Publications
23 results found
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.
Yordanova M, Evison SEF, Gill RJ, et 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.
Piot N, Schweiger O, Meeus I, et al., 2022, Honey bees and climate explain viral prevalence in wild bee communities on a continental scale, Scientific Reports, Vol: 12, ISSN: 2045-2322
Viruses are omnipresent, yet the knowledge on drivers of viral prevalence in wild host populations is often limited. Biotic factors, such as sympatric managed host species, as well as abiotic factors, such as climatic variables, are likely to impact viral prevalence. Managed and wild bees, which harbor several multi-host viruses with a mostly fecal-oral between-species transmission route, provide an excellent system with which to test for the impact of biotic and abiotic factors on viral prevalence in wild host populations. Here we show on a continental scale that the prevalence of three broad host viruses: the AKI-complex (Acute bee paralysis virus, Kashmir bee virus and Israeli acute paralysis virus), Deformed wing virus, and Slow bee paralysis virus in wild bee populations (bumble bees and solitary bees) is positively related to viral prevalence of sympatric honey bees as well as being impacted by climatic variables. The former highlights the need for good beekeeping practices, including Varroa destructor management to reduce honey bee viral infection and hive placement. Furthermore, we found that viral prevalence in wild bees is at its lowest at the extreme ends of both temperature and precipitation ranges. Under predicted climate change, the frequency of extremes in precipitation and temperature will continue to increase and may hence impact viral prevalence in wild bee communities.
Rothman JA, Russell KA, Leger L, et al., 2020, The direct and indirect effects of environmental toxicants on the health of bumblebees and their microbiomes, PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, Vol: 287, ISSN: 0962-8452
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- Citations: 21
Figueroa LL, Grab H, Ng WH, et al., 2020, Landscape simplification shapes pathogen prevalence in plant-pollinator networks, ECOLOGY LETTERS, Vol: 23, Pages: 1212-1222, ISSN: 1461-023X
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- Citations: 52
Graystock P, Ng WH, Parks K, et al., 2020, Dominant bee species and floral abundance drive parasite temporal dynamics in plant-pollinator communities, Nature Ecology and Evolution, Vol: 4, Pages: 1358-1367, ISSN: 2397-334X
Pollinator reductions can leave communities less diverse and potentially at increased risk of infectious diseases. Species-rich plant and bee communities have high species turnover, making the study of disease dynamics challenging. To address how temporal dynamics shape parasite prevalence in plant and bee communities, we screened >5,000 bees and flowers over an entire growing season for five common bee microparasites (Nosema ceranae, Nosema bombi, Crithidia bombi, Crithidia expoeki and neogregarines). Over 110 bee species and 89 flower species were screened, revealing that 42% of bee species (12.2% individual bees) and 70% of flower species (8.7% individual flowers) had at least one parasite in or on them, respectively. Some common flowers (for example, Lychnis flos-cuculi) harboured multiple parasite species whilst others (for example, Lythrum salicaria) had few. Significant temporal variation of parasite prevalence in bees was linked to bee diversity, bee and flower abundance and community composition. Specifically, we found that bee communities had the highest prevalence late in the season, when social bees (Bombus spp. and Apis mellifera) were dominant and bee diversity was lowest. Conversely, prevalence on flowers was lowest late in the season when floral abundance was highest. Thus turnover in the bee community impacted community-wide prevalence, and turnover in the plant community impacted when parasite transmission was likely to occur at flowers. These results imply that efforts to improve bee health will benefit from the promotion of high floral numbers to reduce transmission risk, maintaining bee diversity to dilute parasites and monitoring the abundance of dominant competent hosts.
