Intensive agriculture currently relies on pesticides to maximize crop yield
. Neonicotinoids are the most widely used insecticides globally
, but increasing evidence of negative impacts on important ...pollinators
and other non-target organisms
has led to legislative reassessment and created demand for the development of alternative products. Sulfoximine-based insecticides are the most likely successor
, and are either licensed for use or under consideration for licensing in several worldwide markets
, including within the European Union
, where certain neonicotinoids (imidacloprid, clothianidin and thiamethoxam) are now banned from agricultural use outside of permanent greenhouse structures. There is an urgent need to pre-emptively evaluate the potential sub-lethal effects of sulfoximine-based pesticides on pollinators
, because such effects are rarely detected by standard ecotoxicological assessments, but can have major impacts at larger ecological scales
. Here we show that chronic exposure to the sulfoximine-based insecticide sulfoxaflor, at dosages consistent with potential post-spray field exposure, has severe sub-lethal effects on bumblebee (Bombus terrestris) colonies. Field-based colonies that were exposed to sulfoxaflor during the early growth phase produced significantly fewer workers than unexposed controls, and ultimately produced fewer reproductive offspring. Differences between the life-history trajectories of treated and control colonies first became apparent when individuals exposed as larvae began to emerge, suggesting that direct or indirect effects on a small cohort may have cumulative long-term consequences for colony fitness. Our results caution against the use of sulfoximines as a direct replacement for neonicotinoids. To avoid continuing cycles of novel pesticide release and removal, with concomitant impacts on the environment, a broad evidence base needs to be assessed prior to the development of policy and regulation.
Global concern over widely documented declines in pollinators
has led to the identification of anthropogenic stressors that, individually, are detrimental to bee populations
. Synergistic ...interactions between these stressors could substantially amplify the environmental effect of these stressors and could therefore have important implications for policy decisions that aim to improve the health of pollinators
. Here, to quantitatively assess the scale of this threat, we conducted a meta-analysis of 356 interaction effect sizes from 90 studies in which bees were exposed to combinations of agrochemicals, nutritional stressors and/or parasites. We found an overall synergistic effect between multiple stressors on bee mortality. Subgroup analysis of bee mortality revealed strong evidence for synergy when bees were exposed to multiple agrochemicals at field-realistic levels, but interactions were not greater than additive expectations when bees were exposed to parasites and/or nutritional stressors. All interactive effects on proxies of fitness, behaviour, parasite load and immune responses were either additive or antagonistic; therefore, the potential mechanisms that drive the observed synergistic interactions for bee mortality remain unclear. Environmental risk assessment schemes that assume additive effects of the risk of agrochemical exposure may underestimate the interactive effect of anthropogenic stressors on bee mortality and will fail to protect the pollinators that provide a key ecosystem service that underpins sustainable agriculture.
Pollinators, particularly wild bees, are suffering declines across the globe, and pesticides are thought to be drivers of these declines. Research into, and regulation of pesticides has focused on ...the active ingredients, and their impact on bee health. In contrast, the additional components in pesticide formulations have been overlooked as potential threats. By testing an acute oral dose of the fungicide product Amistar, and equivalent doses of each individual co-formulant, we were able to measure the toxicity of the formulation and identify the ingredient responsible. We found that a co-formulant, alcohol ethoxylates, caused a range of damage to bumble bee health. Exposure to alcohol ethoxylates caused 30% mortality and a range of sublethal effects. Alcohol ethoxylates treated bees consumed half as much sucrose as negative control bees over the course of the experiment and lost weight. Alcohol ethoxylates treated bees had significant melanisation of their midguts, evidence of gut damage. We suggest that this gut damage explains the reduction in appetite, weight loss and mortality, with bees dying from energy depletion. Our results demonstrate that sublethal impacts of pesticide formulations need to be considered during regulatory consideration, and that co-formulants can be more toxic than active ingredients.
Interactions involving several parasite species (multi-parasitized hosts) or several host species (multi-host parasites) are the rule in nature. Only a few studies have investigated these realistic, ...but complex, situations from an evolutionary perspective. Consequently, their impact on the evolution of parasite virulence and transmission remains poorly understood. The mechanisms by which multiple infections may influence virulence and transmission include the dynamics of intrahost competition, mediation by the host immune system and an increase in parasite genetic recombination. Theoretical investigations have yet to be conducted to determine which of these mechanisms are likely to be key factors in the evolution of virulence and transmission. In contrast, the relationship between multi-host parasites and parasite virulence and transmission has seen some theoretical investigation. The key factors in these models are the trade-off between virulence across different host species, variation in host species quality and patterns of transmission. The empirical studies on multi-host parasites suggest that interspecies transmission plays a central role in the evolution of virulence, but as yet no complete picture of the phenomena involved is available. Ultimately, determining how complex host–parasite interactions impact the evolution of host–parasite relationships will require the development of cross-disciplinary studies linking the ecology of quantitative networks with the evolution of virulence.
