Imperial College London

Dr Richard J. Gill

Faculty of Natural SciencesDepartment of Life Sciences (Silwood Park)

Senior Lecturer
 
 
 
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Contact

 

+44 (0)20 7594 2215r.gill Website

 
 
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Location

 

N2.13MunroSilwood Park

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Summary

 

Publications

Publication Type
Year
to

34 results found

Cantwell-Jones A, Tylianakis J, Larson K, Gill Ret al., 2024, Using individual-based trait frequency distributions to forecast plant-pollinator network responses to environmental change, Ecology Letters, Vol: 27, ISSN: 1461-023X

Determining how and why organisms interact is fundamental to understanding ecosystem responses to future environmental change. To assess the impact on plant-pollinator interactions, recent studies have examined how the effects of environmental change on individual interactions accumulate to generate species-level responses. Here, we review recent developments in using plant-pollinator networks of interacting individuals along with their functional traits, where individuals are nested within species nodes. We highlight how these individual-level, trait-based networks connect intraspecific trait variation (as frequency distributions of multiple traits) with dynamic responses within plant-pollinator communities. This approach can better explain interaction plasticity, and changes to interaction probabilities and network structure over spatiotemporal or other environmental gradients. We argue that only through appreciating such trait-based interaction plasticity can we accurately forecast the potential vulnerability of interactions to future environmental change. We follow this with general guidance on how future studies can collect and analyse high-resolution interaction and trait data, with the hope of improving predictions of future plant-pollinator network responses for targeted and effective conservation.

Journal article

Liu Y, Olsson A, Larva T, Cantwell-Jones A, Gill RJ, Cederberg B, Webster MTet al., 2023, Genomic variation in montane bumblebees in Scandinavia: high levels of intraspecific diversity despite population vulnerability., Molecular Ecology, ISSN: 0962-1083

Populations of many bumblebee species are declining, with distributions shifting northwards to track suitable climates. Climate change is considered a major contributing factor. Arctic species are particularly vulnerable as they cannot shift further north, making assessment of their population viability important. Analysis of levels of whole-genome variation is a powerful way to analyse population declines and fragmentation. Here, we use genome sequencing to analyse genetic variation in seven species of bumblebee from the Scandinavian mountains, including two classified as vulnerable. We sequenced 333 samples from across the ranges of these species in Sweden. Estimates of effective population size (NE ) vary from ~55,000 for species with restricted high alpine distributions to 220,000 for more widespread species. Population fragmentation is generally very low or undetectable over large distances in the mountains, suggesting an absence of barriers to gene flow. The relatively high NE and low population structure indicate that none of the species are at immediate risk of negative genetic effects caused by high levels of genetic drift. However, reconstruction of historical fluctuations in NE indicates that the arctic specialist species Bombus hyperboreus has experienced population declines since the last ice age and we detected one highly inbred diploid male of this species close to the southern limit of its range, potentially indicating elevated genetic load. Although the levels of genetic variation in montane bumblebee populations are currently relatively high, their ranges are predicted to shrink drastically due to the effects of climate change and monitoring is essential to detect future population declines.

Journal article

Johansson J, Arce A, Gill R, 2023, How competition between overlapping generations can influence optimal egg-laying strategies in annual social insects, Oecologia, Vol: 202, Pages: 535-547, ISSN: 0029-8549

Annual social insects are an integral functional group of organisms, particularly in temperate environments. An emblematic part of their annual cycle is the social phase, during which the colony-founding queen rears workers that later assist her in rearing sexual progeny (gynes and drones). In many annual social insects, such as species of bees, wasps, and other groups, developing larvae are provisioned gradually as they develop (progressive provisioning) leading to multiple larval generations being reared simultaneously. We present a model for how the queen in such cases should optimize her egg-laying rate throughout the social phase depending on number-size trade-offs, colony age-structure, and energy balance. Complementing previous theory on optimal allocation between workers vs. sexuals in annual social insects and on temporal egg-laying patterns in solitary insects, we elucidate how resource competition among overlapping larval generations can influence optimal egg-laying strategies. With model parameters informed by knowledge of a common bumblebee species, the optimal egg-laying schedule consists of two temporally separated early broods followed by a more continuous rearing phase, matching empirical observations. However, eggs should initially be laid continuously at a gradually increasing rate when resources are scarce or mortality risks high and in cases where larvae are fully supplied with resources at the egg-laying stage (mass-provisioning). These factors, alongside sexual:worker body size ratios, further determine the overall trend in egg-laying rates over the colony cycle. Our analysis provides an inroad to study and mechanistically understand variation in colony development strategies within and across species of annual social insects.