Rothman JA, Russell KA, Leger L, et al., 2020, The direct and indirect effects of environmental toxicants on the health of bumble bees and their microbiomes
<jats:title>Abstract</jats:title><jats:p>Bumble bees (<jats:italic>Bombus</jats:italic> spp.) are important and widespread insect pollinators, but the act of foraging on flowers can expose them to harmful pesticides and environmental chemicals such as oxidizers and heavy metals. How these compounds directly influence bee survival and indirectly affect bee health via the gut microbiome is largely unknown. As the toxins and toxicants in floral nectar and pollen take many forms, we explored the genomes of core bumblebee microbes (Using RAST) for their potential to detoxify cadmium, copper, selenium, the neonicotinoid pesticide imidacloprid, and hydrogen peroxide - which have all been identified in floral nectar and pollen. We then exposed <jats:italic>Bombus impatiens</jats:italic> workers to varying concentrations of these chemicals spiked into their diet and identified the direct effects on bee survival. Using field realistic doses, we further explored indirect effects on bee microbiomes. We found multiple genes in core gut microbes that have the potential to aid in detoxifying harmful chemicals. We also found that while the chemicals are largely toxic at levels within and above field-realistic concentrations, the field-realistic concentrations - except for imidacloprid - altered the composition of the bee microbiome, potentially causing gut dysbiosis. Overall, our study shows that environmental chemicals found in floral nectar and pollen can directly cause bee mortality, and at field-realistic levels, likely have indirect, deleterious effects on bee health via their influence on the bee microbiome.</jats:p>
Rothman JA, Leger L, Graystock P, et al., 2019, The bumble bee microbiome increases survival of bees exposed to selenate toxicity, Environmental Microbiology, Vol: 21, Pages: 3417-3429, ISSN: 1462-2912
Bumble bees are important and widespread insect pollinators who face many environmental challenges. For example, bees are exposed to the metalloid selenate when foraging on pollen and nectar from plants growing in contaminated soils. As it has been shown that the microbiome of animals reduces metalloid toxicity, we assayed the ability of the bee microbiome to increase survivorship against selenate challenge. We exposed uninoculated or microbiota-inoculated Bombus impatiens workers to a field-realistic dose of 0.75 mg l-1 selenate and found that microbiota-inoculated bees survive slightly but significantly longer than uninoculated bees. Using 16S rRNA gene sequencing, we found that selenate exposure altered gut microbial community composition and relative abundance of specific core bacteria. We also grew two core bumble bee microbes - Snodgrassella alvi and Lactobacillus bombicola - in selenate-spiked media and found that these bacteria grew in the tested concentrations of 0.001-10 mg l-1 selenate. Furthermore, the genomes of these microbes harbour genes involved in selenate detoxification. The bumble bee microbiome slightly increases survivorship when the host is exposed to selenate, but the specific mechanisms and colony-level benefits under natural settings require further study.
Southon RJ, Bell EF, Graystock P, et al., 2019, High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp polistes canadensis, Molecular Ecology, Vol: 28, Pages: 3271-3284, ISSN: 0962-1083
Explaining the evolution of helping behaviour in the eusocial insects where non-reproductive ('worker') individuals help raise the offspring of other individuals ('queens'), remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on non-tropical species, where seasonality causes family groups to disperse; cofoundresses forming new colonies the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes - Polistes canadensis. Using both microsatellites and newly-developed single-nucleotide polymorphism (SNP) markers we show that adult cofoundresses are highly related, and that brood production is monopolised by a single female across the nesting cycle. Non-reproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life-history and ecologies when considering the evolution of reproductive strategies.
