Heatwave-like events affect drone production and brood-care behaviour in bumblebees.

Climate change is currently considered one of the major threats to biodiversity and is associated with an increase in the frequency and intensity of extreme weather events, such as heatwaves. Heatwaves create acutely stressful conditions that may lead to disruption in the performance and survival of ecologically and economically important organisms, such as insect pollinators. In this study, we investigated the impact of simulated heatwaves on the performance of queenless microcolonies of Bombus terrestris audax under laboratory conditions. Our results indicate that heatwaves can have significant impacts on bumblebee performance. However, contrary to our expectations, exposure to heatwaves did not affect survival. Exposure to a mild 5-day heatwave (30-32 °C) resulted in increased offspring production compared to those exposed to an extreme heatwave (34-36 °C) and to the control group (24 °C). We also found that brood-care behaviours were impacted by the magnitude of the heatwave. Wing fanning occurred occasionally at temperatures of 30-32 °C, whereas at 34-36 °C the proportion of workers engaged in this thermoregulatory behaviour increased significantly. Our results provide insights into the effects of heatwaves on bumblebee colony performance and underscore the use of microcolonies as a valuable tool for studying the effects of extreme weather events. Future research, especially field-based studies replicating natural foraging conditions, is crucial to complement laboratory-based studies to comprehend how heatwaves compromise the performance of pollinators. Such studies may potentially help to identify those species more resilient to climate change, as well as those that are most vulnerable.

Down-the-drain pathways for fipronil and imidacloprid applied as spot-on parasiticides to dogs: Estimating aquatic pollution.

Fipronil and imidacloprid have been widely detected in UK surface waters in recent years, often at concentrations that ecotoxicological studies have shown can harm aquatic life. Down-the-drain (DTD) passage of pet flea and tick treatments are being implicated as an important source, with many of the UK's 22 million cats and dogs receiving routine, year-round preventative doses containing these parasiticides. The UK Water Industry's 3rd Chemical Investigation Programme (UKWIR CIP3) has confirmed wastewater as a major entry pathway for these chemicals into surface waters, but the routes by which they enter the wastewater system remain unclear. We addressed this knowledge gap by conducting the first quantification of DTD emissions from 98 dogs treated with spot-on ectoparasiticides containing fipronil or imidacloprid, through bathing, bed washing and washing of owners' hands. Both chemicals were detected in 100 % of washoff samples, with bathing accounting for the largest emissions per event (up to 16.8 % of applied imidacloprid and 24.5 % of applied fipronil). Modelled to account for the frequency of emitting activities, owner handwashing was identified as the largest source of DTD emissions from the population overall, with handwash emissions occurring for at least 28 days following product application and an estimated 4.9 % of imidacloprid and 3.1 % of fipronil applied in dog spot-ons passing down-the-drain via this route. The normalised daily per capita emissions for all routes combined were 8.7 µg/person/day for imidacloprid and 2.1 µg/person/day for fipronil, equivalent to 20-40 % of the daily per capita load in wastewater, as estimated from UKWIR CIP3 data. Within the current international regulatory framework adhered to by the UK, the environmental exposure of veterinary medicines intended for use in small companion animals is assumed to be low, and DTD pathways are not considered. We recommend a systematic review of regulations and practices to address this overlooked pollution pathway.

Limited introgression from non-native commercial strains and signatures of adaptation in the key pollinator Bombus terrestris.

Insect pollination is fundamental for natural ecosystems and agricultural crops. The bumblebee species Bombus terrestris has become a popular choice for commercial crop pollination worldwide due to its effectiveness and ease of mass rearing. Bumblebee colonies are mass produced for the pollination of more than 20 crops and imported into over 50 countries including countries outside their native ranges, and the risk of invasion by commercial non-native bumblebees is considered an emerging issue for global conservation and biological diversity. Here, we use genome-wide data from seven wild populations close to and far from farms using commercial colonies, as well as commercial populations, to investigate the implications of utilizing commercial bumblebee subspecies in the UK. We find evidence for generally low levels of introgression between commercial and wild bees, with higher admixture proportions in the bees occurring close to farms. We identify genomic regions putatively involved in local and global adaptation, and genes in locally adaptive regions were found to be enriched for functions related to taste receptor activity, oxidoreductase activity, fatty acid and lipid biosynthetic processes. Despite more than 30 years of bumblebee colony importation into the UK, we observe low impact on the genetic integrity of local B. terrestris populations, but we highlight that even limited introgression might negatively affect locally adapted populations.