Bumble bees are a group of pollinators that are both ecologically and economically important and declining worldwide. Numerous mechanisms could be behind this decline, and the spread of parasites ...from commercial colonies into wild populations has been implicated recently in North America. Commercial breeding may lead to declines because commercial colonies may have high parasite loads, which can lead to colonization of native bumble bee populations; commercial rearing may allow higher parasite virulence to evolve; and global movement of commercial colonies may disrupt spatial patterns in local adaptation between hosts and parasites. We assessed parasite virulence, transmission mode, and infectivity. Microparasites and so-called honey bee viruses may pose the greatest threat to native bumble bee populations because certain risk factors are present; for example, the probability of horizontal transmission of the trypanosome parasite Crithidia bombi is high. The microsporidian parasite Nosema bombi may play a role in declines of bumble bees in the United States. Preliminary indications that C. bombi and the neogregarine Apicystis bombi may not be native in parts of South America. We suggest that the development of molecular screening protocols, thorough sanitation efforts, and cooperation among nongovernmental organizations, governments, and commercial breeders might immediately mitigate these threats. Los abejorros son un grupo de polinizadores que son importantes tanto ecológica como económicamente y están declinando en todo el mundo. Hay numerosos mecanismos que pudieran estar detrás de esta declinación, y en Norte América recientemente se ha involucrado a la extensión de parásitos de colonias comerciales hacia poblaciones silvestres. La crianza comercial puede causar declinaciones porque las colonias comerciales pueden tener cargas altas de parásitos, lo que puede llevar a la colonización de poblaciones de abejorros nativos; la crianza comercial puede permitir que evolucione una mayor virulencia de parásitos; y el movimiento global de colonias comerciales puede alterar patrones espaciales en la adaptación local entre huéspedes y parásitos. Evaluamos la virulencia de parásitos, el modo de transmisión y la infectividad. Los microparásitos y los llamados virus de abejas pueden ser la mayor amenaza para las poblaciones de abejorros nativos debido a la presencia de ciertos factores de riesgo; por ejemplo, la probabilidad de transmisión horizontal del tripanosoma parásito Crithidia bombi es alta. El microesporido parásito Nosema bombi puede jugar un papel en las declinaciones de abejorros en los Estados Unidos. Indicaciones preliminares de que C. bombi y el neogregarino Apicystis bombi posiblemente no son nativos en partes de América del Sur. Sugerimos que el desarrollo de protocolos de análisis molecular, esfuerzos de sanidad minuciosos y la cooperación entre organizaciones no gubernamentales, gobiernos y criadores comerciales puede mitigar estas amenazas inmediatamente.
Bumblebees are essential pollinators of crops and wild plants, but are in decline across the globe. Neonicotinoid pesticides have been implicated as a potential driver of these declines, but most of ...our evidence base comes from studies of a single species. There is an urgent need to understand whether such results can be generalized across a range of species. Here, we present results of a laboratory experiment testing the impacts of field-relevant doses (1.87–5.32 ppb) of the neonicotinoid thiamethoxam on spring-caught wild queens of four bumblebee species: Bombus terrestris, B. lucorum, B. pratorum and B. pascuorum. Two weeks of exposure to the higher concentration of thiamethoxam caused a reduction in feeding in two out of four species, suggesting species-specific anti-feedant, repellency or toxicity effects. The higher level of thiamethoxam exposure resulted in a reduction in the average length of terminal oocytes in queens of all four species. In addition to providing the first evidence for general effects of neonicotinoids on ovary development in multiple species of wild bumblebee queens, the discovery of species-specific effects on feeding has significant implications for current practices and policy for pesticide risk assessment and use.