Brockmeier EK, Hodges G, Hutchinson TH, et al., 2017, The role of omics in the application of adverse outcome pathways for chemical risk assessment, Toxicological Sciences, Vol: 158, Pages: 252-262, ISSN: 1096-0929
In conjunction with the second International Environmental Omics Symposium (iEOS) conference, held at the University of Liverpool (United Kingdom) in September 2014, a workshop was held to bring together experts in toxicology and regulatory science from academia, government and industry. The purpose of the workshop was to review the specific roles that high-content omics datasets (eg, transcriptomics, metabolomics, lipidomics, and proteomics) can hold within the adverse outcome pathway (AOP) framework for supporting ecological and human health risk assessments. In light of the growing number of examples of the application of omics data in the context of ecological risk assessment, we considered how omics datasets might continue to support the AOP framework. In particular, the role of omics in identifying potential AOP molecular initiating events and providing supportive evidence of key events at different levels of biological organization and across taxonomic groups was discussed. Areas with potential for short and medium-term breakthroughs were also discussed, such as providing mechanistic evidence to support chemical read-across, providing weight of evidence information for mode of action assignment, understanding biological networks, and developing robust extrapolations of species-sensitivity. Key challenges that need to be addressed were considered, including the need for a cohesive approach towards experimental design, the lack of a mutually agreed framework to quantitatively link genes and pathways to key events, and the need for better interpretation of chemically induced changes at the molecular level. This article was developed to provide an overview of ecological risk assessment process and a perspective on how high content molecular-level datasets can support the future of assessment procedures through the AOP framework.
Graystock P, Rehan SM, McFrederick QS, 2017, Hunting for healthy microbiomes: determining the core microbiomes of Ceratina, Megalopta, and Apis bees and how they associate with microbes in bee collected pollen, Conservation Genetics, Vol: 18, Pages: 701-711, ISSN: 1566-0621
Social corbiculate bees such as honey bees and bumble bees maintain a specific beneficial core microbiome which is absent in wild bees. It has been suggested that maintaining this microbiome can prevent disease and keep bees healthy. The main aim of our study was to identify if there are any core bacterial groups in the non-corbiculate bees Ceratina and Megalopta that have been previously overlooked. We additionally test for associations between the core bee microbes and pollen provisions to look for potential transmission between the two. We identify three enterotypes in Ceratina samples, with thirteen core bacterial phylotypes in Ceratina females: Rosenbergiella, Pseudomonas, Gilliamella, Lactobacillus, Caulobacter, Snodgrassella, Acinetobacter, Corynebacterium, Sphingomonas, Commensalibacter, Methylobacterium, Massilia, and Stenotrophomonas, plus 19 in pollen (6 of which are shared by bees). Unlike Apis bees, whose gut microbial community differs compared to their pollen, Ceratina adults and pollen largely share a similar microbial composition and enterotype difference was largely explained by pollen age. Megalopta displays a highly diverse composition of microbes throughout all adults, yet Lactobacillus and Saccharibacter were prevalent in 90% of adults as core bacteria. Only Lactobacillus was both a core bee and pollen provision microbe in all three species. The consequences of such diversity in core microbiota between bee genera and their associations with pollen are discussed in relation to identifying potentially beneficial microbial taxa in wild bees to aid the conservation of wild, understudied, non-model bee species.
Smith AR, Graystock P, Hughes WOH, 2016, Specialization on pollen or nectar in bumblebee foragers is not associated with ovary size, lipid reserves or sensory tuning, PeerJ, Vol: 4, ISSN: 2167-8359
Foraging specialization allows social insects to more efficiently exploit resources in their environment. Recent research on honeybees suggests that specialization on pollen or nectar among foragers is linked to reproductive physiology and sensory tuning (the Reproductive Ground-Plan Hypothesis; RGPH). However, our understanding of the underlying physiological relationships in non-Apis bees is still limited. Here we show that the bumblebee Bombus terrestris has specialist pollen and nectar foragers, and test whether foraging specialization in B. terrestris is linked to reproductive physiology, measured as ovarian activation. We show that neither ovary size, sensory sensitivity, measured through proboscis extension response (PER), or whole-body lipid stores differed between pollen foragers, nectar foragers, or generalist foragers. Body size also did not differ between any of these three forager groups. Non-foragers had significantly larger ovaries than foragers. This suggests that potentially reproductive individuals avoid foraging.