To flea or not to flea: survey of UK companion animal ectoparasiticide usage and activities affecting pathways to the environment.

Due to the convenience and efficacy of modern ectoparasiticides, routine prophylactic use has become commonplace for dogs and cats. However, the environmental consequences of this large-scale use are not well-understood, and multiple potential pathways for ectoparasiticides to the environment exist. Of particular concern is the potential for topically applied ectoparasiticides to pass to waterways, both down-the-drain via wastewater treatment plants and directly through swimming. In this online cross-sectional survey of 1,009 UK cat and dog owners, we investigated ectoparasiticide usage and the frequency of activities that are likely to result in transfer of the active substance to the environment, with a focus on pathways to waterways. A total of 603 dog owners and 406 cat owners completed the survey. Amongst dog and cat owners, 86.1% and 91.1% had administered an ectoparasiticide treatment to their pet in the preceding 12 months. Imidacloprid was the most frequently administered ectoparasiticide in both cats and dogs, followed by fluralaner in dogs and fipronil in cats. Eighty-four percent of owners who applied topical ectoparasiticides to their dog said they were aware of product warnings regarding swimming and bathing after application. Spot-on treated dogs were reported to swim significantly less frequently than non spot-on treated dogs (p = 0.007); however, 36.2% were reported to swim at least monthly. Similarly, significant differences were found in bathing frequency between spot-on treated and non spot-on treated dogs, with treated dogs less likely to be bathed at frequent (weekly) intervals, however 54.6% were reported to be bathed at least monthly. Washing of bedding was unaffected by ectoparasiticide treatment, and 87.8% of dog owners and 69.1% of cat-owners reported washing their pet's bedding at least every 3 months, suggesting that residue washoff from bedding may be occurring for most topically treated animals. Results suggest that transfer of ectoparasiticides to the environment is likely to occur for many of the millions of animals treated annually in the UK, with imidacloprid spot-on treated dogs estimated to swim, be bathed and have their bedding washed over 3.3 million, 5 million and 6.3 million times per year, respectively.

Feeling the heat: Bumblebee workers show no acclimation capacity of upper thermal tolerance to simulated heatwaves.

Climate change is our most significant challenge in the 21st century and among the main drivers of biodiversity loss. Recent distributional shifts and declines in crucial pollinators, such as bumblebees, seem to be associated to this phenomenon. However, despite future climate projections on climate warming, few studies have assessed the ability of temperate bumblebees to acclimate to extreme weather events, such as heatwaves. This study estimates the upper critical thermal limits (Critical Thermal Maximum (CTmax) and Heat Coma Temperature (HCT)), of the bumblebee subspecies Bombus terrestris audax, and assesses whether CTmax increases following exposure to a simulated heatwave. The critical thermal maximum occurred between 48.9 and 52.7 °C, while the heat coma temperature varied between 50.7 and 53.4 °C. After measurement of HCT, around 23% of bees survived 24 h or longer, but coordination was never recovered. There was no significant association between upper critical thermal limits and body mass, which highlights the need to investigate other factors to comprehend the mechanisms behind thermal tolerance limits. Furthermore, the heatwave treatments had no significant effect on the CTmax of bumblebee workers, indicating no acclimation capacity of upper thermal tolerance to simulated heatwaves. Our study provides insights into the upper thermal tolerance limits of Bombus terrestris audax and reveals that exposure to heatwave-like events does not change the upper thermal tolerance of bees, highlighting the need to develop effective strategies that might enable them to cope with extreme weather events.

Habitat quality, urbanisation & pesticides influence bird abundance and richness in gardens.