Journal article

Kenna D, Graystock P, Gill R, 2023, Toxic temperatures: bee behaviours exhibit divergent pesticide toxicity relationships with warming, Global Change Biology, Vol: 29, Pages: 2981-2998, ISSN: 1354-1013

Climate change and agricultural intensification are exposing insect pollinators to temperature extremes and increasing pesticide usage. Yet, we lack good quantification of how temperature modulates the sublethal effects of pesticides on behaviours vital for fitness and pollination performance. Consequently, we are uncertain if warming decreases or increases the severity of different pesticide impacts, and whether separate behaviours vary in the direction of response. Quantifying these interactive effects is vital in forecasting pesticide risk across climate regions and informing pesticide application strategies and pollinator conservation. This multi-stressor study investigated the responses of six functional behaviours of bumblebees when exposed to either a neonicotinoid (imidacloprid) or a sulfoximine (sulfoxaflor) across a standardised low, mid, and high temperature. We found the neonicotinoid had a significant effect on five of the six behaviours, with a greater effect at the lower temperature(s) when measuring responsiveness, the likelihood of movement, walking rate, and food consumption rate. In contrast, the neonicotinoid had a greater impact on flight distance at the higher temperature. Our findings show that different organismal functions can exhibit divergent thermal responses, with some pesticide-affected behaviours showing greater impact as temperatures dropped, and others as temperatures rose. We must therefore account for environmental context when determining pesticide risk. Moreover, we found evidence of synergistic effects, with just a 3°C increase causing a sudden drop in flight performance, despite seeing no effect of pesticide at the two lower temperatures. Our findings highlight the importance of multi-stressor studies to quantify threats to insects, which will help to improve dynamic evaluations of population tipping points and spatiotemporal risks to biodiversity across different climate regions.

Journal article

Cantwell-Jones A, Larson K, Ward A, Bates OK, Cox T, Gibbons C, Richardson R, Al-Hayali AMR, Svedin J, Aronsson M, Brannlund F, Tylianakis JM, Johansson J, Gill RJet al., 2023, Mapping trait versus species turnover reveals spatiotemporal variation in functional redundancy and network robustness in a plant-pollinator community, Functional Ecology, Vol: 37, Pages: 748-762, ISSN: 0269-8463

Functional overlap among species (redundancy) is considered important in shaping competitive and mutualistic interactions that determine how communities respond to environmental change. Most studies view functional redundancy as static, yet traits within species—which ultimately shape functional redundancy—can vary over seasonal or spatial gradients. We therefore have limited understanding of how trait turnover within and between species could lead to changes in functional redundancy or how loss of traits could differentially impact mutualistic interactions depending on where and when the interactions occur in space and time. Using an Arctic bumblebee community as a case study, and 1277 individual measures from 14 species over three annual seasons, we quantified how inter- and intraspecific body-size turnover compared to species turnover with elevation and over the season. Coupling every individual and their trait with a plant visitation, we investigated how grouping individuals by a morphological trait or by species identity altered our assessment of network structure and how this differed in space and time. Finally, we tested how the sensitivity of the network in space and time differed when simulating extinction of nodes representing either morphological trait similarity or traditional species groups. This allowed us to explore the degree to which trait-based groups increase or decrease interaction redundancy relative to species-based nodes. We found that (i) groups of taxonomically and morphologically similar bees turn over in space and time independently from each other, with trait turnover being larger over the season; (ii) networks composed of nodes representing species versus morphologically similar bees were structured differently; and (iii) simulated loss of bee trait groups caused faster coextinction of bumblebee species and flowering plants than when bee taxonomic groups were lost. Crucially, the magnitude of these effects varied in spa

Journal article

Mullin VE, Stephen W, Arce AN, Nash W, Raine C, Notton DG, Whiffin A, Blagderov V, Gharbi K, Hogan J, Hunter T, Irish N, Jackson S, Judd S, Watkins C, Haerty W, Ollerton J, Brace S, Gill RJ, Barnes Iet al., 2023, First large-scale quantification study of DNA preservation in insects from natural history collections using genome-wide sequencing, Methods in Ecology and Evolution, Vol: 14, Pages: 360-371, ISSN: 2041-210X

