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Biology subjects

Gill, R. J.

Publications and source records attributed to Gill, R. J..

11 recordsLinked to original sources

Revealing centurial changes in butterfly wing shape via the automated analysis of museum specimens.

O_LIUnderstanding how environmental change is shaping organismal morphology of key functional guilds is important, since morphological traits determine the delivery of ecosystem services we depend upon. Adult butterflies, as pollinators, are commercially and culturally important, but the longitudinal data across appropriate time frames to understand trait response trends are generally limited. C_LIO_LIHere we leverage digitised museum butterfly specimens to help fill this data gap by employing automated methods (machine learning and Elliptical Fourier Analysis) to achieve high-throughput measurements of traits across large collections. We analyse how wing shape (the outline of the whole butterfly) varies in over 178,000 specimens of 65 butterfly species collected across the UK and Ireland over two centuries. C_LIO_LIWe identify two major biologically attributable axes of butterfly wing shape: aspect ratio and asymmetry. Analysing a subset of these specimens (108,511 from 34 species), we find directional trends in wing shape. Over a period of 105 years (1901-2006), wings generally became narrower and longer in over half (18) of the studied species. This response may be affecting butterfly behaviour by favouring gliding flight. C_LIO_LIUltimately, we highlight that historical processes including temperature change have historically shaped butterfly wing shape. We demonstrate that studying whole wing outline using automated methods allows us to extract the high-throughput, long-term data required to understand the responses of ecologically important taxa at scales that we were previously unable to achieve. C_LI

ecology↗

Can near-infrared exposure help mitigate pesticide-impaired thermoregulation in adult bees?

For terrestrial animals, maintaining body temperature is vital for successful movement, feeding and reproduction. Exposure to environmental toxins such as pesticides, however, may place individual thermoregulation at risk. Identifying potential mitigative solutions is thus important, especially given widespread pesticide applications across landscapes are forecast to continue. In mammals, near infrared (NIR) light has been put forward as a method for countering the effects of toxin exposure, but limited evidence has been found for insects. Here, we orally expose an important insect pollinator group - adult bumblebees - to a cholinergic pesticide (a neonicotinoid) to first quantify the baseline impact on body temperature (using thermal imaging), and second to investigate how exposure to near infrared (NIR) light mediates this effect. For bumblebees kept at 18{degrees}C ambient we show, relative to control bees who maintained their body temperature at ca.30{degrees}C, that neonicotinoid exposed bees exhibited a steep (by nearly 8{degrees}C) body temperature drop over the 73hr assay showing a pattern of convergence towards ambient. We did however find some evidence that NIR can partially counter such neonicotinoid impairment. Of two different wavelengths (600nm, 850nm) and three exposure durations (5, 10 or 20 minutes per hour), we found evidence that 660 nm for 5 minutes appeared to more than halve the rate to which the neonicotinoid decreased body temperature. Yet, intriguingly, the mitigation effect of 660 nm NIR appeared to lessen as exposure time increased. We further found tentative evidence that 850 nm for 20 mins may alleviate the decline in body temperature (by nearly 40%). In conclusion, our study further highlights a mechanism by which pesticides threaten the critical functioning of non-target organisms but also provides a potential therapy worthy of further investigation.

ecology↗

Polli-markers: spectral and chemical biomarkers for detecting cryptic early plant pollination responses

O_LIPollination is essential for plant reproduction, ecosystem resilience and human health. Yet, our capability to map pollination service delivery in real-time across large areas remains poor. Determining where and when flowers are pollinated is vital to mitigate widespread pollination deficits, increase plant health and yield, and support pollinator management. Hence, innovative approaches are urgently needed for establishing scalable predictive bioindicators of plant pollination status with the goal of achieving real-time landscape-scale monitoring. C_LIO_LIHere we present two parallel controlled pollination assays in which we characterise the post-pollination petal physiology of a world leading flowering crop, Brassica napus, using in-situ close-range hyperspectral reflectance and semi-untargeted metabolomics. C_LIO_LIThis multiomics approach coupled with supervised machine learning and biomarker detection reveals cryptic changes in the UV petal reflectance spectrum which are predictive of pollination status, representing a novel set of candidate pollination bioindicators ( polli-markers), and our high-resolution time series enables prediction of when this pollination event occurred. It also reveals an associated set of candidate metabolites, including flavonoids and senescence markers, shedding light on the functional pathways related to our polli-markers. C_LIO_LIThis study provides key insights into floral development, enabling a transformative step towards predicting, mapping and quantifying pollination service delivery at the landscape scale. C_LI

ecology↗

Pesticide-exposed bees fail to thermoregulate leading to cold colonies with consequences for offspring development

For many organisms, effective thermoregulation is needed to cope with changing environmental temperatures. But if exposure to pesticides in the environment were to impair this homeostatic process, reproduction and population viability could be at risk. Focusing on an important insect pollinator, we conducted three complementary experiments exposing bumblebees to a pesticide under different temperature challenges and measuring the impacts on thermoregulatory ability and brood development. First, we reveal that pesticide-exposed individuals cannot maintain a stable thorax temperature, especially at lower temperatures. Second, reductions in body temperature are accompanied by behavioural changes and that pesticide-exposed colonies fail to maintain appropriate brood temperatures. Third, such collective impairment on brood thermoregulation (not the pesticide toxicity to offspring per se) leads to delayed pupal development and reduced adult population growth. Our study provides a valid mechanistic explanation for why terrestrial insects requiring brood thermoregulation have declined. With frequent extreme weather events forecasted, our findings have concerning implications for how populations will adequately persist and grow under current pesticide-use regimes with ramifications on pollination services.

ecology↗

Phenological turnover matters when making trait-based predictions of plant-pollinator interactions