Gardens are regularly portrayed as green oases, refuges for wildlife that has been displaced from the countryside by intensive farming practices which have reduced habitat availability. Pesticides are also commonly used in urban areas, but few studies have investigated their impacts. In this study, we explored how bird richness and abundance in gardens across the UK are influenced by habitat quality, urbanisation level and pesticide practices. To achieve this, we collaborated with the British Trust for Ornithology (BTO) which runs Garden Birdwatch, a citizen-science-based garden bird recording scheme. Participants in the study were asked to complete a questionnaire about their pesticide practice. From the 615 gardens that provided useful data, we found that 32.2 % applied pesticides in their gardens and that glyphosate comprised 53.3 % of these applications. We found that bird abundance and species richness was lower in suburban compared to rural gardens but positively influenced by measures of garden quality and by surrounding habitat quality. We show that there was an interaction between the habitat quality of the surrounding area and pesticide use: negative effects of pesticides on species richness were more pronounced in gardens in areas of high habitat quality compared to those surrounded by poor habitat. We found that pesticide use, and particularly glyphosate and metaldehyde, negatively predicted the abundance of house sparrows, a fast-declining bird species. The average house sparrow abundance was 12.1 % lower in gardens applying any pesticide, 24.9 % lower with glyphosate, and 38.6 % lower with metaldehyde. Overall, our study shows that garden bird abundance and richness is strongly influenced by both extrinsic and intrinsic factors, and suggests that garden management, particularly regarding pesticide use, has a significant effect on bird life.

DoPI: The Database of Pollinator Interactions.

Despite the importance of pollinating insects to natural environments and agriculture, there have been few attempts to unite the existing plant-pollinator interaction datasets into a single depository using a common format. Accordingly, we have created one of the world's first online, open-access, and searchable pollinator-plant interaction databases. DoPI (The Database of Pollinator Interactions) was built from a systematic review of the scientific literature and unpublished datasets requested from researchers and organizations. We collated records of interactions between British plant and insect flower-visitor species (or genera), together with associated metadata (date, location, habitat, source publication) when available. The dataset currently (December 2021) contains 101,539 records, detailing over 320,000 interactions. The number of interactions (i.e., the number of times a pairwise species interaction was recorded per occasion) varies considerably among records, averaging 3.6. These include records from 1888 pollinator species and 1241 plant species, totaling >17,000 pairwise species interactions. By combining a large volume of information in a single repository, DoPI can be used to answer fundamental ecological questions on the dynamics of pollination interactions in space and time, as well as applied questions in conservation practice. We hope this dynamic database will be a useful tool not only for researchers, but also for conservationists, funding agencies, governmental departments, beekeepers, agronomists, and gardeners. We request that this paper is cited when using the data in publications and individual studies when appropriate. Researchers and organizations are encouraged to add further data in the future. The database can be accessed at: https://www.dopi.org.uk/.

Anthropogenic influences on bee foraging.

Efficient foraging is vital to bee fitness but is challenging in the Anthropocene.

Field evidence of UK wild bird exposure to fludioxonil and extrapolation to other pesticides used as seed treatments.

We determine the exposure of wild birds to pesticides via consumption of fludioxonil-treated winter wheat seeds following autumn drilling. We recorded the density of seeds left on the soil surface, bird density, and consumption of pesticide-treated seed by birds using camera traps. We calculated the dose ingested by each bird species in a single feeding bout and if they ate treated seeds exclusively for 1 day. We extrapolated this for an additional 19 pesticides commonly used as seed treatments, assuming equal consumption rates. All three fields contained grains on the soil surface (mean 7.14 seeds/m2 on sowing day). In total, 1,374 granivorous birds spanning 18 different species were observed in the fields, with 11 species filmed eating the seeds. Fludioxonil appears to pose a low risk to birds, with <1.14% of the LD50 potentially ingested by a bird for a daily maximum amount of seeds. Analysis of the further 19 pesticides commonly used as seed dressings suggests that the neonicotinoid insecticides imidacloprid, clothianidin, and thiamethoxam represent the highest risk for granivorous birds. For example, chaffinch (Fringilla coelebs) could consume 63% of LD50 of imidacloprid in a single feeding bout, and 370% in a day. Further investigation is clearly required to determine whether seeds treated with these other pesticides are consumed as readily as those treated with fludioxonil, as if so this is likely to cause significant harm.