1. Insect declines are a global issue with significant ecological and economic ramifications. Yet we have a poor understanding of the genomic impact these losses can have. Genome-wide data from historical specimens has the potential to provide baselines of population genetic measures to study population change, with natural history collections representing large repositories of such specimens. However, an initial challenge in conducting historical DNA data analyses, is to understand how molecular preservation varies between specimens.2. Here, we highlight how Next Generation Sequencing methods developed for studying archaeological samples can be applied to determine DNA preservation from only a single leg taken from entomological museum specimens, some of which are more than a century old. An analysis of genome-wide data from a set of 113 red-tailed bumblebee (Bombus lapidarius) specimens, from five British museum collections, was used to quantify DNA preservation over time. Additionally, to improve our analysis and further enable future research we generated a novel assembly of the red-tailed bumblebee genome. 3. Our approach shows that museum entomological specimens are comprised of short DNA fragments with mean lengths below 100 base pairs (BP), suggesting a rapid and large-scale post-mortem reduction in DNA fragment size. After this initial decline, however, we find a relatively consistent rate of DNA decay in our dataset, and estimate a mean reduction in fragment length of 1.9bp per decade. The proportion of quality filtered reads mapping to our assembled reference genome was around 50%, and decreased by 1.1 % per decade. 4. We demonstrate that historical insects have significant potential to act as sources of DNA to create valuable genetic baselines. The relatively consistent rate of DNA degradation, both across collections and through time, mean that population level analyses - for example for conservation or evolutionary studies - are entirely feasible, a

Journal article

Arce A, Cantwell-Jones A, Tansley M, Barnes I, Brace S, Mullin VE, Notton D, Ollerton J, Eatough E, Rhodes MW, Bian X, Hogan J, Hunter T, Jackson S, Whiffin A, Blagoderov V, Broad G, Judd S, Kokkini P, Livermore L, Dixit MK, Pearse WD, Gill Ret al., 2023, Signatures of increasing environmental stress in bumblebee wings over the past century: Insights from museum specimens, Journal of Animal Ecology, Vol: 92, Pages: 297-309, ISSN: 0021-8790

1. Determining when animal populations have experienced stress in the past is fundamental to understanding how risk factors drive contemporary and future species’ responses to environmental change. For insects, quantifying stress and associating it with environmental factors has been challenging due to a paucity of time-series data and because detectable population-level responses can show varying lag effects. One solution is to leverage historic entomological specimens to detect morphological proxies of stress experienced at the time stressors emerged, allowing us to more accurately determine population responses.2. Here we studied specimens of four bumblebee species, an invaluable group of insect pollinators, from five museums collected across Britain over the 20th century. We calculated the degree of fluctuating asymmetry (FA; random deviations from bilateral symmetry) between the right and left forewings as a potential proxy of developmental stress.3. We: i) investigated whether baseline FA levels vary between species, and how this compares between the first and second half of the century; ii) determined the extent of FA change over the century in the four bumblebee species, and whether this followed a linear or non-linear trend; iii) tested which annual climatic conditions correlated with increased FA in bumblebees.4. Species differed in their baseline FA, with FA being higher in the two species that have recently expanded their ranges in Britain. Overall, FA significantly increased over the century but followed a non-linear trend, with the increase starting c. 1925. We found relatively warm and wet years were associated with higher FA. 5. Collectively our findings show that FA in bumblebees increased over the 20th century and under weather conditions that will likely increase in frequency with climate change. By plotting FA trends and quantifying the contribution of annual climate conditions on past populations, we provide an important step towards impro

Journal article

Palmer J, Samuelson AE, Gill RJ, Leadbeater E, Jansen VAAet al., 2022, Honeybees vary communication and collective decision making across landscapes

<jats:title>Abstract</jats:title><jats:p>Honeybee (<jats:italic>Apis mellifera</jats:italic>) colony foraging decisions arise from the waggle dances of individual foragers, processed and filtered through a series of feedback loops that produce emergent collective behaviour. This process is an example of animal communication at the height of eusociality, yet a growing body of evidence suggests that its value for colony foraging success is heavily dependent on local ecology. Although colonies are thought to vary their use of the waggle dance in response to local ecological conditions, this is yet to be empirically established. Here, we quantify waggle dance use based on colony level dance-decoding and show that the impact of dance use on collective foraging is clear in some colonies but nearly negligible in others. We outline how these estimates of dance use can be combined with land-use data to explore the landscape characteristics that drive collective foraging. Our methodology provides a means to quantify the real-world importance of a celebrated example of animal communication and opens the door to the exploration of the selection pressures that may have driven the evolution of this remarkable collective behaviour.</jats:p>