Graystock P, Jones JC, Pamminger T, et al., 2016, Hygienic food to reduce pathogen risk to bumblebees, JOURNAL OF INVERTEBRATE PATHOLOGY, Vol: 136, Pages: 68-73, ISSN: 0022-2011
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- Citations: 24
Graystock P, Blane EJ, McFrederick QS, et al., 2016, Do managed bees drive parasite spread and emergence in wild bees?, International Journal for Parasitology: Parasites and Wildlife, Vol: 5, Pages: 64-75, ISSN: 2213-2244
Bees have been managed and utilised for honey production for centuries and, more recently, pollination services. Since the mid 20th Century, the use and production of managed bees has intensified with hundreds of thousands of hives being moved across countries and around the globe on an annual basis. However, the introduction of unnaturally high densities of bees to areas could have adverse effects. Importation and deployment of managed honey bee and bumblebees may be responsible for parasite introductions or a change in the dynamics of native parasites that ultimately increases disease prevalence in wild bees. Here we review the domestication and deployment of managed bees and explain the evidence for the role of managed bees in causing adverse effects on the health of wild bees. Correlations with the use of managed bees and decreases in wild bee health from territories across the globe are discussed along with suggestions to mitigate further health reductions in wild bees.
Graystock P, Meeus I, Smagghe G, et al., 2016, The effects of single and mixed infections of <i>Apicystis bombi</i> and deformed wing virus in <i>Bombus terrestris</i>, PARASITOLOGY, Vol: 143, Pages: 358-365, ISSN: 0031-1820
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- Citations: 49
Graystock P, Goulson D, Hughes WOH, 2015, Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species, Proceedings of the Royal Society B: Biological Sciences, Vol: 282, ISSN: 0962-8452
The dispersal of parasites is critical for epidemiology, and the interspecific vectoring of parasites when species share resources may play an underappreciated role in parasite dispersal. One of the best examples of such a situation is the shared use of flowers by pollinators, but the importance of flowers and interspecific vectoring in the dispersal of pollinator parasites is poorly understood and frequently overlooked. Here, we use an experimental approach to show that during even short foraging periods of 3 h, three bumblebee parasites and two honeybee parasites were dispersed effectively onto flowers by their hosts, and then vectored readily between flowers by non-host pollinator species. The results suggest that flowers are likely to be hotspots for the transmission of pollinator parasites and that considering potential vector, as well as host, species will be of general importance for understanding the distribution and transmission of parasites in the environment and between pollinators.
Southon RJ, Bell EF, Graystock P, et al., 2015, Long live the wasp: adult longevity in captive colonies of the eusocial paper wasp Polistes canadensis (L.), PeerJ, Vol: 3, ISSN: 2167-8359
Insects have been used as an exemplary model in studying longevity, from extrinsic mortality pressures to intrinsic senescence. In the highly eusocial insects, great degrees of variation in lifespan exist between morphological castes in relation to extreme divisions of labour, but of particular interest are the primitively eusocial insects. These species represent the ancestral beginnings of eusociality, in which castes are flexible and based on behaviour rather than morphology. Here we present data on the longevity of the primitively eusocial Neotropical paper wasp P. canadensis, in a captive setting removed of environmental hazards. Captive Polistes canadensis had an average lifespan of 193 ± 10.5 days; although this average is shorter than most bee and ant queens, one individual lived for 506 days in the lab—longer than most recorded wasps and bees. Natal colony variation in longevity does exist between P. canadensis colonies, possibly due to nutritional and genetic factors. This study provides a foundation for future investigations on the effects of intrinsic and extrinsic factors on longevity in primitively eusocial insects, as well as the relationship with natal group and cohort size.