Novel nectar robbing negatively affects reproduction in Digitalis purpurea.

With many plant-pollinator interactions undergoing change as species' distributions shift, we require a better understanding of how the addition of new interacting partners can affect plant reproduction. One such group of floral visitors, nectar robbers, can deplete plants of nectar rewards without contributing to pollination. The addition of nectar robbing to the floral visitor assemblage could therefore have costs to the plant´s reproductive output. We focus on a recent plant colonist, Digitalis purpurea, a plant that in its native range is rarely robbed, but experiences intense nectar robbing in areas it has been introduced to. Here, we test the costs to reproduction following experimental nectar robbing. To identify any changes in the behavior of the principal pollinators in response to nectar robbing, we measured visitation rates, visit duration, proportion of flowers visited, and rate of rejection of inflorescences. To find the effects of robbing on fitness, we used proxies for female and male components of reproductive output, by measuring the seeds produced per fruit and the pollen export, respectively. Nectar robbing significantly reduced the rate of visitation and lengths of visits by bumblebees. Additionally, bumblebees visited a lower proportion of flowers on an inflorescence that had robbed flowers. We found that flowers in the robbed treatment produced significantly fewer seeds per fruit on average but did not export fewer pollen grains. Our finding that robbing leads to reduced seed production could be due to fewer and shorter visits to flowers leading to less effective pollination. We discuss the potential consequences of new pollinator environments, such as exposure to nectar robbing, for plant reproduction.

Evaluating competition for forage plants between honey bees and wild bees in Denmark.

A recurrent concern in nature conservation is the potential competition for forage plants between wild bees and managed honey bees. Specifically, that the highly sophisticated system of recruitment and large perennial colonies of honey bees quickly exhaust forage resources leading to the local extirpation of wild bees. However, different species of bees show different preferences for forage plants. We here summarize known forage plants for honey bees and wild bee species at national scale in Denmark. Our focus is on floral resources shared by honey bees and wild bees, with an emphasis on both threatened wild bee species and foraging specialist species. Across all 292 known bee species from Denmark, a total of 410 plant genera were recorded as forage plants. These included 294 plant genera visited by honey bees and 292 plant genera visited by different species of wild bees. Honey bees and wild bees share 176 plant genera in Denmark. Comparing the pairwise niche overlap for individual bee species, no significant relationship was found between their overlap and forage specialization or conservation status. Network analysis of the bee-plant interactions placed honey bees aside from most other bee species, specifically the module containing the honey bee had fewer links to any other modules, while the remaining modules were more highly inter-connected. Despite the lack of predictive relationship from the pairwise niche overlap, data for individual species could be summarized. Consequently, we have identified a set of operational parameters that, based on a high foraging overlap (>70%) and unfavorable conservation status (Vulnerable+Endangered+Critically Endangered), can guide both conservation actions and land management decisions in proximity to known or suspected populations of these species.

Investigating the Foraging, Guarding and Drifting Behaviors of Commercial Bombus terrestris.

Social insects have high levels of cooperation and division of labor. In bumble bees this is partly size-based, with larger bees performing tasks outside the nest and smaller bees remaining inside, although bumble bees still display considerable behavioral plasticity. The level of specialization in tasks outside the colony, including foraging, guarding and drifting (entering a foreign colony), is currently unknown for bumble bees. This study aimed to assess division of labor between outside tasks and the degree of specialization in foraging, guarding, and switching colonies in commercially reared bumble bees placed in the field. Nine factory-bought Bombus terrestris colonies were placed on three farms in Sussex, UK, between June and August 2015. Forty workers from each colony were radio-tagged and a reader on the colony entrance recorded the date, time and bee ID as they passed. The length and frequency of foraging trips and guarding behavior were calculated, and drifting recorded. The mean (±SD) length of foraging trips was 45 ± 36 min, and the mean number of foraging trips per day was 7.75 ± 7.71. Low levels of specialization in guarding or foraging behavior were found; however, some bees appeared to guard more frequently than others, and twenty bees were categorized as guards. Five bees appeared to exhibit repeated "stealing" behavior, which may have been a specialist task. The division of labor between tasks was not size-based. It is concluded that commercial bumble bees are flexible in performing outside nest tasks and may have diverse foraging strategies including intra-specific nest robbing. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10905-021-09790-0.