Journal article

Yordanova M, Evison SEF, Gill RJ, Graystock Pet al., 2022, The threat of pesticide and disease co-exposure to managed and wild bee larvae, International Journal for Parasitology: Parasites and Wildlife, Vol: 17, Pages: 319-326, ISSN: 2213-2244

Brood diseases and pesticides can reduce the survival of bee larvae, reduce bee populations, and negatively influence ecosystem biodiversity. However, major gaps persist in our knowledge regarding the routes and implications of co-exposure to these stressors in managed and wild bee brood. In this review, we evaluate the likelihood for co-exposure to brood pathogen and pesticide stressors by examining the routes of potential co-exposure and the possibility for pollen and nectar contaminated with pathogens and pesticides to become integrated into brood food. Furthermore, we highlight ways in which pesticides may increase brood disease morbidity directly, through manipulating host immunity, and indirectly through disrupting microbial communities in the guts of larvae, or compromising brood care provided by adult bees. Lastly, we quantify the brood research bias towards Apis species and discuss the implications the bias has on brood disease and pesticide risk assessment in wild bee communities. We advise that future studies should place a higher emphasis on evaluating bee brood afflictions and their interactions with commonly encountered stressors, especially in wild bee species.

Journal article

Colgan TJ, Arce AN, Gill RJ, Ramos Rodrigues A, Kanteh A, Duncan EJ, Li L, Chittka L, Wurm Yet al., 2022, Genomic signatures of recent adaptation in a wild bumblebee, Molecular Biology and Evolution, Vol: 39, Pages: 1-9, ISSN: 0737-4038

Environmental changes threaten insect pollinators, creating risks for agriculture and ecosystem stability. Despite their importance, we know little about how wild insects respond to environmental pressures. To understand the genomic bases of adaptation in an ecologically important pollinator, we analyzed genomes of Bombus terrestris bumblebees collected across Great Britain. We reveal extensive genetic diversity within this population, and strong signatures of recent adaptation throughout the genome affecting key processes including neurobiology and wing development. We also discover unusual features of the genome, including a region containing 53 genes that lacks genetic diversity in many bee species, and a horizontal gene transfer from a Wolbachia bacteria. Overall, the genetic diversity we observe and how it is distributed throughout the genome and the population should support the resilience of this important pollinator species to ongoing and future selective pressures. Applying our approach to more species should help understand how they can differ in their adaptive potential, and to develop conservation strategies for those most at risk.

Journal article

Watrobska C, Ramos Rodrigues A, Arce A, Clarke J, Gill Ret al., 2021, Pollen source richness may be a poor predictor of bumblebee (Bombus terrestris) colony growth, Frontiers in Insect Science, Vol: 1, Pages: 1-11, ISSN: 2673-8600

Agricultural intensification has drastically altered foraging landscapes for bees, with large-scale crop monocultures associated with floral diversity loss. 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. Studying queen-right bumblebee (Bombus terrestris) colonies, we monitored colony development under polyfloral pollen diet or monofloral pollen dietwith 1.5-1.8 times higher crude protein concentration. 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. Our findings i) provide well-needed daily growth dynamics of queenright colonies under varied diets, and ii) support the view that pollen protein content in the foraging landscape rather than floral species richness per se is likely a key driver of colony health and success.

