaired and the relative impacts of acute and chronic effects.Using Radio‐Frequency Identification (RFID) tagging technology, we examined how the day‐to‐day foraging patterns of bumblebees (Bombus terrestris) were affected when exposed to either a neonicotinoid (imidacloprid) and/or a pyrethroid (λ‐cyhalothrin) independently and in combination over a four‐week period. This is the first study to provide data on the impacts of combined and individual pesticide exposure on the temporal dynamics of foraging behaviour in the field over a prolonged period of time.Our results show that neonicotinoid exposure has both acute and chronic effects on overall foraging activity. Whilst foragers from control colonies improved their pollen foraging performance as they gained experience, the performance of bees exposed to imidacloprid became worse: chronic behavioural impairment. We also found evidence, suggesting that pesticide exposure can change forager preferences for the flower types from which they collect pollen.Our findings highlight the importance of considering prolonged exposure (which happens in the field) when assessing the risk that pesticides pose to bees. The effects of chronic pesticide exposure could have serious detrimental consequences for both colony survival and also the pollination ser
Bryden J, Gill RJ, Mitton RAA, et al., 2013, Chronic sublethal stress causes bee colony failure, ECOLOGY LETTERS, Vol: 16, Pages: 1463-1469, ISSN: 1461-023X
Gill RJ, Ramos-Rodriguez O, Raine NE, 2012, Combined pesticide exposure severely affects individual- and colony-level traits in bees, NATURE, Vol: 491, Pages: 105-U119, ISSN: 0028-0836
Gill RJ, Hammond RL, 2011, Workers determine queen inheritance of reproduction in a functionally monogynous ant population, ANIMAL BEHAVIOUR, Vol: 82, Pages: 119-129, ISSN: 0003-3472
Coston DJ, Gill RJ, Hammond RL, 2011, No evidence of volatile chemicals regulating reproduction in a multiple queen ant, NATURWISSENSCHAFTEN, Vol: 98, Pages: 625-629, ISSN: 0028-1042
Gill RJ, Hammond RL, 2011, Workers influence royal reproduction, PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, Vol: 278, Pages: 1524-1531, ISSN: 0962-8452
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