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems.

New information on the lethal and sublethal effects of neonicotinoids and fipronil on organisms is presented in this review, complementing the previous Worldwide Integrated Assessment (WIA) in 2015. The high toxicity of these systemic insecticides to invertebrates has been confirmed and expanded to include more species and compounds. Most of the recent research has focused on bees and the sublethal and ecological impacts these insecticides have on pollinators. Toxic effects on other invertebrate taxa also covered predatory and parasitoid natural enemies and aquatic arthropods. Little new information has been gathered on soil organisms. The impact on marine and coastal ecosystems is still largely uncharted. The chronic lethality of neonicotinoids to insects and crustaceans, and the strengthened evidence that these chemicals also impair the immune system and reproduction, highlights the dangers of this particular insecticidal class (neonicotinoids and fipronil), with the potential to greatly decrease populations of arthropods in both terrestrial and aquatic environments. Sublethal effects on fish, reptiles, frogs, birds, and mammals are also reported, showing a better understanding of the mechanisms of toxicity of these insecticides in vertebrates and their deleterious impacts on growth, reproduction, and neurobehaviour of most of the species tested. This review concludes with a summary of impacts on the ecosystem services and functioning, particularly on pollination, soil biota, and aquatic invertebrate communities, thus reinforcing the previous WIA conclusions (van der Sluijs et al. 2015).

Multiple stressors interact to impair the performance of bumblebee Bombus terrestris colonies.

Bumblebees are constantly exposed to a wide range of biotic and abiotic stresses which they must defend themselves against to survive. Pathogens and pesticides represent important stressors that influence bumblebee health, both when acting alone or in combination. To better understand bumblebee health, we need to investigate how these factors interact, yet experimental studies to date generally focus on only one or two stressors. The aim of this study is to evaluate how combined effects of four important stressors (the gut parasite Nosema ceranae, the neonicotinoid insecticide thiamethoxam, the pyrethroid insecticide cypermethrin and the EBI fungicide tebuconazole) interact to affect bumblebees at the individual and colony levels. We established seven treatment groups of colonies that we pulse exposed to different combinations of these stressors for 2 weeks under laboratory conditions. Colonies were subsequently placed in the field for 7 weeks to evaluate the effect of treatments on the prevalence of N. ceranae in inoculated bumblebees, expression levels of immunity and detoxification-related genes, food collection, weight gain, worker and male numbers, and production of worker brood and reproductives. Exposure to pesticide mixtures reduced food collection by bumblebees. All immunity-related genes were upregulated in the bumblebees inoculated with N. ceranae when they had not been exposed to pesticide mixtures, and bumblebees exposed to the fungicide and the pyrethroid were less likely to have N. ceranae. Combined exposure to the three-pesticide mixture and N. ceranae reduced bumblebee colony growth, and all treatments had detrimental effects on brood production. The groups exposed to the neonicotinoid insecticide produced 40%-76% fewer queens than control colonies. Our findings show that exposure to combinations of stressors that bumblebees frequently come into contact with have detrimental effects on colony health and performance and could therefore have an impact at the population level. These results also have significant implications for current practices and policies for pesticide risk assessment and use as the combinations tested here are frequently applied simultaneously in the field. Understanding the interactions between different stressors will be crucial for improving our ability to manage bee populations and for ensuring pollination services into the future.