Journal article

Kenna D, Pawar S, Gill R, 2021, Thermal flight performance reveals impact of warming on bumblebee foraging potential, Functional Ecology, Vol: 35, Pages: 2508-2522, ISSN: 0269-8463

1. The effects of environmental temperature on components of insect flight determine life history traits, fitness, adaptability, and ultimately, organism ecosystem functional roles. Despite the crucial role of flying insects across landscapes, our understanding of how temperature affects insect flight performance remains limited.2. Many insect pollinators are considered under threat from climatic warming. Quantifying the relationship between temperature and behavioural performance traits allows us to understand where species are operating in respect to their thermal limits, helping predict responses to projected temperature increases and/or erratic weather events.3. Using a tethered flight mill, we quantify how flight performance of a widespread bumblebee, Bombus terrestris, varies over a temperature range (12-30oC). Given that body mass constrains insect mobility and behaviour, bumblebees represent a useful system to study temperature-mediated size-dependence of flight performance owing to the large intra-colony variation in worker body size they exhibit..4. Workers struggled to fly over a few hundred metres at the lowest tested temperature of 12oC, however flight endurance increased as temperatures rose, peaking around 25oC after which it declined. Our findings further revealed variation in flight capacity across the workforce, with larger workers flying further, longer, and faster than their smaller nestmates. Body mass was also positively related with the likelihood of flight, although importantly this relationship became stronger as temperatures cooled, such that at 12oC only the largest workers were successful fliers. Our study thus highlights that colony foraging success under variable thermal environments can be dependent on the body mass distribution of constituent workers, and more broadly suggests smaller-bodied insects may benefit disproportionately more from warming than larger-bodied ones in terms of flight performance.5. By incorporating both flight e

Journal article

Rother L, Kraft N, Smith DB, el Jundi B, Gill RJ, Pfeiffer Ket al., 2021, A micro-CT-based standard brain atlas of the bumblebee, Cell and Tissue Research, Vol: 386, Pages: 29-45, 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>

Journal article

Watrobska C, Rodrigues AR, Arce A, Clarke J, Gill Ret al., 2020, Pollen source richness may be a poor predictor of bumblebee colony growth, Publisher: Cold Spring Harbor Laboratory

Agricultural intensification has drastically altered foraging landscapes for bees, with large-scale crop monocultures associated with floral diversity loss.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.Studying queen-right bumblebee (Bombus terrestris) colonies, we monitored colony development under polyfloral pollen diet or monofloral pollen diet with 1.5-1.8 times higher crude protein concentration.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.Our findings i) provide well-needed daily growth dynamics of queenright colonies under varied diets, and ii) support the view that pollen protein content in the foraging landscape rather than floral species richness per se is likely a key driver of colony success.

Working paper

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.

Journal article

Smith D, Arce A, Ana RR, Bischoff P, Burris D, Ahmed F, Gill Ret 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.

Journal article

Kenna D, Cooley H, Pretelli I, Ramos Rodrigues A, Gill S, Gill Ret 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.

Journal article

Colgan TJ, Fletcher IK, Arce AA, Gill R, Ramos Rodrigues A, Stolle E, Chittka L, Wurm Yet 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.

Journal article

Arce A, Ramos Rodrigues A, Yu J, Colgan T, Wurm Y, Gill RJet 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

Journal article

Samuelson A, Gill RJ, Brown M, Leadbeater Eet 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.

Journal article

Gray R, Ewers R, Boyle M, Chung A, Gill RJet 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.

Journal article

Samuelson EEW, Chen-Wishart ZP, Gill RJ, Leadbeater Eet 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.

Journal article

Arce AN, David TI, Randall E, Ramos Rodrigues A, Colgan TJ, Wurm Y, Gill RJet 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

Journal article

Gill RJ, Smith DB, Raine NE, Bernhardt G, Abel RL, Sykes D, Ahmed F, Pedroso Iet 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.

Journal article

Gill RJ, Baldock KCR, Brown MJF, Cresswell JE, Dicks LV, Fountain MT, Garratt MPD, Gough LA, Heard MS, Holland JM, Ollerton J, Stone GN, Tang CQ, Vanbergen AJ, Vogler AP, Woodward G, Arce AN, Boatman ND, Brand-Hardy R, Breeze TD, Green M, Hartfield CM, O'Connor RS, Osborne JL, Phillips J, Sutton PB, Potts SGet 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.

Journal article

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.

Journal article

Raine NE, Gill RJ, 2015, ECOLOGY Tasteless pesticides affect bees in the field, NATURE, Vol: 521, Pages: 38-40, ISSN: 0028-0836

Journal article

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

Journal article

Bryden J, Gill RJ, Mitton RAA, Raine NE, Jansen VAAet al., 2013, Chronic sublethal stress causes bee colony failure, ECOLOGY LETTERS, Vol: 16, Pages: 1463-1469, ISSN: 1461-023X

Journal article

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

Journal article

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