1. Understanding the processes determining species interactions is key to predicting and safeguarding ecological networks under rapid environmental change. One approach to estimating interactions is to use morphologies of taxa interacting across trophic levels to reveal suites of traits they are more likely to interact with (i.e. a trait niche). 2. Previous work studying these morphological trait niches has typically used interactions between species that are pooled in space and time. However, species assemblages, and the traits of individuals within species, can change across even small landscapes over a season, leading to morphological trait space being dynamically reshaped. Therefore, it is unclear how morphological trait turnover affects our inferences of trait niches, and our ability to answer this is in part limited by a lack of individual-level trait data. 3. Here, we directly address this by studying a montane Arctic plant-pollinator community over five growing seasons (>1,300 hours of fieldwork). Specifically, we linked every recorded plant-bumblebee interaction with the traits of the bee individual involved (n = 1,150), to investigate 1) whether plant taxa (n = 10) exhibited bee trait niches by interacting with specific regions of multidimensional trait space of visiting bumblebees, and 2) how our inference of these trait niches was affected by considering bumblebee trait turnover and plant taxon turnover. 4. When not considering turnover (interactions in space and time are pooled), plant taxa demonstrated bee trait niches. However, next we considered how bee trait space is reshaped over the elevational and seasonal gradient (especially with the emergence of different castes), and how this reshaping co-occurs with different spatiotemporal ranges of the plant taxa. From this we found the degree to which plant taxa exhibited trait niches declined significantly, and that seasonal reshaping of bee trait space was the primary driver of this trend. 5. Overall, in highly dynamic systems, like the Arctic, overlooking community turnover could mask and even overestimate the ability of morphology to explain interactions. Hence, determining how morphological traits of individual interaction partners are in phenological synchrony at localised scales will be fundamental to understanding the role morphology plays in underpinning plant-pollinator interactions.

ecology↗

Acute and chronic pesticide exposure trigger fundamentally different molecular responses in bumble bee brains

Beneficial wild insects including pollinators encounter various pesticide exposure conditions, from brief high concentrations to continuous low-level exposure. To effectively assess the environmental risks of pesticides, it is critical to understand how different exposure patterns influence their effects. Unfortunately, this knowledge remains limited. To clarify whether different exposure schemes disrupt the physiology of pollinators in similar manners, we exposed bumble bees to acute and chronic treatments of three different pesticides: Acetamiprid, clothianidin, and sulfoxaflor. Gene expression profiling enabled us to compare the effects of these treatments on the brain in a high-resolution manner. There were two main surprises: First, acute and chronic exposure schemes affected largely non-overlapping sets of genes. Second, different pesticides under the same exposure scheme showed more comparable effects than the same pesticide under different exposure schemes. Acute exposure caused up-regulation of stress response mechanisms causing distinct regulatory changes, rather than amplifying the effects of prolonged low-dose exposure that affected predominantly immunity and energy metabolism. These findings show that the mode of exposure critically determines the effects of pesticides. Our results signal the need for safety testing practices to better consider mode-of-exposure dependent effects and suggest that transcriptomics can support such improvements.

ecology↗

Honeybees vary collective decision making across landscapes

Honeybee (Apis mellifera) 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.

animal behavior and cognition↗

Mapping trait versus species turnover reveals spatiotemporal variation in functional redundancy in a plant-pollinator network

Functional overlap between species (redundancy) shapes competitive and mutualistic interactions, determining community responses to perturbations. Most studies view functional redundancy as static, even though individuals within species vary in traits over seasonal or spatial gradients. Consequently, we lack knowledge on trait turnover within species, how functional redundancy spatiotemporally varies, and when and where interaction networks are vulnerable to functional loss. Studying an Arctic bumblebee community, we investigated how body-size turnover over elevation and season shapes their host-plant interactions, and test how sensitive networks are to sequentially losing body-size groups. With trait turnover being larger than species, we found: i) late-season networks were less specialised when nodes comprised functionally similar bumblebees; ii) removal of bumblebee-body-size groups over species accelerated coextinction of host plants, with the magnitude varying in space and time. We demonstrate functional redundancy can vary spatiotemporally, and functional loss impacts interaction partners more than expected from species loss alone.

ecology↗

Genomic signatures of recent adaptation in a wild bumblebee

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 Bombus terrestris 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 Wolbachia 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.

evolutionary biology↗

Pollen source richness may be a poor predictor of bumblebee colony growth

O_LIAgricultural intensification has drastically altered foraging landscapes for bees, with large-scale crop monocultures associated with floral diversity loss. C_LIO_LIResearch 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. C_LIO_LIStudying 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. C_LIO_LIOver 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. C_LIO_LIOur 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. C_LI

ecology↗

Developmental exposure to pesticide contaminated food impedes bumblebee brain growth predisposing adults to become poorer learners

Understanding the risk to biodiversity from pesticide exposure is a global priority. For bees, an understudied step in evaluating pesticide risk is understanding how pesticide contaminated foraged food brought back to the colony can affect developing individuals. Provisioning bumblebee colonies with pesticide (neonicotinoid) treated food, we investigated how exposure during two key developmental phases (brood and/or early-adult), impacted brain growth and assessed the consequent effects on adult learning behaviour. Using micro-computed tomography ({micro}CT) scanning and 3D image analysis, we compared brain development for multiple neuropils in workers 3 and 12-days post-emergence. Mushroom body calyces were the neuropils most affected by exposure during either of the developmental phases, with both age cohorts showing smaller structural volumes. Critically, reduced calyces growth in pesticide exposed workers was associated with lower responsiveness to a sucrose reward and impaired learning performance. Furthermore, the impact from brood exposure appeared irrecoverable despite no exposure during adulthood.

ecology↗