Los abejorros están constantemente expuestos a una amplia gama de agentes estresantes bióticos y abióticos de los que deben defenderse para sobrevivir. Los patógenos y los pesticidas son importantes factores estresantes que influyen en la salud de los abejorros, tanto cuando actúan solos como en combinación. Para tener un mejor conocimiento sobre la salud de los abejorros, debemos investigar cómo interactúan estos factores estresantes, pero los estudios experimentales hasta la fecha generalmente se centran en estudiar solo uno o dos factores. El objetivo de nuestro estudio es evaluar cómo los efectos combinados de cuatro importantes factores estresantes (el parásito intestinal Nosema ceranae, el insecticida neonicotinoide tiametoxam, el insecticida piretroide cipermetrina y el fungicida EBI tebuconazol) interactúan para afectar a los abejorros a nivel individual y de colonia. Establecimos siete grupos de tratamiento de colonias de abejorros que expusimos a diferentes combinaciones de estos factores estresantes durante dos semanas en condiciones de laboratorio, y posteriormente se colocaron en el campo durante siete semanas, para evaluar el efecto de los tratamientos sobre la prevalencia de N. ceranae en abejorros inoculados, los niveles de expresión de genes relacionados con la inmunidad y la desintoxicación, la recolección de alimentos, el aumento de peso, el número de obreras y machos, y la producción de cría de obreras, machos y reinas. La exposición a mezclas de pesticidas redujo la recolección de alimentos por parte de los abejorros. Todos los genes relacionados con la inmunidad se sobre-expresaron en los abejorros inoculados con N. ceranae cuando no habían estado expuestos a mezclas de pesticidas, y los abejorros expuestos al fungicida y al piretroide presentaron menos probabilidades de tener N. ceranae. La exposición combinada a la mezcla de tres pesticidas y N. ceranae redujo el crecimiento de la colonia de abejorros y todos los tratamientos tuvieron efectos perjudiciales en la producción de crías. Los grupos expuestos al insecticida neonicotinoide produjeron entre un 40 y un 76% menos de reinas que las colonias control. Nuestros hallazgos muestran que la exposición a combinaciones de factores estresantes con los que los abejorros entran frecuentemente en contacto tiene efectos perjudiciales sobre la salud y el rendimiento de la colonia y, por lo tanto, podría tener un impacto a nivel poblacional. Estos resultados también tienen importantes implicaciones para las prácticas y políticas actuales de evaluación de riesgos y uso de plaguicidas, ya que las combinaciones probadas aquí se aplican con frecuencia simultáneamente en el campo. Comprender las interacciones entre los diferentes factores de estrés es fundamental para mejorar nuestra capacidad de gestión de las poblaciones de abejas y así garantizar los servicios de polinización en el futuro.

Potential role of veterinary flea products in widespread pesticide contamination of English rivers.

Little is known about the environmental fate or impact of pesticides used to control companion animal parasites. Using data from the Environment Agency, we examined the occurrence of fipronil, fipronil metabolites and imidacloprid in 20 English rivers from 2016 to 2018, as indicators of the potential contamination of waterways from their use as ectoparasiticides on pets. Water samples were collected by the Environment Agency as part of their chemical surveillance programme and analysed using Liquid Chromatography Mass Spectrometry / Quadrupole-Time-of-Flight Mass spectrometry (LC/Q-TOF-MS) methods. A total of 3861 chemical analyses were examined, and the significance and potential sources of this contamination were assessed. Fipronil, fipronil sulfone, fipronil sulfide (collectively known as fiproles) and imidacloprid were detected in 98.6%, 96.5%, 68.7% and 65.9% of samples, respectively. Across the river sites sampled, the mean concentrations of fipronil (17 ng/l, range <0.3-980 ng/l), and fipronil sulfone (6.5 ng/l, range <0.2-39 ng/l) were 5.3 and 38.1 times their chronic toxicity limits of 3.2 and 0.17 ng/l, respectively. Imidacloprid had a mean concentration of 31.7 ng/l (range <1-360 ng/l), which was below its chronic toxicity limit of 35 ng/l, however seven out of 20 sites exceeded that limit. Chronic risk quotients indicate a high environmental risk to aquatic ecosystems from fiproles, and a moderate risk from imidacloprid. Sites immediately downstream of wastewater treatment works had the highest levels of fipronil and imidacloprid, supporting the hypothesis that potentially significant quantities of pesticides from veterinary flea products may be entering waterways via household drains. These findings suggest the need for a reevaluation of the environmental risks associated with the use of companion animal parasiticide products, and the risk assessments that these products undergo prior to regulatory approval.