Summary Background Animals can act as a reservoir and source for the emergence of novel meticillin-resistant Staphylococcus aureus (MRSA) clones in human beings. Here, we report the discovery of a ...strain of S aureus (LGA251) isolated from bulk milk that was phenotypically resistant to meticillin but tested negative for the mecA gene and a preliminary investigation of the extent to which such strains are present in bovine and human populations. Methods Isolates of bovine MRSA were obtained from the Veterinary Laboratories Agency in the UK, and isolates of human MRSA were obtained from diagnostic or reference laboratories (two in the UK and one in Denmark). From these collections, we searched for mecA PCR-negative bovine and human S aureus isolates showing phenotypic meticillin resistance. We used whole-genome sequencing to establish the genetic basis for the observed antibiotic resistance. Findings A divergent mecA homologue ( mecALGA251 ) was discovered in the LGA251 genome located in a novel staphylococcal cassette chromosome mec element, designated type-XI SCC mec . The mecALGA251 was 70% identical to S aureus mecA homologues and was initially detected in 15 S aureus isolates from dairy cattle in England. These isolates were from three different multilocus sequence type lineages (CC130, CC705, and ST425); spa type t843 (associated with CC130) was identified in 60% of bovine isolates. When human mecA -negative MRSA isolates were tested, the mecALGA251 homologue was identified in 12 of 16 isolates from Scotland, 15 of 26 from England, and 24 of 32 from Denmark. As in cows, t843 was the most common spa type detected in human beings. Interpretation Although routine culture and antimicrobial susceptibility testing will identify S aureus isolates with this novel mecA homologue as meticillin resistant, present confirmatory methods will not identify them as MRSA. New diagnostic guidelines for the detection of MRSA should consider the inclusion of tests for mecALGA251. Funding Department for Environment, Food and Rural Affairs, Higher Education Funding Council for England, Isaac Newton Trust (University of Cambridge), and the Wellcome Trust.
Emerging infectious diseases (EIDs) have contributed significantly to the current biodiversity crisis, leading to widespread epidemics and population loss. Owing to genetic variation in pathogen ...virulence, a complete understanding of species decline requires the accurate identification and characterization of EIDs. We explore this issue in the Western honeybee, where increasing mortality of populations in the Northern Hemisphere has caused major concern. Specifically, we investigate the importance of genetic identity of the main suspect in mortality, deformed wing virus (DWV), in driving honeybee loss. Using laboratory experiments and a systematic field survey, we demonstrate that an emerging DWV genotype (DWV-B) is more virulent than the established DWV genotype (DWV-A) and is widespread in the landscape. Furthermore, we show in a simple model that colonies infected with DWV-B collapse sooner than colonies infected with DWV-A. We also identify potential for rapid DWV evolution by revealing extensive genome-wide recombination in vivo. The emergence of DWV-B in naive honeybee populations, including via recombination with DWV-A, could be of significant ecological and economic importance. Our findings emphasize that knowledge of pathogen genetic identity and diversity is critical to understanding drivers of species decline.
1. Most insecticides are insect neurotoxins. Evidence is emerging that sublethal doses of these neurotoxins are affecting the learning and memory of both wild and managed bee colonies, exacerbating ...the negative effects of pesticide exposure and reducing individual foraging efficiency. 2. Variation in methodologies and interpretation of results across studies has precluded the quantitative evaluation of these impacts that is needed to make recommendations for policy change. It is not clear whether robust effects occur under acute exposure regimes (often argued to be more field-realistic than the chronic regimes upon which many studies are based), for field-realistic dosages, and for pesticides other than neonicotinoids. 3. Here we use meta-analysis to examine the impact of pesticides on bee performance in proboscis extension-based learning assays, the paradigm most commonly used to assess learning and memory in bees. We draw together 104 (learning) and 167 (memory) estimated effect sizes across a diverse range of studies. 4. We detected significant negative effects of pesticides on learning and memory (i) at field realistic dosages, (ii) under both chronic and acute application, and (iii) for both neonicotinoid and non-neonicotinoid pesticides groups. 5. We also expose key gaps in the literature that include a critical lack of studies on non-Apis bees, on larval exposure (potentially one of the major exposure routes), and on performance in alternative learning paradigms. 6. Policy implications. Procedures for the registration of new pesticides within EU member states now typically require assessment of risks to pollinators if potential target crops are attractive to bees. However, our results provide robust quantitative evidence for subtle, sublethal effects, the consequences of which are unlikely to be detected within small-scale prelicensing laboratory or field trials, but can be critical when pesticides are used at a landscape scale. Our findings highlight the need for long-term postlicensing environmental safety monitoring as a requirement within licensing policy for plant protection products.
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 (
) 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.
PDF