Graystock P, Goulson D, Hughes WOH, 2014, The relationship between managed bees and the prevalence of parasites in bumblebees, PeerJ, Vol: 2, Pages: 1-14, ISSN: 2167-8359
Honey bees and, more recently, bumblebees have been domesticated and are now managed commercially primarily for crop pollination, mixing with wild pollinators during foraging on shared flower resources. There is mounting evidence that managed honey bees or commercially produced bumblebees may affect the health of wild pollinators such as bumblebees by increasing competition for resources and the prevalence of parasites in wild bees. Here we screened 764 bumblebees from around five greenhouses that either used commercially produced bumblebees or did not, as well as bumblebees from 10 colonies placed at two sites either close to or far from a honey bee apiary, for the parasites Apicystis bombi, Crithidia bombi, Nosema bombi, N. ceranae, N. apis and deformed wing virus. We found that A. bombi and C. bombi were more prevalent around greenhouses using commercially produced bumblebees, while C. bombi was 18% more prevalent in bumblebees at the site near to the honey bee apiary than those at the site far from the apiary. Whilst these results are from only a limited number of sites, they support previous reports of parasite spillover from commercially produced bumblebees to wild bumblebees, and suggest that the impact of stress from competing with managed bees or the vectoring of parasites by them on parasite prevalence in wild bees needs further investigation. It appears increasingly likely that the use of managed bees comes at a cost of increased parasites in wild bumblebees, which is not only a concern for bumblebee conservation, but which may impact other pollinators as well.
Tranter C, Graystock P, Shaw C, et al., 2014, Sanitizing the fortress: protection of ant brood and nest material by worker antibiotics, BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY, Vol: 68, Pages: 499-507, ISSN: 0340-5443
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- Citations: 26
Maharramov J, Meeus I, Maebe K, et al., 2013, Genetic variability of the neogregarine apicystis bombi, an etiological agent of an emergent bumblebee disease, PLoS One, Vol: 8, Pages: 1-8, ISSN: 1932-6203
The worldwide spread of diseases is considered a major threat to biodiversity and a possible driver of the decline of pollinator populations, particularly when novel species or strains of parasites emerge. Previous studies have suggested that populations of introduced European honeybee (Apis mellifera) and bumblebee species (Bombus terrestris and Bombus ruderatus) in Argentina share the neogregarine parasite Apicystis bombi with the native bumblebee (Bombus dahlbomii). In this study we investigated whether A. bombi is acting as an emergent parasite in the non-native populations. Specifically, we asked whether A. bombi, recently identified in Argentina, was introduced by European, non-native bees. Using ITS1 and ITS2 to assess the parasite’s intraspecific genetic variation in bees from Argentina and Europe, we found a largely unstructured parasite population, with only 15% of the genetic variation being explained by geographic location. The most abundant haplotype in Argentina (found in all 9 specimens of non-native species) was identical to the most abundant haplotype in Europe (found in 6 out of 8 specimens). Similarly, there was no evidence of structuring by host species, with this factor explaining only 17% of the genetic variation. Interestingly, parasites in native Bombus ephippiatus from Mexico were genetically distant from the Argentine and European samples, suggesting that sufficient variability does exist in the ITS region to identify continent-level genetic structure in the parasite. Thus, the data suggest that A. bombi from Argentina and Europe share a common, relatively recent origin. Although our data did not provide information on the direction of transfer, the absence of genetic structure across space and host species suggests that A. bombi may be acting as an emergent infectious disease across bee taxa and continents.
Graystock P, Yates K, Darvill B, et al., 2013, Emerging dangers: Deadly effects of an emergent parasite in a new pollinator host, JOURNAL OF INVERTEBRATE PATHOLOGY, Vol: 114, Pages: 114-119, ISSN: 0022-2011
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- Citations: 111
Graystock P, Yates K, Evison SEF, et al., 2013, The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies, JOURNAL OF APPLIED ECOLOGY, Vol: 50, Pages: 1207-1215, ISSN: 0021-8901
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- Citations: 147
Graystock P, Hughes WOH, 2011, Disease resistance in a weaver ant, Polyrhachis dives, and the role of antibiotic-producing glands, BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY, Vol: 65, Pages: 2319-2327, ISSN: 0340-5443
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- Citations: 41
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